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Effects of short photoperiod on cashmere growth, hormone concentrations and hair follicle development-related gene expression in cashmere goats

Effects of short photoperiod on cashmere growth, hormone concentrations and hair follicle... JOURNAL OF APPLIED ANIMAL RESEARCH 2023, VOL. 51, NO. 1, 52–61 https://doi.org/10.1080/09712119.2022.2153853 Effects of short photoperiod on cashmere growth, hormone concentrations and hair follicle development-related gene expression in cashmere goats a a a a a a b a Junda Li , Guangjie Tian , Xingtao Wang , Hongyu Tang , Yuyang Liu , Hongran Guo , Chunxin Wang , Yulin Chen and Yuxin Yang a b College of Animal Science and Technology, Northwest A&F University, Yangling, People’s Republic of China; Jilin Academy of Agriculture Sciences, Gongzhuling, People’s Republic of China ABSTRACT ARTICLE HISTORY Received 16 June 2022 Shanbei White Cashmere goat is a typical goat species, the growth of cashmere is affected by Accepted 27 November 2022 photoperiod. To further investigate the effects of short photoperiod treatment on cashmere growth, hormone concentrations and hair follicle development-related gene expression in cashmere goats, KEYWORDS twenty Shannbei white cashmere goats were selected and randomly divided into long-day Cashmere goat; photoperiod; photoperiod treatment group and short-day photoperiod treatment group. The results revealed the hair follicles; hormone; gene cashmere on short-day photoperiod treatment began to develop earlier, and its length and growth rate increased dramatically (P < 0.05). The short-day photoperiod treatment increased the concentration of serum Melatonin, reduced the concentration of serum prolactin, decreased the expression of estrogen receptor alpha and raised the expression of hair follicle development-related genes [catenin beta-1, Bone morphogenetic protein 2, Fibroblast growth factor 5 and platelet-derived growth factor subunit A] (P < 0.05), thereby accelerating the reconstruction of the secondary follicle, increasing the density of the secondary follicle (P < 0.05) and triggering the growth of cashmere goats. The present study provides new insights into the dynamic changes in cashmere growth, hormone concentrations and hair follicle development-related gene expression in cashmere goats under short photoperiod, and is expected to be useful for future studies on intensive feeding research. Introduction (Yang et al. 2019). Studies have pointed out that thyroid hor- Cashmere goats have primary hair follicles (PHFs) and second- mones and 17β-estradiol (E2) also are involved with the ary hair follicles (SHFs), which are two different types of skin fol- growth of cashmere (Rhind and McMillen 1995; Movérare licles (Zhang et al. 2020). SHFs evolved into cashmere, while et al. 2002). These hormones interact with each other. MT PHFs produced coarse hair (Ansari-Renani et al. 2011). Cash- induces the secretion of prolactin, which causes hair follicles mere is a crucial raw material for the textile industry in the to enter the anagen phase (Nixon et al. 1993; Foitzik et al. world with a substantial economic value (Liu et al. 2012). 2006; Plikus et al. 2008). The transformation of anagen, The SHFs of cashmere goats are clearly periodic, requiring catagen, and telogen phases were regulated by some specific passage through the anagen, catagen and telogen phases (Rile pathways (Millar 2002; Blanpain and Fuchs 2006). The Wnt/β- et al. 2018). The periodicity of SHFs in cashmere goats is directly catenin signalling pathway is the primary regulator of epider- to the photoperiod. The reduction of daylight encouraged the mal and mesenchymal cell differentiation (Andl et al. 2002). development and manufacturing of cashmere (Zhang et al. 2019). β-catenin (catenin beta-1) is a crucial downstream component Changes in photoperiod influence the growth of cashmere of the canonical Wnt signalling pathway that binds to insulin- by modulating hormones. The light causes the pineal gland like growth factor 1 (IGF-1) to create transcription factors that to secrete melatonin (MT) by transmitting nerve impulses regulate the growth and development of hair follicles in through the retina to the superior chiasmal nucleus, then the animals. Bone morphogenetic protein (BMP) is a growth and paraventricular nucleus, and lastly the pineal gland (Cassone differentiation agent that stimulates bone production (Myllylä 1990). MT is essential to the growth of cashmere. Welch R et al. 2014). The ratio of BMP to β-catenin activity controls found that injecting MT to goats increased cashmere pro- the direction of hair follicle stem cell development (Plikus duction in September (Welch et al. 1990). Implantation of mel- et al. 2008; Kandyba et al. 2013). Bone morphogenetic atonin from July to September improved cashmere production protein 2 (BMP2) and bone morphogenetic protein 4 (BMP4) (Klören and Norton 1995). MT implantation significantly pro- are the two most biologically active genes in the BMP family, longs the growth phase of cashmere in the winter solstice which primarily influence the periodic growth and develop- (Cong et al. 2011). Recent research indicates that melatonin ment of hair follicles (Bai W et al. 2016). Platelet-derived stimulated Cashmere growth by boosting antioxidant levels growth factor subunit A (PDGFA) is expressed in epidermal CONTACT Yuxin Yang yangyuxin2002@126.com College of Animal Science and Technology, Northwest A&F University, Yangling, Shaanxi 712100, People’s Republic of China © 2023 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, dis- tribution, and reproduction in any medium, provided the original work is properly cited. JOURNAL OF APPLIED ANIMAL RESEARCH 53 and follicular epithelial cells, promotes the formation of dermal goats were exposed to photoperiod treatment between 15 papilla, stromal sheath, and dermal fibroblasts, IGF-1 treatment May 2020 and 15 October 2020 (153 days in total). The can up-regulate the expression of PDGFA, inhibit apoptosis, sampling period lasted from 15 May 2020 to 15 May 2021 promote hair follicle growth, and maintain hair follicles in the (365 days in total). anagen phase (Ahn et al. 2012). However, the pattern of hair regeneration varies among different species (Plikus et al. Cashmere collection 2011), with the majority of these studies focusing on humans and other animals. There are few studies relating the short- On May 15, a 10-by-10-centimeter region on the right side of day photoperiod treatment to the cashmere growth of goats, each goat was sheared to the skin level. Fibre samples from particularly the Shanbei White Cashmere goat. Therefore, it is the shorn area were clipped at skin level using stainless steel necessary to evaluate the association between the short-day clippers on 21 July and 21 August. Each clipping was obtained photoperiod treatment and cashmere growth in cashmere adjacent to the location of the last shearing but was always dis- goats. In this context, We hypothesized that the short-day tinct from any previously sampling location. A 30 mm patch of photoperiod treatment could affect the Shanbei White Cash- cashmere sample on the left scapular region of each goat was mere goat’s cashmere development, and the aim of this obtained at the beginning of harvest in the following April. study was to compare the cashmere growth, hormone concen- Samples were separated into cashmere fibre and guard hair trations and hair follicle development-related gene expression samples. Then, the cashmere fibre samples were stored in of cashmere goats under short-day photoperiod and natural sealed polythene bags at room temperature for fibre character- conditions, and to determine the effect of short-day light on istic analyses. Cashmere samples were collected annually at the the cashmere growth of the Shanbei White Cashmere goat end of April by combing or shearing and weighed using an by comparing these differences. This research will be of great electronic scale (CP214; OHAUS, USA). use for farming cashmere goat in places with short photo- periods and enhancing cashmere production through suitable light regulation. Cashmere measurement The cashmere fibre samples were soaked in carbon tetrachloride detergent solution overnight, rinsed thoroughly washed with Materials and methods deionized water and dried at 80°C. A total of 100 fibres were ran- Animals domly chosen from each sampling date of each goat to measure the stretched length of the cashmere using a steel ruler to calcu- This study was conducted from 15 May 2020 to 15 May 2021 at late the amount of cashmere growth, while 200 fibres were ran- the Shaanbei White Cashmere Goat Farm in Yulin, Shaanxi pro- ′ ′ domly selected for the diameter measurement using an optical vince, China (latitude N37°38 , longitude E109°12 ; altitude: fibre diameter analyzer (FZ-002; SRI, China). 