Effect of Fibroblast Growth Factor 10 and an Interacting Non-Coding RNA on Secondary Hair Follicle Dermal Papilla Cells in Cashmere Goats’ Follicle Development Assessed by Whole-Transcriptome Sequencing Technology

Animals : an Open Access Journal from MDPI · 8 authors, 1 centre

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This study used whole-transcriptome sequencing to identify a competing endogenous RNA network in cashmere goat embryos, revealing that miR-184 targets FGF10 to regulate secondary hair follicle dermal papilla cell proliferation, apoptosis, and cell cycle. Overexpression of miR-184 inhibited cell proliferation and promoted apoptosis, while interference had opposite effects, suggesting a key regulatory role in hair follicle development. These findings provide a theoretical basis for improving cashmere yield and quality through genetic breeding.

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**Background:** Cashmere, a keratinized product of secondary hair follicles (SHFs) in cashmere goats, is a high-value textile. The molecular mechanisms underlying hair follicle (HF) development, particularly the role of non-coding RNAs (ncRNAs), are poorly understood. This study aimed to systematically investigate a competing endogenous RNA (ceRNA) regulatory network involving circular RNAs (circRNAs), microRNAs (miRNAs), and messenger RNAs (mRNAs) during SHF development in cashmere goat embryos, focusing on the interaction between miR-184 and fibroblast growth factor 10 (FGF10).

**Methods:** Skin samples were collected from Inner Mongolian cashmere goat fetuses at embryonic days 75 (E75) and 125 (E125), representing early and late stages of HF development. Whole-transcriptome sequencing (long RNA-seq and small RNA-seq) was performed on six samples (three per time point). After quality control, sequence alignment, and differential expression analysis (p < 0.05, fold change ≥ 2), differentially expressed mRNAs, circRNAs, and miRNAs were identified. A ceRNA network was constructed using Cytoscape. The targeting relationship between miR-184 and FGF10 was validated via dual-luciferase reporter assays in 293T and GFF cells. Secondary HF dermal papilla cells (SHF-DPCs) were transfected with miR-184 mimics/inhibitors or FGF10 overexpression/siRNA vectors. Cell proliferation was assessed using CCK-8 at 12, 24, 36, and 48 h. Apoptosis was detected by Annexin V-FITC/PI staining and flow cytometry at 48 h. Cell cycle analysis was performed using PI staining and flow cytometry at 48 h. FGF10 expression was measured by RT-qPCR and Western blotting.

**Key Results:** Sequencing yielded 813,141,270 raw reads from long RNA-seq and 91,915,124 from small RNA-seq, with clean read percentages >99% and >96%, respectively. A total of 6468 differentially expressed mRNAs (3234 upregulated, 3234 downregulated), 394 differentially expressed circRNAs (154 upregulated, 240 downregulated), and 239 differentially expressed miRNAs (97 upregulated, 142 downregulated) were identified between E75 and E125. The ceRNA network included 5581 ncRNA relationship pairs, covering 219 miRNAs, 2477 mRNAs, and 232 circRNAs. Dual-luciferase assays confirmed that miR-184 binds to the 3'UTR of FGF10 and to chi-circRNA-0001141. In SHF-DPCs, miR-184 overexpression significantly reduced FGF10 mRNA and protein levels (p < 0.01 and p < 0.001, respectively), while miR-184 interference increased them (p < 0.01 and p < 0.001). FGF10 overexpression promoted cell proliferation (OD higher at 36 h, p < 0.01; 48 h, p < 0.05) and inhibited apoptosis (apoptosis rate lower, p < 0.05), while FGF10 knockdown had opposite effects (proliferation lower at 36 and 48 h, p < 0.01; apoptosis higher, p < 0.01). miR-184 overexpression inhibited proliferation (OD lower at 36 h, p < 0.05; 48 h, p < 0.01) and promoted apoptosis (apoptosis rate higher, p < 0.01), while miR-184 interference promoted proliferation (OD higher at 36 h, p < 0.001; 48 h, p < 0.05) and inhibited apoptosis (apoptosis rate lower, p < 0.001). Cell cycle analysis showed that FGF10 overexpression decreased G0/G1 phase (p < 0.001) and increased S phase (p < 0.001), while FGF10 knockdown increased G0/G1 (p < 0.05) and decreased S phase (p < 0.05). miR-184 overexpression increased G0/G1 (p < 0.05) and decreased S phase (p < 0.01), while miR-184 interference decreased G0/G1 (p < 0.01) and increased S phase (p < 0.05) and G2/M phase (p < 0.05).