1498 m). Randomly selected 20 empty pregnant ewes from 130 healthy Shaanbei white cashmere goats aged 2.5 years old, similar in weight and body condition, and divided evenly Hair follicle density measurement between the treatment group and the control group. The use of animals and all experimental protocols (protocol number: From the body side of the goats, approximately 1 cm of skin 100403) were authorized by the Institutional Animal Care and tissues was taken, placed in Sample Protector (Takara, Dalian, Use Committee of Northwest A&F University (Yangling, China) and frozen at −80°C. After drying, the skin tissues Shaanxi, China, Approval ID: 2014ZX08008-002). were trimmed according to the cross-section, dehydrated by gradient ethanol, cleaned with xylene, embedded in paraffin, stained with HE, sealed with neutral gum and observed. Photoperiodic manipulations Using digital microphotography (KEYENCE, Japan), The number of primary and secondary hair follicles in 10 complete After a two-week acclimation period on a long-day photo- hair follicles was recorded. ImageJ 1.60 image processing soft- period, ten female Shanbei White Cashmere goats (2.5 years ware was utilized to calculate the density of PHFs and SHFs in old with an initial body weight of 34.12 ± 1.54 kg) were the skin area. The ratio of PHFs and SHFs was calculated. placed into short-day photoperiod treatment conditions (Receive light from 9:30 am to 16:30 pm, 7 h of light per day) as the treatment group, and they were housed in a dark Blood sampling environment for the remainder of the time. The illumination was controlled at approximately 0.1 lux (Illuminance in the Blood samples were collected from a jugular vein using 5 mL dark) by closing the doors and using shade cloth to avoid sun- EDTA-coated vacutainer tubes (KANGJIAN, China) to examine light. As the control group, 10 additional goats were housed in the effect of photoperiod treatment on hormone levels and an identical shed with long-day photoperiod (Natural photo- hormone receptor gene expression in Shaanbei cashmere period, 12–13.5 h of light per day) conditions. All goats were goats. Blood was drawn on the 15th of each month at 9:30 fed and allowed to drink from 9:30 am to 16:30 pm daily . am Blood samples were allowed to stand at 37°C for 30 min These goats were administered to identical feeding and man- before being centrifuged at 3 000 r / min for 15 min. The agement environmental conditions, and the shed was routinely upper serum samples were collected and stored at −20°C for sanitized and poop removed. These Shanbei White Cashmere further analysis. 54 J. LI ET AL. Hormone assay Statistical analysis Serum melatonin concentrations were measured using a The data were done using Statistical Package for the Social commercial radioimmunoassay kit (HY 10177). The inter Sciences (SPSS) ver. 20.0 (SPSS Inc., Chicago, IL, USA). The and intra-assay coefficients of variation (CVs) were 14% and Shapiro–Wilk test was used to examine the data’s normality. Stu- 8.3%, respectively, while the sensitivity of the assay was 1.0 dent’s t-test was used to examine differences between groups, pg/ml. Serum prolactin concentrations were assessed using and P values less than 0.05 were considered statistically signifi- a I-prolactin radioimmunoassay kit (HY-10026), and inter cant. Results were presented as mean ± standard error (SE). and intra-assay CVs were 10% and 5%, respectively. The sen- sitivity of the assay was 1.0 ng/ml. All commercial kits were Results provided by SINO-UK Institute of Biological Technology (Beijing, China). Cashmere growth, fibre quality and hair follicle density The cashmere treated with short-day photoperiod treatment began to develop earlier, and its length increased significantly from June to July and September to April the following year (P Quantitative real-time polymerase chain reaction (qRT- < 0.05; Figure 1A). In June and July, the cashmere growth rate PCR) increased significantly (P < 0.05; Figure 1B). The effect of short-day photoperiod treatment on the weight of cashmere According to the manufacturer’s instructions, total RNA was fluff mixes and cashmere fibre diameter was insignificant (P > extracted from skin tissues using the Eastep® Super Total RNA 0.05; Table 2). The cashmere fibre length of the treatment Extraction Kit (Promega, Shanghai, China). The concentration group rose by 1.25 cm (P < 0.05), although the cashmere and quality of the extracted total RNA were assessed with the weight did not differ substantially. (P > 0.05; Table 2). NanoDrop spectrophotometer (Bio-Rad, Benicia, USA). Comp- Compared to the long-day photoperiod treatment, the lementary DNAs (cDNAs) were obtained from the reverse tran- short-day photoperiod treatment significantly decreased the scription of RNA with oligo (dT) primer using M-MLV reverse primary hair follicle density in September (P < 0.05; Table 3), transcriptase kit (TaKaRa, Dalian, China). qRT-PCR was per- and increased the secondary hair follicle density in June and formed in triplicate on a Bio-Rad IQ5 Real-Time PCR system July (P < 0.05; Table 3). April had the lowest ratio of secondary with a final volume of 25 μl containing 12.5 μl 2×SYBR® TM to primary follicle density (S:P). In July and September, short- Premix Ex Taq II (TaKaRa, Dalian, China), 1 μl of forward or day photoperiod treatment significantly enhanced the S:P reverse primer (10 μmol/L), 2 μl diluted template cDNA and ratio (P < 0.05; Table 3). 8.5 μl ddH O. The reaction conditions were carried out in accordance with the manufacturer’s guidelines. Three technical replicates were allocated to each sample, and the average Ct Serum hormone concentration value was determined. Using succinate dehydrogenase complex flavoprotein subunit A (SDHA) as the reference gene In June, July and September, Short-day photoperiod treatment (Bai et al. 2014), the 2-ΔΔCt technique was used to calculate significantly raised MT concentrations (P < 0.05; Figure 2A). In the relative expression of each gene. All sequences of primers the short-day photoperiod treatment group, the cyclical fluctu- are shown in Table 1. ations of MT concentrations fluctuated differently than in the Table 1. Primer sequences for quantitative real-time polymerase chain reaction (PCR). Product length Gene GenBank ID Full gene name Primer sequence (bp) Ta (1°C) SDHA XM_018065656.1 Succinate dehydrogenase complex, subunit A F: AGCACTGGAGGAAGCACAC 105 53 R: CACAGTCGGTCTCGTTCAA TRβ XM_005698927.2 Thyroid hormone receptor beta F: ACTCTACGAAGCACACCCAG 208 55 R: GTCCGAGTCCCTGCTTTTCA TRα XM_018065021.1 Thyroid hormone receptor alpha F: GAATGGAACAGAAGCCAAGC 117 57 R: TGCTGGTTTTCAGGGAACAT PRLR NM_001285669.1 Prolactin receptor F: TGCAGCATCTAGAGTGGTTTTC 125 57 R: AGGTGAACGTTTCCTTTCCA ERα XM_013966607.1 Estrogen receptor alpha F: CGGTGGATGTGGTCCTTCTCT 234 61 R: AGGGAAGCTCCTATTTGCTCC ERβ NM_001285688.1 Estrogen receptor beta F: GCTAACCTGCTGATGCTCCTGTCTC 204 65 R: GCCCTCTTTGCTCTCACTGTCCTC RORα NM_001285652.1 Receptor alpha F: TGTGCTTCTCAAAGCAGGTT 120 56 R: GATTTGAAGACATCGGGGCT β-catenin XM_018066894.1 Catenin beta-1 F: GCTGATTTGATGGAGCTGGA 182 58 R: TCATACAGGACTTGGGTGGT PDGFA XM_018040679.1 Platelet-derived growth factor subunit A F: CAGTCAGATCCACAGCATCC 85 56 R: CAGACTGGTTTCCAAAGGCT BMP2 NM_001287564.1 Bone morphogenetic protein 2 F: AAGAGGCATGTGCGGATTAG 129 58 R: TTGCCGCTTTTCTCTTCTGT BMP4 NM_001285646.1 Bone morphogenetic protein 4 F: GCTCTACGTGGACTTCAGTG 126 53 R: TGGTTGGTTGAGTTGAGGTG Ta:annealing temperature. JOURNAL OF APPLIED ANIMAL RESEARCH 55 Short-day photoperiod treatment increased thyroxine 4 (T4) concentrations significantly in July, October and November (P < 0.05), but no significant difference in other months (Figure 2C). In the short-day photoperiod treatment group, blood E2 concentrations were substantially higher in June, August, January, February and March (P < 0.05; Figure 2D). Hormone receptor expression In the long-day photoperiod treatment group, retinoid-related orphan receptor alpha (RORα) expression was lower in August, October and February and greater in November, March and April. The expression of RORα was considerably up-regulated in June, October, December and February and significantly down-regulated in July, November, January, March and April in the short-day photoperiod treatment group (P < 0.05; Figure 3A), delaying the expression peak to December (Figure 3A). As shown in Figure 3, the expression of prolactin receptor (PRLR) in the long-day photoperiod treatment group increased from May until November, when it reached its initial peak, and then decreased. The short-day photoperiod treatment group showed similar patterns. With the short-day photoperiod treat- ment, PRLR expression was substantially higher in May, June, August, December, February and March (P < 0.05) and signifi- cantly lower in October and January (P < 0.05; Figure 3B). The expression of thyroid hormone receptor alpha (TRα)in the short-day photoperiod treatment group was significantly higher in June and August and significantly lower in July, Sep- tember, January, March and April (P < 0.05; Figure 3C). The expression of thyroid hormone receptor beta (TRβ)in the long-day photoperiod treatment group showed a trend of increasing volatility from May and peaked in March of the fol- lowing year. The short-day photoperiod treatment group Figure 1. Effects of short-day photoperiod treatment on growth length and advanced the expression peak of TRβ to February, significantly growth rate of Shaanbei white cashmere goats. (A) Cashmere growth length of up-regulated the expression of TRβ in August, October, Decem- Shaanbei white cashmere goats. * P < 0.05. (B) Cashmere growth rate of Shaanbei ber and February, and significantly down-regulated the white cashmere goats.Different letters means significant difference P < 0.05. Control: Long-day photoperiod treatment group; Treatment: Short-day photo- expression of TRβ in March (P < 0.05; Figure 3D). period treatment group. The expression of estrogen receptor alpha (ERα) in the long- day photoperiod treatment group increased from May, reached a peak in August and then dropped. Short-day photoperiod long-day photoperiod treatment group from May to August, treatment group significantly down-regulated the expression and MT concentrations kept at a high level from June to of ERα in July, August, January, March and April (P < 0.05). In October in the short-day photoperiod treatment group September and October, the concentrations of ERα were elev- (Figure 2A). ated in the short-day photoperiod group (P < 0.05). The peak The initial peak of prolactin (PRL) concentrations in serum of was postponed to October (Figure 3E). long-day photoperiod treatment group occurred in July, fol- In the long-day photoperiod treatment group, the lowed by the second peak in October. Short-day photoperiod expression of estrogen receptor beta (ERβ) was lowest in treatment significantly reduced PRL concentrations in June, October and highest in January. In the short-day photoperiod July and December (P < 0.05; Figure 2B) and altered the peri- treatment group, ERβ expression was significantly up-regulated odic fluctuation of PRL (Figure 2B). (P < 0.05) in June, August, October and March, and significantly down-regulated in July, February and April (P < 0.05; Figure 3F), with the peak occurring in August. Table 2. Effects of short-day photoperiod treatment on cashmere fibre quality of Shaanbei white cashmere goats. Data are expressed as mean ± standard error (SE). Items Control Treatment P-value Gene expression associated with hair follicle Fluff mixtures weight (g) 1153.35 ± 145.11 1228.16 ± 66.58 0.462 development Cashmere weight (g) 593.15 ± 51.04 692.49 ± 49.31 0.072 Cashmere fibre length (cm) 9.34 ± 0.46 10.59 ± 0.53 0.036 The expression of β-catenin in two groups increased gradually Cashmere fibre diameter (µm) 16.92 ± 0.98 17.15 ± 1.07 0.794 from May and reached the highest peak in November and then Note: Control: Long-day photoperiod treatment group. Treatment: Short-day photoperiod treatment group. decreased. From May to July, the expression of β-catenin and 56 J. LI ET AL. Table 3. Effects of short-day photoperiod treatment on hair follicle density of Shaanbei white cashmere goats. Data are expressed as mean ± standard error (SE). Month Group Primary follicle density (per mm-2) p value Secondary follicle density (per mm-2) p value S:P ratio p value May Control 3.34 ± 0.50 0.371 22.08 ± 2.29 0.088 6.75 ± 0.70 0.427 Treatment 2.75 ± 0.31 16.39 ± 1.86 6.03 ± 0.42 June Control 3.00 ± 0.31 0.195 22.04 ± 0.87 0.049 7.44 ± 0.50 0.869 Treatment 3.68 ± 0.30 27.56 ± 1.78 7.58 ± 0.66 July Control 3.06 ± 0.29 0.691 21.50 ± 0.63 0.002 7.15 ± 0.65 0.027 Treatment 3.19 ± 0.08 32.81 ± 1.32 10.33 ± 0.66 August Control 3.37 ± 0.18 0.140 19.94 ± 1.40 0.101 5.98 ± 0.67 0.072 Treatment 2.51 ± 0.43 22.95 ± 0.21 9.60 ± 1.34 September Control 3.52 ± 0.05 0.001 24.45 ± 2.19 0.387 6.93 ± 0.54 0.048 Treatment 2.61 ± 0.06 22.28 ± 0.44 8.62 ± 0.15 October Control 2.68 ± 0.21 0.990 20.00 ± 1.59 0.312 7.51 ± 0.64 0.276 Treatment 2.69 ± 0.12 17.92 ± 0.83 6.67 ± 0.16 November Control 2.53 ± 0.29 0.194 18.18 ± 1.35 0.054 7.30 ± 0.69 0.542 Treatment 3.02 ± 0.13 23.52 ± 1.44 7.77 ± 0.16 December Control 2.44 ± 0.25 0.182 17.48 ± 1.15 0.182 7.22 ± 0.31 0.952 Treatment 1.99 ± 0.12 14.51 ± 1.44 7.26 ± 0.47 January Control 2.27 ± 0.12 0.347 16.94 ± 0.29 0.134 7.51 ± 0.47 0.889 Treatment 2.05 ± 0.16 15.23 ± 0.89 7.44 ± 0.14 February Control 1.84 ± 0.24 0.186 18.95 ± 3.41 0.118 10.18 ± 0.43 0.744 Treatment 2.64 ± 0.44 27.11 ± 2.30 10.58 ± 1.05 March Control 3.12 ± 0.11 0.235 20.74 ± 1.02 0.574 6.68 ± 0.55 0.401 Treatment 2.89 ± 0.13 23.12 ± 3.75 8.05 ± 1.36 April Control 3.72 ± 0.55 0.171 15.21 ± 1.00 0.776 4.33 ± 0.82 0.247 Treatment 2.79 ± 0.04 15.72 ± 1.35 5.63 ± 0.50 Note: Control: Long-day photoperiod treatment group. Treatment: Short-day photoperiod treatment group. Platelet Derived Growth Factor Subunit A (PDGFA) was con- treatment, the first expression peak of PDGFA was observed siderably upregulated by Short-day photoperiod treatment (P in August, one month earlier than with long-day photoperiod < 0.05; Figure 4A; Figure 4B). With short-day photoperiod treatment (Figure 4B). Compared with the long-day Figure 2. Effects of short-day photoperiod treatment on related hormone concentrations of Shaanbei white cashmere goats. (A) Melatonin (MT). (B) Prolactin (PRL). (C) Thyroxine (T4). (D) Estradiol (E2). * P < 0.05. Control: Long-day photoperiod treatment group; Treatment: Short-day photoperiod treatment group. JOURNAL OF APPLIED ANIMAL RESEARCH 57 Figure 3. Effects of short-day photoperiod treatment on related hormone receptor expression of Shaanbei white cashmere goats. (A) Retinoid-related orphan receptor alpha (RORα).(B) Prolactin receptor (PRLR).(C) Thyroid hormone receptor alpha (TRα).(D) Thyroid hormone receptor beta (TRβ). (E) Estrogen receptor alpha (ERα). (F) Estrogen receptor beta (ERβ). * P < 0.05. Control: Long-day photoperiod treatment group; Treatment: Short-day photoperiod treatment group. Figure 4. Effects of short photoperiod treatment on the hair follicle development-related gene expression of Shaanbei white cashmere goats. (A) Catenin beta-1 (β- catenin). (B) Platelet-derived growth factor subunit A (PDGFA). (C) Bone morphogenetic protein 2 (BMP2). (D) Bone morphogenetic protein 4 (BMP4). * P < 0.05. Control: Long-day photoperiod treatment group; Treatment: Short-day photoperiod treatment group. 58 J. LI ET AL. photoperiod treatment, the short-day photoperiod treatment group. We hypothesize that short-day treatment could affect increased the expression of bone morphogenetic protein-2 the interaction between MT and RORα. But the relevant mech- considerably from June to August (P < 0.05; Figure 4C). Short- anism of action has not been elucidated and there are various day photoperiod treatment reduced the expression of bone controversies as to whether MT directly impacts RORα (Ma et al. morphogenetic protein-4 during July (P < 0.05; Figure 4D). 2021), so further research is required. Except for March, short-day photoperiod treatment dramati- Previous research indicates that PRL has an inhibitory effect cally raised the expression of Fibroblast growth factor 5 gene on hair cycle, with high concentrations promoting the termin- in all months (P < 0.05; Figure 4E). ation of cashmere growth (Kloren and Norton 1993; Dicks et al. 1994; Craven et al. 2001). This is consistent with the results of our study. During the early stage of cashmere growth, from Discussion May to August, PRL concentrations were considerably lower Length, diameter and yield are important traits of cashmere, in the short-day photoperiod treatment group than in the which determine the economic value of cashmere. Feral doe long-day photoperiod treatment group, Additionally, PRL and goats have seasonal characteristics, and the change of illumina- MT levels exhibited opposing tendencies simultaneously. MT tion time affects the growth rate, length and diameter of Aus- is able to reduce PRL secretion (Rose et al. 1985; Emesih et al. tralian cashmere goats (McDonald and Hoey 1987). The results 1993; Nixon et al. 1993; Dicks et al. 1995; Duan et al. 2017). of our investigation revealed that the short-day photoperiod By boosting MT concentrations to inhibit PRL levels in cash- treatment boosted cashmere length by 1.25 cm and cashmere mere’s early growth period, short-day photoperiod treatment output by 99.34 g, which increased by 16.75% year-on-year. may enhance the advanced growth of cashmere. PRL exerts Both hair follicle density and the S:P ratio are essential morpho- its biological effects via receptor binding (Morammazi et al. logical parameters of villus hair follicles, having high heritability 2016). During the anagen phase (August to December), high related to sheep wool production (Ansari-Renani et al. 2011). concentrations of PRL up-regulated PRLR expression, which Previous research has demonstrated that melatonin can stimu- peaked during the catagen (January to February) and telogen late the growth of hair follicles (Feng and Gun 2021). Embed- (March to April) phases, which supports the research findings ding MT in vitro induced cashmere growth in advance, of Nixon et al (Nixon et al. 2002). prolonged the growth of the cashmere and increased the T4 regulates the metabolism and growth of the body. Its length of the cashmere (Welch et al. 1990; Cong et al. 2011). secretion is related to the physiological state of an individual. In this study, short-day photoperiod treatment reduced sun- The T4 concentrations of Australian cashmere goats were shine hours in June, July and September, and as melatonin pro- higher in the summer than in the winter, although the seasonal duction is directly related to light, there was less melatonin variation was not obvious (Kloren et al. 1993). The findings of secretion during the day and more at night (Bedrosian et al. this study agree with previous reports. Short-day photoperiod 2013). Due to the prolonged darkness, the MT concentration treatment significantly increased the T4 