**Clinical Implications:** This study elucidates a novel ceRNA regulatory mechanism involving miR-184 and FGF10 in cashmere goat SHF development. The findings suggest that miR-184 acts as a negative regulator of SHF-DPC proliferation and survival by targeting FGF10, while FGF10 promotes proliferation and inhibits apoptosis. This knowledge provides a theoretical foundation for genetic breeding strategies to improve cashmere yield and quality. Additionally, the identified ceRNA network may offer insights into hair follicle biology in other mammals, potentially informing treatments for hair loss disorders. However, the study is limited by its focus on in vitro cell experiments and lack of in vivo validation, and the role of chi-circRNA-0001141 requires further investigation.

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veterinary medicine

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ORIGINAL PAPER

PMC10340072

Effect of Fibroblast Growth Factor 10 and an Interacting Non-Coding RNA on Secondary Hair Follicle Dermal Papilla Cells in Cashmere Goats’ Follicle Development Assessed by Whole-Transcriptome Sequencing Technology

Animals : an Open Access Journal from MDPI

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ABSTRACT

Abstract Simple Summary Cashmere goats are one of the most important animal breeds in northern China. Cashmere is characterised by good quality and high yield and represents an excellent textile material. However, the molecular mechanism underlying the development of cashmere hair follicles is poorly understood, which limits the further development of the cashmere industry. Here, we used whole-transcriptome sequencing to analyse goat embryonic skin samples and carried out experimental verification. We found that fibroblast growth factor 10 and the interacting non-coding RNA miR-184 play important roles in dermal papilla cells of cashmere goat secondary hair follicles. This discovery not only further improves the theoretical understanding of the development of cashmere wool follicles but also has significant implications for functional research on fibroblast growth factor 10 and miR-184. Abstract Cashmere, a keratinised product of secondary hair follicles (SHFs) in cashmere goats, holds an important place in international high-end textiles. However, research on the complex molecular and signal regulation during the development and growth of hair follicles (HFs), which is essential for the development of the cashmere industry, is limited. Moreover, increasing evidence indicates that non-coding RNAs (ncRNAs) participate in HF development. Herein, we systematically investigated a competing endogenous RNA (ceRNA) regulatory network mediated by circular RNAs (circRNAs), microRNAs (miRNAs), and messenger RNAs (mRNAs) in skin samples of cashmere goat embryos, using whole-transcriptome sequencing technology. We obtained 6468, 394, and 239 significantly differentially expressed mRNAs, circRNAs, and miRNAs, respectively. These identified RNAs were further used to construct a ceRNA regulatory network, mediated by circRNAs, for cashmere goats at a late stage of HF development. Among the molecular species identified, miR-184 and fibroblast growth factor (FGF) 10 exhibited competitive targeted interactions. In secondary HF dermal papilla cells (SHF-DPCs), miR-184 promotes proliferation, inhibits apoptosis, and alters the cell cycle via the competitive release of FGF10. This study reports that FGF10 and its interaction with ncRNAs significantly affect SHF-DPCs, providing a reference for research on the biology of HFs in cashmere goats and other mammals. Keywords: cashmere goats, hair follicle development, FGF10

CITATION EXPORT

Yuan Gao, Weiguo Song, Fei Hao et al.. Effect of Fibroblast Growth Factor 10 and an Interacting Non-Coding RNA on Secondary Hair Follicle Dermal Papilla Cells in Cashmere Goats’ Follicle Development Assessed by Whole-Transcriptome Sequencing Technology. Animals : an Open Access Journal from MDPI. (2023). https://doi.org/10.3390/ani13132234

AUTHORS

8 · 1 CENTRES

Yuan Gao, Weiguo Song, Fei Hao, Lei Duo, Xiaoshu Zhe, Chunyan Gao, Xudong Guo, Dongjun Liu

1State Key Laboratory of Reproductive Regulation and Breeding of Grassland Livestock, School of Life Sciences, Inner Mongolia University, Hohhot 010070, China; [email protected] (Y.G.); [email protected] (W.S.); [email protected] (F.H.); [email protected] (L.D.); [email protected] (X.Z.); [email protected] (C.G.); [email protected] (X.G.)