concentrations in the of the short-day photoperiod treatment group was significantly short-day photoperiod group in July, October and November, higher than that of the long-day photoperiod treatment group but did not significantly change the T4 secretion trend. In in June, July and September, which advanced the reconstruc- addition, short-day photoperiod treatment had no significant tion of secondary hair follicles and stimulated the accelerated effect on their expression patterns. growth of cashmere. The research conducted by Chanda demonstrated that E2 MT has both membrane receptors (MT1, MT2 and MT3) and could promote suppression of the telogen to anagen transition. nuclear receptors (RORα, RORβ and RORγ) (Fischer et al. 2008; It induced hair follicles in the catagen phase to enter the Cutando et al. 2011). The expression of membrane receptor telogen phase and regulated the hair follicle cycle (Chanda was not detected in goat skin (Dicks et al. 1996). In addition, et al. 2000a). E2 increased gradually during the late catagen a prior study demonstrated that RORα was expressed in the phase of SHFs (December). The SHFs were transformed from secondary hair follicles of the hair shaft, inner root sheath, the anagen phase to catagen phase. In male mice, E2 regulated outer root sheath and medulla (Zhao et al. 2015). On the the vital movement of hair follicles by mediating the inhibition basis of these studies, we detected the relative expression of of telogen–anagen transition (Movérare et al. 2002). The RORα gene in the samples and found that the expression of catagen-promoting activities of E2 were mediated by Erα RORα in the long-day photoperiod treatment group peaked (Chanda et al. 2000b; Ohnemus et al. 2005). ERβ antagonized in November, but the short-day photoperiod treatment the mediated action of ERα and MT inhibited the expression delayed the peak expression to December. Melatonin affects of ERα (Ohnemus et al. 2005; Martinez-Campa et al. 2006). the transcriptional control of ROR (Karasek et al. 2003), and Our study demonstrated that short-day photoperiod treatment Fischer suggests that MT mediates the role of RORα in regulat- inhibited the expression of ERα between June and August, ing hair growth (Fischer et al. 2008). Therefore, we compared which is due to the increase of serum MT concentration and MT concentration and RORα expression, and found that in the up-regulation of expression of ERβ. These regulations atte- the long-day photoperiod treatment group, RORα expression nuated the inhibition of hair follicle growth by E2 and pro- and MT concentration appeared opposite peaks in October, moted the growth and development of hair follicles. February and November. The result confirmed the negative Wnt / β-catenin signalling pathway plays a key role in the correlation between MT concentration and RORα expression development of hair follicles. The expression of Wnt signalling (Wang et al. 2013). In June and January, however, contrasting can promote the development, occurrence and differentiation results emerged in the short-day photoperiod treatment of hair follicles (Andl et al. 2002; Fu and Hsu 2013). Low JOURNAL OF APPLIED ANIMAL RESEARCH 59 expression of β-catenin stimulates hair follicle stem cell differ- Disclosure statement entiation to epithelial and hair follicle sebaceous glands, No potential conflict of interest was reported by the author(s). while high expression of β-catenin induces hair follicle recon- struction (Silva-Vargas et al. 2005). Implantation of MT in vitro significantly up-regulated the expression of β-catenin gene in Funding Inner Mongolia cashmere goats (Liu et al. 2016). The present study found that short-day photoperiod treatment boosted This work was supported by Key Science and Technology Program of Inner Mongolia Autonomous Region [grant number 2021ZD0012]; China Agricul- β-catenin gene expression during the early anagen phase of ture Research System [grant number CARS-39-12]; Special Fund for Agro- the cashmere growth (May to July). scientific Research in the Public Interest [grant number 201303059]. The bone morphogenetic protein (BMP) signal pathway plays a crucial role in hair follicle morphogenesis and hair follicle cycling (Botchkarev and Kishimoto 2003). BMP signalling limits References hair follicle cell growth and maintains hair follicles in the telogen period (Millar 2002). Our research revealed that short- Ahn, S.-Y., Pi, L.-Q., Hwang, S.T., Lee, W.-S., 2012.Effect of IGF-I on hair growth is related to the anti-apoptotic effect of IGF-I and up-regulation day photoperiod treatment increased the expression of BMP2 of PDGF-A and PDGF-B. Ann Dermatol. 24, 26-31. doi:10.5021/ad.2012. gene during the early anagen phase, but had no effect on the 24.1.26 expression of BMP4 during the telogen and catagen phases. Andl, T., Reddy, S.T., Gaddapara, T., Millar, S.E., 2002. WNT signals are PDGF is a cell growth factor that inhibits apoptosis (Gruber required for the initiation of hair follicle development. Dev Cell 2, 643- et al. 2000). It is associated with hair follicle growth and angio- 653. doi:10.1016/S1534-5807(02)00167-3 Ansari-Renani, H., Ebadi, Z., Moradi, S., Baghershah, H., Ansari-Renani, M., genesis (Kamp et al. 2003). Insulin-like growth factor 1 (IGF-1) Ameli, S., 2011. Determination of hair follicle characteristics, density treatment up-regulated the expression of PDGFA and plate- and activity of Iranian cashmere goat breeds. Small Ruminant Res 95, let-derived growth factor subunit B (PDGFB), thereby inhibiting 128-132. doi:10.1016/j.smallrumres.2010.09.013 cell apoptosis. These regulations promote hair follicle growth Bai, W. L., Dang, Y. L., Wang, J. J., Yin, R. H., Wang, Z. Y., Zhu, Y. B., Cong, Y. Y., and maintain hair follicles in the anagen phase (Ahn et al. Xue, H. L., Deng, L., Guo, D., Wang, S. Q., Yang, S. H. 2016. Molecular characterization, expression and methylation status analysis of BMP4 2012; Pazzaglia et al. 2019). Our research demonstrated that gene in skin tissue of Liaoning cashmere goat during hair follicle short-day photoperiod treatment increased PDGFA gene cycle. Genetica, 144(4): 457-467. doi:10.1007/s10709-016-9914-1 expression significantly during the early anagen phase. Bai, W.L., Yin, R.H., Yin, R.L., Jiang, W.Q., Wang, J.J., Wang, Z.Y., Zhu, Y.B., Noggin is an inhibitor of BMP (Zimmerman et al. 1996). BMP Zhao, Z.H., Yang, R.J., Luo, G.B., He, J.B., 2014. Selection and validation is located downstream of Wnt /β-catenin (Suzuki et al. 2009). of suitable reference genes in skin tissue of Liaoning cashmere goat during hair follicle cycle. Livest Sci 161, 28–35. doi:10.1016/j.livsci.2013. High expression of β-catenin up-regulated noggin expression 12.031 (Plikus et al. 2008). PDGFA and SHH enhanced the expression Bedrosian, T.A., Herring, K.L., Walton, J.C., Fonken, L.K., Weil, Z.M., Nelson, of the noggin gene in dermal papilla cells. By upregulating R.J., 2013. Evidence for feedback control of pineal melatonin secretion. the expression of -catenin and PDGFA genes in anagen, Neurosci Lett 542, 123–125. doi:10.1016/j.neulet.2013.03.021 short-day photoperiod treatment suppressed the expression Blanpain, C., Fuchs, E., 2006. Epidermal stem cells of the skin. Annu Rev Cell Dev Biol. 22, 339-373. doi:10.1146/annurev.cellbio.22.010305.104357 of the BMP4 gene, hence encouraging hair follicle rebuilding. Botchkarev, V.A., Kishimoto, J., 2003. Molecular control of epithelial– It has been reported that human hair follicles cultured in vitro mesenchymal interactions during hair follicle cycling. J Investig and exposed to recombinant FGF5 enters into catagen phase Dermatol Symp Proc, pp. 46-55. doi:10.1046/j.1523-1747.2003.12171.x prematurely (Higgins et al. 2014). In the early stages of the Cassone, V.M., 1990.Effects of melatonin on vertebrate circadian systems. study, the serum FGF5 concentration and cashmere length of Trends Neurosci 13, 457-464. doi:10.1016/0166-2236(90)90099-V Chanda, S., Robinette, C.L., Couse, J.F., Smart, R.C., 2000a. 17beta-estradiol goats in the short-day photoperiod treatment group were signifi- and ICI-182780 regulate the hair follicle cycle in mice through an estro- cantly higher than those of the control group, suggesting that gen receptor-alpha pathway. Am J Physiol Endocrinol Metab 278, E202- the increase in serum FGF5 concentration lead to the catagen E210. doi:10.1152/ajpendo.2000.278.2.E202 phase of hair follicles, thus promoting cashmere growth. Chanda, S., Robinette, C.L., Couse, J.F., Smart, R.C., 2000b.17β-Estradiol and ICI-182780 regulate the hair follicle cycle in mice through an estrogen receptor-α pathway. Am J Physiol Endocrinol Metab 278, E202-E210. doi:10.1152/ajpendo.2000.278.2.E202 Conclusion Cong, Y., Deng, H., Feng, Y., Chen, Q., Sun, Y., 2011. Melatonin implantation from winter solstice could extend the cashmere growth phase effec- In summary, under the short-day photoperiod treatment, tively. Small Ruminant Res 99, 48-53. doi:10.1016/j.smallrumres.2011. primary hair follicle density dropped by 0.91 follicles/mm2 in 03.055 Craven, A.J., Ormandy, C.J., Robertson, F.G., Wilkins, R.J., Kelly, P.A., Nixon, A.J., September, secondary hair follicle density rose by 5.52 and 2 Pearson, A.J., 2001. 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Effects of short photoperiod on cashmere growth, hormone concentrations and hair follicle development-related gene expression in cashmere goats

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JOURNAL OF APPLIED ANIMAL RESEARCH 2023, VOL. 51, NO. 1, 52–61 https://doi.org/10.1080/09712119.2022.2153853 Effects of short photoperiod on cashmere growth, hormone concentrations and hair follicle development-related gene expression in cashmere goats a a a a a a b a Junda Li , Guangjie Tian , Xingtao Wang , Hongyu Tang , Yuyang Liu , Hongran Guo , Chunxin Wang , Yulin Chen and Yuxin Yang a b College of Animal Science and Technology, Northwest A&F University, Yangling, People’s Republic of China; Jilin Academy of Agriculture Sciences, Gongzhuling, People’s Republic of China ABSTRACT ARTICLE HISTORY Received 16 June 2022 Shanbei White Cashmere goat is a typical goat species, the growth of cashmere is affected by Accepted 27 November 2022 photoperiod. To further investigate the effects of short photoperiod treatment on cashmere growth, hormone concentrations and hair follicle development-related gene expression in cashmere goats, KEYWORDS twenty Shannbei white cashmere goats were selected and randomly divided into long-day Cashmere goat; photoperiod; photoperiod treatment group and short-day photoperiod treatment group. The results revealed the hair follicles; hormone; gene cashmere on short-day photoperiod treatment began to develop earlier, and its length and growth rate increased dramatically (P < 0.05). The short-day photoperiod treatment increased the concentration of serum Melatonin, reduced the concentration of serum prolactin, decreased the expression of estrogen receptor alpha and raised the expression of hair follicle development-related genes [catenin beta-1, Bone morphogenetic protein 2, Fibroblast growth factor 5 and platelet-derived growth factor subunit A] (P < 0.05), thereby accelerating the reconstruction of the secondary follicle, increasing the density of the secondary follicle (P < 0.05) and triggering the growth of cashmere goats. The present study provides new insights into the dynamic changes in cashmere growth, hormone concentrations and hair follicle development-related gene expression in cashmere goats under short photoperiod, and is expected to be useful for future studies on intensive feeding research. Introduction (Yang et al. 2019). Studies have pointed out that thyroid hor- Cashmere goats have primary hair follicles (PHFs) and second- mones and 17β-estradiol (E2) also are involved with the ary hair follicles (SHFs), which are two different types of skin fol- growth of cashmere (Rhind and McMillen 1995; Movérare licles (Zhang et al. 2020). SHFs evolved into cashmere, while et al. 2002). These hormones interact with each other. MT PHFs produced coarse hair (Ansari-Renani et al. 2011). Cash- induces the secretion of prolactin, which causes hair follicles mere is a crucial raw material for the textile industry in the to enter the anagen phase (Nixon et al. 1993; Foitzik et al. world with a substantial economic value (Liu et al. 2012). 2006; Plikus et al. 2008). The transformation of anagen, The SHFs of cashmere goats are clearly periodic, requiring catagen, and telogen phases were regulated by some specific passage through the anagen, catagen and telogen phases (Rile pathways (Millar 2002; Blanpain and Fuchs 2006). The Wnt/β- et al. 2018). The periodicity of SHFs in cashmere goats is directly catenin signalling pathway is the primary regulator of epider- to the photoperiod. The reduction of daylight encouraged the mal and mesenchymal cell differentiation (Andl et al. 2002). development and manufacturing of cashmere (Zhang et al. 2019). β-catenin (catenin beta-1) is a crucial downstream component Changes in photoperiod influence the growth of cashmere of the canonical Wnt signalling pathway that binds to insulin- by modulating hormones. The light causes the pineal gland like growth factor 1 (IGF-1) to create transcription factors that to secrete melatonin (MT) by transmitting nerve impulses regulate the growth and development of hair follicles in through the retina to the superior chiasmal nucleus, then the animals. Bone morphogenetic protein (BMP) is a growth and paraventricular nucleus, and lastly the pineal gland (Cassone differentiation agent that stimulates bone production (Myllylä 1990). MT is essential to the growth of cashmere. Welch R et al. 2014). The ratio of BMP to β-catenin activity controls found that injecting MT to goats increased cashmere pro- the direction of hair follicle stem cell development (Plikus duction in September (Welch et al. 1990). Implantation of mel- et al. 2008; Kandyba et al. 2013). Bone morphogenetic atonin from July to September improved cashmere production protein 2 (BMP2) and bone morphogenetic protein 4 (BMP4) (Klören and Norton 1995). MT implantation significantly pro- are the two most biologically active genes in the BMP family, longs the growth phase of cashmere in the winter solstice which primarily influence the periodic growth and develop- (Cong et al. 2011). Recent research indicates that melatonin ment of hair follicles (Bai W et al. 2016). Platelet-derived stimulated Cashmere growth by boosting antioxidant levels growth factor subunit A (PDGFA) is expressed in epidermal CONTACT Yuxin Yang yangyuxin2002@126.com College of Animal Science and Technology, Northwest A&F University, Yangling, Shaanxi 712100, People’s Republic of China © 2023 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, dis- tribution, and reproduction in any medium, provided the original work is properly cited. JOURNAL OF APPLIED ANIMAL RESEARCH 53 and follicular epithelial cells, promotes the formation of dermal goats were exposed to photoperiod treatment between 15 papilla, stromal sheath, and dermal fibroblasts, IGF-1 treatment May 2020 and 15 October 2020 (153 days in total). The can up-regulate the expression of PDGFA, inhibit apoptosis, sampling period lasted from 15 May 2020 to 15 May 2021 promote hair follicle growth, and maintain hair follicles in the (365 days in total). anagen phase (Ahn et al. 2012). However, the pattern of hair regeneration varies among different species (Plikus et al. Cashmere collection 2011), with the majority of these studies focusing on humans and other animals. There are few studies relating the short- On May 15, a 10-by-10-centimeter region on the right side of day photoperiod treatment to the cashmere growth of goats, each goat was sheared to the skin level. Fibre samples from particularly the Shanbei White Cashmere goat. Therefore, it is the shorn area were clipped at skin level using stainless steel necessary to evaluate the association between the short-day clippers on 21 July and 21 August. Each clipping was obtained photoperiod treatment and cashmere growth in cashmere adjacent to the location of the last shearing but was always dis- goats. In this context, We hypothesized that the short-day tinct from any previously sampling location. A 30 mm patch of photoperiod treatment could affect the Shanbei White Cash- cashmere sample on the left scapular region of each goat was mere goat’s cashmere development, and the aim of this obtained at the beginning of harvest in the following April. study was to compare the cashmere growth, hormone concen- Samples were separated into cashmere fibre and guard hair trations and hair follicle development-related gene expression samples. Then, the cashmere fibre samples were stored in of cashmere goats under short-day photoperiod and natural sealed polythene bags at room temperature for fibre character- conditions, and to determine the effect of short-day light on istic analyses. Cashmere samples were collected annually at the the cashmere growth of the Shanbei White Cashmere goat end of April by combing or shearing and weighed using an by comparing these differences. This research will be of great electronic scale (CP214; OHAUS, USA). use for farming cashmere goat in places with short photo- periods and enhancing cashmere production through suitable light regulation. Cashmere measurement The cashmere fibre samples were soaked in carbon tetrachloride detergent solution overnight, rinsed thoroughly washed with Materials and methods deionized water and dried at 80°C. A total of 100 fibres were ran- Animals domly chosen from each sampling date of each goat to measure the stretched length of the cashmere using a steel ruler to calcu- This study was conducted from 15 May 2020 to 15 May 2021 at late the amount of cashmere growth, while 200 fibres were ran- the Shaanbei White Cashmere Goat Farm in Yulin, Shaanxi pro- ′ ′ domly selected for the diameter measurement using an optical vince, China (latitude N37°38 , longitude E109°12 ; altitude: fibre diameter analyzer (FZ-002; SRI, China). 1498 m). Randomly selected 20 empty pregnant ewes from 130 healthy Shaanbei white cashmere goats aged 2.5 years old, similar in weight and body condition, and divided evenly Hair follicle density measurement between the treatment group and the control group. The use of animals and all experimental protocols (protocol number: From the body side of the goats, approximately 1 cm of skin 100403) were authorized by the Institutional Animal Care and tissues was taken, placed in Sample Protector (Takara, Dalian, Use Committee of Northwest A&F University (Yangling, China) and frozen at −80°C. After drying, the skin tissues Shaanxi, China, Approval ID: 2014ZX08008-002). were trimmed according to the cross-section, dehydrated by gradient ethanol, cleaned with xylene, embedded in paraffin, stained with HE, sealed with neutral gum and observed. Photoperiodic manipulations Using digital microphotography (KEYENCE, Japan), The number of primary and secondary hair follicles in 10 complete After a two-week acclimation period on a long-day photo- hair follicles was recorded. ImageJ 1.60 image processing soft- period, ten female Shanbei White Cashmere goats (2.5 years ware was utilized to calculate the density of PHFs and SHFs in old with an initial body weight of 34.12 ± 1.54 kg) were the skin area. The ratio of PHFs and SHFs was calculated. placed into short-day photoperiod treatment conditions (Receive light from 9:30 am to 16:30 pm, 7 h of light per day) as the treatment group, and they were housed in a dark Blood sampling environment for the remainder of the time. The illumination was controlled at approximately 0.1 lux (Illuminance in the Blood samples were collected from a jugular vein using 5 mL dark) by closing the doors and using shade cloth to avoid sun- EDTA-coated vacutainer tubes (KANGJIAN, China) to examine light. As the control group, 10 additional goats were housed in the effect of photoperiod treatment on hormone levels and an identical shed with long-day photoperiod (Natural photo- hormone receptor gene expression in Shaanbei cashmere period, 12–13.5 h of light per day) conditions. All goats were goats. Blood was drawn on the 15th of each month at 9:30 fed and allowed to drink from 9:30 am to 16:30 pm daily . am Blood samples were allowed to stand at 37°C for 30 min These goats were administered to identical feeding and man- before being centrifuged at 3 000 r / min for 15 min. The agement environmental conditions, and the shed was routinely upper serum samples were collected and stored at −20°C for sanitized and poop removed. These Shanbei White Cashmere further analysis. 54 J. LI ET AL. Hormone assay Statistical analysis Serum melatonin concentrations were measured using a The data were done using Statistical Package for the Social commercial radioimmunoassay kit (HY 10177). The inter Sciences (SPSS) ver. 20.0 (SPSS Inc., Chicago, IL, USA). The and intra-assay coefficients of variation (CVs) were 14% and Shapiro–Wilk test was used to examine the data’s normality. Stu- 8.3%, respectively, while the sensitivity of the assay was 1.0 dent’s t-test was used to examine differences between groups, pg/ml. Serum prolactin concentrations were assessed using and P values less than 0.05 were considered statistically signifi- a I-prolactin radioimmunoassay kit (HY-10026), and inter cant. Results were presented as mean ± standard error (SE). and intra-assay CVs were 10% and 5%, respectively. The sen- sitivity of the assay was 1.0 ng/ml. All commercial kits were Results provided by SINO-UK Institute of Biological Technology (Beijing, China). Cashmere growth, fibre quality and hair follicle density The cashmere treated with short-day photoperiod treatment began to develop earlier, and its length increased significantly from June to July and September to April the following year (P Quantitative real-time polymerase chain reaction (qRT- < 0.05; Figure 1A). In June and July, the cashmere growth rate PCR) increased significantly (P < 0.05; Figure 1B). The effect of short-day photoperiod treatment on the weight of cashmere According to the manufacturer’s instructions, total RNA was fluff mixes and cashmere fibre diameter was insignificant (P > extracted from skin tissues using the Eastep® Super Total RNA 0.05; Table 2). The cashmere fibre length of the treatment Extraction Kit (Promega, Shanghai, China). The concentration group rose by 1.25 cm (P < 0.05), although the cashmere and quality of the extracted total RNA were assessed with the weight did not differ substantially. (P > 0.05; Table 2). NanoDrop spectrophotometer (Bio-Rad, Benicia, USA). Comp- Compared to the long-day photoperiod treatment, the lementary DNAs (cDNAs) were obtained from the reverse tran- short-day photoperiod treatment significantly decreased the scription of RNA with oligo (dT) primer using M-MLV reverse primary hair follicle density in September (P < 0.05; Table 3), transcriptase kit (TaKaRa, Dalian, China). qRT-PCR was per- and increased the secondary hair follicle density in June and formed in triplicate on a Bio-Rad IQ5 Real-Time PCR system July (P < 0.05; Table 3). April had the lowest ratio of secondary with a final volume of 25 μl containing 12.5 μl 2×SYBR® TM to primary follicle density (S:P). In July and September, short- Premix Ex Taq II (TaKaRa, Dalian, China), 1 μl of forward or day photoperiod treatment significantly enhanced the S:P reverse primer (10 μmol/L), 2 μl diluted template cDNA and ratio (P < 0.05; Table 3). 8.5 μl ddH O. The reaction conditions were carried out in accordance with the manufacturer’s guidelines. Three technical replicates were allocated to each sample, and the average Ct Serum hormone concentration value was determined. Using succinate dehydrogenase complex flavoprotein subunit A (SDHA) as the reference gene In June, July and September, Short-day photoperiod treatment (Bai et al. 2014), the 2-ΔΔCt technique was used to calculate significantly raised MT concentrations (P < 0.05; Figure 2A). In the relative expression of each gene. All sequences of primers the short-day photoperiod treatment group, the cyclical fluctu- are shown in Table 1. ations of MT concentrations fluctuated differently than in the Table 1. Primer sequences for quantitative real-time polymerase chain reaction (PCR). Product length Gene GenBank ID Full gene name Primer sequence (bp) Ta (1°C) SDHA XM_018065656.1 Succinate dehydrogenase complex, subunit A F: AGCACTGGAGGAAGCACAC 105 53 R: CACAGTCGGTCTCGTTCAA TRβ XM_005698927.2 Thyroid hormone receptor beta F: ACTCTACGAAGCACACCCAG 208 55 R: GTCCGAGTCCCTGCTTTTCA TRα XM_018065021.1 Thyroid hormone receptor alpha F: GAATGGAACAGAAGCCAAGC 117 57 R: TGCTGGTTTTCAGGGAACAT PRLR NM_001285669.1 Prolactin receptor F: TGCAGCATCTAGAGTGGTTTTC 125 57 R: AGGTGAACGTTTCCTTTCCA ERα XM_013966607.1 Estrogen receptor alpha F: CGGTGGATGTGGTCCTTCTCT 234 61 R: AGGGAAGCTCCTATTTGCTCC ERβ NM_001285688.1 Estrogen receptor beta F: GCTAACCTGCTGATGCTCCTGTCTC 204 65 R: GCCCTCTTTGCTCTCACTGTCCTC RORα NM_001285652.1 Receptor alpha F: TGTGCTTCTCAAAGCAGGTT 120 56 R: GATTTGAAGACATCGGGGCT β-catenin XM_018066894.1 Catenin beta-1 F: GCTGATTTGATGGAGCTGGA 182 58 R: TCATACAGGACTTGGGTGGT PDGFA XM_018040679.1 Platelet-derived growth factor subunit A F: CAGTCAGATCCACAGCATCC 85 56 R: CAGACTGGTTTCCAAAGGCT BMP2 NM_001287564.1 Bone morphogenetic protein 2 F: AAGAGGCATGTGCGGATTAG 129 58 R: TTGCCGCTTTTCTCTTCTGT BMP4 NM_001285646.1 Bone morphogenetic protein 4 F: GCTCTACGTGGACTTCAGTG 126 53 R: TGGTTGGTTGAGTTGAGGTG Ta:annealing temperature. JOURNAL OF APPLIED ANIMAL RESEARCH 55 Short-day photoperiod treatment increased thyroxine 4 (T4) concentrations significantly in July, October and November (P < 0.05), but no significant difference in other months (Figure 2C). In the short-day photoperiod treatment group, blood E2 concentrations were substantially higher in June, August, January, February and March (P < 0.05; Figure 2D). Hormone receptor expression In the long-day photoperiod treatment group, retinoid-related orphan receptor alpha (RORα) expression was lower in August, October and February and greater in November, March and April. The expression of RORα was considerably up-regulated in June, October, December and February and significantly down-regulated in July, November, January, March and April in the short-day photoperiod treatment group (P < 0.05; Figure 3A), delaying the expression peak to December (Figure 3A). As shown in Figure 3, the expression of prolactin receptor (PRLR) in the long-day photoperiod treatment group increased from May until November, when it reached its initial peak, and then decreased. The short-day photoperiod treatment group showed similar patterns. With the short-day photoperiod treat- ment, PRLR expression was substantially higher in May, June, August, December, February and March (P < 0.05) and signifi- cantly lower in October and January (P < 0.05; Figure 3B). The expression of thyroid hormone receptor alpha (TRα)in the short-day photoperiod treatment group was significantly higher in June and August and significantly lower in July, Sep- tember, January, March and April (P < 0.05; Figure 3C). The expression of thyroid hormone receptor beta (TRβ)in the long-day photoperiod treatment group showed a trend of increasing volatility from May and peaked in March of the fol- lowing year. The short-day photoperiod treatment group Figure 1. Effects of short-day photoperiod treatment on growth length and advanced the expression peak of TRβ to February, significantly growth rate of Shaanbei white cashmere goats. (A) Cashmere growth length of up-regulated the expression of TRβ in August, October, Decem- Shaanbei white cashmere goats. * P < 0.05. (B) Cashmere growth rate of Shaanbei ber and February, and significantly down-regulated the white cashmere goats.Different letters means significant difference P < 0.05. Control: Long-day photoperiod treatment group; Treatment: Short-day photo- expression of TRβ in March (P < 0.05; Figure 3D). period treatment group. The expression of estrogen receptor alpha (ERα) in the long- day photoperiod treatment group increased from May, reached a peak in August and then dropped. Short-day photoperiod long-day photoperiod treatment group from May to August, treatment group significantly down-regulated the expression and MT concentrations kept at a high level from June to of ERα in July, August, January, March and April (P < 0.05). In October in the short-day photoperiod treatment group September and October, the concentrations of ERα were elev- (Figure 2A). ated in the short-day photoperiod group (P < 0.05). The peak The initial peak of prolactin (PRL) concentrations in serum of was postponed to October (Figure 3E). long-day photoperiod treatment group occurred in July, fol- In the long-day photoperiod treatment group, the lowed by the second peak in October. Short-day photoperiod expression of estrogen receptor beta (ERβ) was lowest in treatment significantly reduced PRL concentrations in June, October and highest in January. In the short-day photoperiod July and December (P < 0.05; Figure 2B) and altered the peri- treatment group, ERβ expression was significantly up-regulated odic fluctuation of PRL (Figure 2B). (P < 0.05) in June, August, October and March, and significantly down-regulated in July, February and April (P < 0.05; Figure 3F), with the peak occurring in August. Table 2. Effects of short-day photoperiod treatment on cashmere fibre quality of Shaanbei white cashmere goats. Data are expressed as mean ± standard error (SE). Items Control Treatment P-value Gene expression associated with hair follicle Fluff mixtures weight (g) 1153.35 ± 145.11 1228.16 ± 66.58 0.462 development Cashmere weight (g) 593.15 ± 51.04 692.49 ± 49.31 0.072 Cashmere fibre length (cm) 9.34 ± 0.46 10.59 ± 0.53 0.036 The expression of β-catenin in two groups increased gradually Cashmere fibre diameter (µm) 16.92 ± 0.98 17.15 ± 1.07 0.794 from May and reached the highest peak in November and then Note: Control: Long-day photoperiod treatment group. Treatment: Short-day photoperiod treatment group. decreased. From May to July, the expression of β-catenin and 56 J. LI ET AL. Table 3. Effects of short-day photoperiod treatment on hair follicle density of Shaanbei white cashmere goats. Data are expressed as mean ± standard error (SE). Month Group Primary follicle density (per mm-2) p value Secondary follicle density (per mm-2) p value S:P ratio p value May Control 3.34 ± 0.50 0.371 22.08 ± 2.29 0.088 6.75 ± 0.70 0.427 Treatment 2.75 ± 0.31 16.39 ± 1.86 6.03 ± 0.42 June Control 3.00 ± 0.31 0.195 22.04 ± 0.87 0.049 7.44 ± 0.50 0.869 Treatment 3.68 ± 0.30 27.56 ± 1.78 7.58 ± 0.66 July Control 3.06 ± 0.29 0.691 21.50 ± 0.63 0.002 7.15 ± 0.65 0.027 Treatment 3.19 ± 0.08 32.81 ± 1.32 10.33 ± 0.66 August Control 3.37 ± 0.18 0.140 19.94 ± 1.40 0.101 5.98 ± 0.67 0.072 Treatment 2.51 ± 0.43 22.95 ± 0.21 9.60 ± 1.34 September Control 3.52 ± 0.05 0.001 24.45 ± 2.19 0.387 6.93 ± 0.54 0.048 Treatment 2.61 ± 0.06 22.28 ± 0.44 8.62 ± 0.15 October Control 2.68 ± 0.21 0.990 20.00 ± 1.59 0.312 7.51 ± 0.64 0.276 Treatment 2.69 ± 0.12 17.92 ± 0.83 6.67 ± 0.16 November Control 2.53 ± 0.29 0.194 18.18 ± 1.35 0.054 7.30 ± 0.69 0.542 Treatment 3.02 ± 0.13 23.52 ± 1.44 7.77 ± 0.16 December Control 2.44 ± 0.25 0.182 17.48 ± 1.15 0.182 7.22 ± 0.31 0.952 Treatment 1.99 ± 0.12 14.51 ± 1.44 7.26 ± 0.47 January Control 2.27 ± 0.12 0.347 16.94 ± 0.29 0.134 7.51 ± 0.47 0.889 Treatment 2.05 ± 0.16 15.23 ± 0.89 7.44 ± 0.14 February Control 1.84 ± 0.24 0.186 18.95 ± 3.41 0.118 10.18 ± 0.43 0.744 Treatment 2.64 ± 0.44 27.11 ± 2.30 10.58 ± 1.05 March Control 3.12 ± 0.11 0.235 20.74 ± 1.02 0.574 6.68 ± 0.55 0.401 Treatment 2.89 ± 0.13 23.12 ± 3.75 8.05 ± 1.36 April Control 3.72 ± 0.55 0.171 15.21 ± 1.00 0.776 4.33 ± 0.82 0.247 Treatment 2.79 ± 0.04 15.72 ± 1.35 5.63 ± 0.50 Note: Control: Long-day photoperiod treatment group. Treatment: Short-day photoperiod treatment group. Platelet Derived Growth Factor Subunit A (PDGFA) was con- treatment, the first expression peak of PDGFA was observed siderably upregulated by Short-day photoperiod treatment (P in August, one month earlier than with long-day photoperiod < 0.05; Figure 4A; Figure 4B). With short-day photoperiod treatment (Figure 4B). Compared with the long-day Figure 2. Effects of short-day photoperiod treatment on related hormone concentrations of Shaanbei white cashmere goats. (A) Melatonin (MT). (B) Prolactin (PRL). (C) Thyroxine (T4). (D) Estradiol (E2). * P < 0.05. Control: Long-day photoperiod treatment group; Treatment: Short-day photoperiod treatment group. JOURNAL OF APPLIED ANIMAL RESEARCH 57 Figure 3. Effects of short-day photoperiod treatment on related hormone receptor expression of Shaanbei white cashmere goats. (A) Retinoid-related orphan receptor alpha (RORα).(B) Prolactin receptor (PRLR).(C) Thyroid hormone receptor alpha (TRα).(D) Thyroid hormone receptor beta (TRβ). (E) Estrogen receptor alpha (ERα). (F) Estrogen receptor beta (ERβ). * P < 0.05. Control: Long-day photoperiod treatment group; Treatment: Short-day photoperiod treatment group. Figure 4. Effects of short photoperiod treatment on the hair follicle development-related gene expression of Shaanbei white cashmere goats. (A) Catenin beta-1 (β- catenin). (B) Platelet-derived growth factor subunit A (PDGFA). (C) Bone morphogenetic protein 2 (BMP2). (D) Bone morphogenetic protein 4 (BMP4). * P < 0.05. Control: Long-day photoperiod treatment group; Treatment: Short-day photoperiod treatment group. 58 J. LI ET AL. photoperiod treatment, the short-day photoperiod treatment group. We hypothesize that short-day treatment could affect increased the expression of bone morphogenetic protein-2 the interaction between MT and RORα. But the relevant mech- considerably from June to August (P < 0.05; Figure 4C). Short- anism of action has not been elucidated and there are various day photoperiod treatment reduced the expression of bone controversies as to whether MT directly impacts RORα (Ma et al. morphogenetic protein-4 during July (P < 0.05; Figure 4D). 2021), so further research is required. Except for March, short-day photoperiod treatment dramati- Previous research indicates that PRL has an inhibitory effect cally raised the expression of Fibroblast growth factor 5 gene on hair cycle, with high concentrations promoting the termin- in all months (P < 0.05; Figure 4E). ation of cashmere growth (Kloren and Norton 1993; Dicks et al. 1994; Craven et al. 2001). This is consistent with the results of our study. During the early stage of cashmere growth, from Discussion May to August, PRL concentrations were considerably lower Length, diameter and yield are important traits of cashmere, in the short-day photoperiod treatment group than in the which determine the economic value of cashmere. Feral doe long-day photoperiod treatment group, Additionally, PRL and goats have seasonal characteristics, and the change of illumina- MT levels exhibited opposing tendencies simultaneously. MT tion time affects the growth rate, length and diameter of Aus- is able to reduce PRL secretion (Rose et al. 1985; Emesih et al. tralian cashmere goats (McDonald and Hoey 1987). The results 1993; Nixon et al. 1993; Dicks et al. 1995; Duan et al. 2017). of our investigation revealed that the short-day photoperiod By boosting MT concentrations to inhibit PRL levels in cash- treatment boosted cashmere length by 1.25 cm and cashmere mere’s early growth period, short-day photoperiod treatment output by 99.34 g, which increased by 16.75% year-on-year. may enhance the advanced growth of cashmere. PRL exerts Both hair follicle density and the S:P ratio are essential morpho- its biological effects via receptor binding (Morammazi et al. logical parameters of villus hair follicles, having high heritability 2016). During the anagen phase (August to December), high related to sheep wool production (Ansari-Renani et al. 2011). concentrations of PRL up-regulated PRLR expression, which Previous research has demonstrated that melatonin can stimu- peaked during the catagen (January to February) and telogen late the growth of hair follicles (Feng and Gun 2021). Embed- (March to April) phases, which supports the research findings ding MT in vitro induced cashmere growth in advance, of Nixon et al (Nixon et al. 2002). prolonged the growth of the cashmere and increased the T4 regulates the metabolism and growth of the body. Its length of the cashmere (Welch et al. 1990; Cong et al. 2011). secretion is related to the physiological state of an individual. In this study, short-day photoperiod treatment reduced sun- The T4 concentrations of Australian cashmere goats were shine hours in June, July and September, and as melatonin pro- higher in the summer than in the winter, although the seasonal duction is directly related to light, there was less melatonin variation was not obvious (Kloren et al. 1993). The findings of secretion during the day and more at night (Bedrosian et al. this study agree with previous reports. Short-day photoperiod 2013). Due to the prolonged darkness, the MT concentration treatment significantly increased the T4 concentrations in the of the short-day photoperiod treatment group was significantly short-day photoperiod group in July, October and November, higher than that of the long-day photoperiod treatment group but did not significantly change the T4 secretion trend. In in June, July and September, which advanced the reconstruc- addition, short-day photoperiod treatment had no significant tion of secondary hair follicles and stimulated the accelerated effect on their expression patterns. growth of cashmere. The research conducted by Chanda demonstrated that E2 MT has both membrane receptors (MT1, MT2 and MT3) and could promote suppression of the telogen to anagen transition. nuclear receptors (RORα, RORβ and RORγ) (Fischer et al. 2008; It induced hair follicles in the catagen phase to enter the Cutando et al. 2011). The expression of membrane receptor telogen phase and regulated the hair follicle cycle (Chanda was not detected in goat skin (Dicks et al. 1996). In addition, et al. 2000a). E2 increased gradually during the late catagen a prior study demonstrated that RORα was expressed in the phase of SHFs (December). The SHFs were transformed from secondary hair follicles of the hair shaft, inner root sheath, the anagen phase to catagen phase. In male mice, E2 regulated outer root sheath and medulla (Zhao et al. 2015). On the the vital movement of hair follicles by mediating the inhibition basis of these studies, we detected the relative expression of of telogen–anagen transition (Movérare et al. 2002). The RORα gene in the samples and found that the expression of catagen-promoting activities of E2 were mediated by Erα RORα in the long-day photoperiod treatment group peaked (Chanda et al. 2000b; Ohnemus et al. 2005). ERβ antagonized in November, but the short-day photoperiod treatment the mediated action of ERα and MT inhibited the expression delayed the peak expression to December. Melatonin affects of ERα (Ohnemus et al. 2005; Martinez-Campa et al. 2006). the transcriptional control of ROR (Karasek et al. 2003), and Our study demonstrated that short-day photoperiod treatment Fischer suggests that MT mediates the role of RORα in regulat- inhibited the expression of ERα between June and August, ing hair growth (Fischer et al. 2008). Therefore, we compared which is due to the increase of serum MT concentration and MT concentration and RORα expression, and found that in the up-regulation of expression of ERβ. These regulations atte- the long-day photoperiod treatment group, RORα expression nuated the inhibition of hair follicle growth by E2 and pro- and MT concentration appeared opposite peaks in October, moted the growth and development of hair follicles. February and November. The result confirmed the negative Wnt / β-catenin signalling pathway plays a key role in the correlation between MT concentration and RORα expression development of hair follicles. The expression of Wnt signalling (Wang et al. 2013). In June and January, however, contrasting can promote the development, occurrence and differentiation results emerged in the short-day photoperiod treatment of hair follicles (Andl et al. 2002; Fu and Hsu 2013). Low JOURNAL OF APPLIED ANIMAL RESEARCH 59 expression of β-catenin stimulates hair follicle stem cell differ- Disclosure statement entiation to epithelial and hair follicle sebaceous glands, No potential conflict of interest was reported by the author(s). while high expression of β-catenin induces hair follicle recon- struction (Silva-Vargas et al. 2005). Implantation of MT in vitro significantly up-regulated the expression of β-catenin gene in Funding Inner Mongolia cashmere goats (Liu et al. 2016). The present study found that short-day photoperiod treatment boosted This work was supported by Key Science and Technology Program of Inner Mongolia Autonomous Region [grant number 2021ZD0012]; China Agricul- β-catenin gene expression during the early anagen phase of ture Research System [grant number CARS-39-12]; Special Fund for Agro- the cashmere growth (May to July). scientific Research in the Public Interest [grant number 201303059]. The bone morphogenetic protein (BMP) signal pathway plays a crucial role in hair follicle morphogenesis and hair follicle cycling (Botchkarev and Kishimoto 2003). BMP signalling limits References hair follicle cell growth and maintains hair follicles in the telogen period (Millar 2002). Our research revealed that short- Ahn, S.-Y., Pi, L.-Q., Hwang, S.T., Lee, W.-S., 2012.Effect of IGF-I on hair growth is related to the anti-apoptotic effect of IGF-I and up-regulation day photoperiod treatment increased the expression of BMP2 of PDGF-A and PDGF-B. Ann Dermatol. 24, 26-31. doi:10.5021/ad.2012. gene during the early anagen phase, but had no effect on the 24.1.26 expression of BMP4 during the telogen and catagen phases. Andl, T., Reddy, S.T., Gaddapara, T., Millar, S.E., 2002. WNT signals are PDGF is a cell growth factor that inhibits apoptosis (Gruber required for the initiation of hair follicle development. Dev Cell 2, 643- et al. 2000). It is associated with hair follicle growth and angio- 653. doi:10.1016/S1534-5807(02)00167-3 Ansari-Renani, H., Ebadi, Z., Moradi, S., Baghershah, H., Ansari-Renani, M., genesis (Kamp et al. 2003). Insulin-like growth factor 1 (IGF-1) Ameli, S., 2011. Determination of hair follicle characteristics, density treatment up-regulated the expression of PDGFA and plate- and activity of Iranian cashmere goat breeds. Small Ruminant Res 95, let-derived growth factor subunit B (PDGFB), thereby inhibiting 128-132. doi:10.1016/j.smallrumres.2010.09.013 cell apoptosis. These regulations promote hair follicle growth Bai, W. L., Dang, Y. L., Wang, J. J., Yin, R. H., Wang, Z. Y., Zhu, Y. B., Cong, Y. Y., and maintain hair follicles in the anagen phase (Ahn et al. Xue, H. L., Deng, L., Guo, D., Wang, S. Q., Yang, S. H. 2016. Molecular characterization, expression and methylation status analysis of BMP4 2012; Pazzaglia et al. 2019). Our research demonstrated that gene in skin tissue of Liaoning cashmere goat during hair follicle short-day photoperiod treatment increased PDGFA gene cycle. Genetica, 144(4): 457-467. doi:10.1007/s10709-016-9914-1 expression significantly during the early anagen phase. Bai, W.L., Yin, R.H., Yin, R.L., Jiang, W.Q., Wang, J.J., Wang, Z.Y., Zhu, Y.B., Noggin is an inhibitor of BMP (Zimmerman et al. 1996). BMP Zhao, Z.H., Yang, R.J., Luo, G.B., He, J.B., 2014. Selection and validation is located downstream of Wnt /β-catenin (Suzuki et al. 2009). of suitable reference genes in skin tissue of Liaoning cashmere goat during hair follicle cycle. Livest Sci 161, 28–35. doi:10.1016/j.livsci.2013. High expression of β-catenin up-regulated noggin expression 12.031 (Plikus et al. 2008). PDGFA and SHH enhanced the expression Bedrosian, T.A., Herring, K.L., Walton, J.C., Fonken, L.K., Weil, Z.M., Nelson, of the noggin gene in dermal papilla cells. By upregulating R.J., 2013. Evidence for feedback control of pineal melatonin secretion. the expression of -catenin and PDGFA genes in anagen, Neurosci Lett 542, 123–125. doi:10.1016/j.neulet.2013.03.021 short-day photoperiod treatment suppressed the expression Blanpain, C., Fuchs, E., 2006. Epidermal stem cells of the skin. Annu Rev Cell Dev Biol. 22, 339-373. doi:10.1146/annurev.cellbio.22.010305.104357 of the BMP4 gene, hence encouraging hair follicle rebuilding. Botchkarev, V.A., Kishimoto, J., 2003. Molecular control of epithelial– It has been reported that human hair follicles cultured in vitro mesenchymal interactions during hair follicle cycling. J Investig and exposed to recombinant FGF5 enters into catagen phase Dermatol Symp Proc, pp. 46-55. doi:10.1046/j.1523-1747.2003.12171.x prematurely (Higgins et al. 2014). In the early stages of the Cassone, V.M., 1990.Effects of melatonin on vertebrate circadian systems. study, the serum FGF5 concentration and cashmere length of Trends Neurosci 13, 457-464. doi:10.1016/0166-2236(90)90099-V Chanda, S., Robinette, C.L., Couse, J.F., Smart, R.C., 2000a. 17beta-estradiol goats in the short-day photoperiod treatment group were signifi- and ICI-182780 regulate the hair follicle cycle in mice through an estro- cantly higher than those of the control group, suggesting that gen receptor-alpha pathway. Am J Physiol Endocrinol Metab 278, E202- the increase in serum FGF5 concentration lead to the catagen E210. doi:10.1152/ajpendo.2000.278.2.E202 phase of hair follicles, thus promoting cashmere growth. Chanda, S., Robinette, C.L., Couse, J.F., Smart, R.C., 2000b.17β-Estradiol and ICI-182780 regulate the hair follicle cycle in mice through an estrogen receptor-α pathway. Am J Physiol Endocrinol Metab 278, E202-E210. doi:10.1152/ajpendo.2000.278.2.E202 Conclusion Cong, Y., Deng, H., Feng, Y., Chen, Q., Sun, Y., 2011. Melatonin implantation from winter solstice could extend the cashmere growth phase effec- In summary, under the short-day photoperiod treatment, tively. Small Ruminant Res 99, 48-53. doi:10.1016/j.smallrumres.2011. primary hair follicle density dropped by 0.91 follicles/mm2 in 03.055 Craven, A.J., Ormandy, C.J., Robertson, F.G., Wilkins, R.J., Kelly, P.A., Nixon, A.J., September, secondary hair follicle density rose by 5.52 and 2 Pearson, A.J., 2001. 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Journal

Journal of Applied Animal ResearchTaylor & Francis

Published: Dec 31, 2023

Keywords: Cashmere goat; photoperiod; hair follicles; hormone; gene

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