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LncRNA ST6GALNAC3 inhibits dermal fibroblast proliferation and migration in cashmere goat hair follicles via the chi-miR-24-3p/ID4 axis

  • Rong Ma (College of Animal Science, Inner Mongolia Agricultural University) ;
  • Qing Ma (College of Animal Science, Inner Mongolia Agricultural University) ;
  • Lu Zhang (Science and Technology Development Center of Ulanqab) ;
  • Bingjie Ma (College of Animal Science, Inner Mongolia Agricultural University) ;
  • Xuxu Bao (College of Animal Science, Inner Mongolia Agricultural University) ;
  • Yiming Zhang (College of Animal Science, Inner Mongolia Agricultural University) ;
  • Le Wang (College of Animal Science, Inner Mongolia Agricultural University) ;
  • Qi Lv (College of Animal Science, Inner Mongolia Agricultural University) ;
  • Zhiying Wang (College of Animal Science, Inner Mongolia Agricultural University) ;
  • Ruijun Wang (College of Animal Science, Inner Mongolia Agricultural University) ;
  • Rui Su (College of Animal Science, Inner Mongolia Agricultural University) ;
  • Yanhong Zhao (College of Animal Science, Inner Mongolia Agricultural University) ;
  • Fangzheng Shang (College of Animal Science, Inner Mongolia Agricultural University) ;
  • Yu Wang (College of Veterinary Medicine, Inner Mongolia Agricultural University) ;
  • Yanjun Zhang (College of Animal Science, Inner Mongolia Agricultural University)
  • Received : 2025.02.21
  • Accepted : 2025.06.07
  • Published : 2025.09.01

Abstract

Objective: Dermal papilla is developed from the continuous proliferation and differentiation of dermal fibroblasts, which is the key to the normal development of hair follicles. This study aims to elucidate the role of lncRNA ST6GALNAC3, which is significantly differentially expressed during the secondary hair follicle development stage in cashmere goats, on dermal fibroblasts, and to analyze the regulatory mechanism of this lncRNA thoroughly. Methods: We conducted a screening process and characterization for lncRNAs associated with the development of secondary hair follicles. The effects of lncRNA ST6GALNAC3 on cell proliferation and migration were assessed using CCK8, EdU, and flow cytometry. Subsequently, we employed bioinformatics analysis to identify the target miRNAs of lncRNA ST6GALNAC3 and the corresponding target genes of these miRNAs, respectively, and initially constructed the regulatory axis of lncRNA ST6GALNAC3-chi-miR-24-3p-ID4. Luciferase reporter assays and rescue experiments were performed to confirm the regulatory axis at both molecular and cellular levels, thus elucidating the mechanism by which lncRNA ST6GALNAC3 regulates dermal fibroblasts. Results: One hundred fifty-eight lncRNAs related to secondary hair follicle morphogenesis were identified. Among them, lncRNA ST6GALNAC3 was significantly differentially expressed on embryonic day 75 and significantly inhibited the proliferation and migration of dermal fibroblasts. The results showed that lncRNA ST6GALNAC3 can target chi-miR-24-3p, which in turn can target the ID4 gene. The results of the luciferase reporter assay and rescue assay showed that chi-miR-24-3p binds to both lncRNA ST6GALNAC3 and ID4. Furthermore, lncRNA ST6GALNAC3 can indirectly regulate the proliferation and migration of dermal fibroblasts through chi-miR-24-3p/ID4 axis. Conclusion: LncRNA ST6GALNAC3 inhibits the proliferation and migration of dermal fibroblasts through the chi-miR-24-3p/ID4 axis, thus suppressing the formation of dermal papilla structures and influencing the morphogenesis of secondary hair follicles during embryonic development.

Keywords

Acknowledgement

We thank the Inner Mongolia Jinlai Animal Husbandry for providing experimental samples and LC Biological (Guangzhou, China) for the RNA-seq sequencing in this study.

References

  1. Wang M, Ma R, Ma Q, et al. Role of LncRNA MSTRG. 20890.1 in hair follicle development of cashmere goats. Genes 2024;15:1392. https://doi.org/10.3390/genes15111392
  2. Zhang PY. Production and research status of cashmere goat industry in the world. Anim Husb Feed Sci 1994;1:20-4.
  3. Mapar M, Chopra D, Stephan L, et al. Genetic and molecular analysis of root hair development in Arabis alpina. Front Plant Sci 2021;12:767772. https://doi.org/10.3389/fpls.2021.767772
  4. Schneider MR, Schmidt-Ullrich R, Paus R. The hair follicle as a dynamic miniorgan. Curr Biol 2009;19:R132-42. https://doi.org/10.1016/j.cub.2008.12.005
  5. Jiang H. Hair follicle structure traits and developmental mechanisms of Chinese cashmere goat. J Jilin Agric Univ 2012;34:473-82. https://doi.org/10.13327/j.jjlau.2012.05.020
  6. Ma R, Wang M, Ma Q, Zhang Y, Shang F, Wang R. LncRNA MSTRG.14227.1 regulates the morphogenesis of secondary hair follicles in inner Mongolia cashmere goats via targeting ADAMTS3 by sponging chi-miR-433. J Anim Sci 2024;103:skae382. https://doi.org/10.1093/jas/skae382
  7. Zhang YJ, Yin J, Li CQ. Study on development of skin and hair follicle from fetal inner Mongolian Arbas cashmere goats. Acta Vet Zootech Sin 2006;37:761-8.
  8. Yanjun Z, Jun Y, Jinquan L. Study on hair follicle structure and morphogenesis of the inner Mongolian Arbas cashmere goat. Sci Agric Sin 2007;40:1017-23.
  9. Feng ZQ, Sun YF, Song YP, et al. Research progress of Wnt/β-catenin signaling pathway in the regulation of hair follicle development and hair cycle. Chin J Anim Sci 2021;57:88-95. https://doi.org/10.19556/j.0258-7033.20200807-03
  10. Chang Y, Bao P, Chu M, Wu X, Liang C, Yn P. Research progress on the regulation of LncRNA in the development of mammalian hair follicle. Biotechnol Bull 2019;35:205-12. https://doi.org/10.13560/j.cnki.biotech.bull.1985.2019-0187
  11. Zhang T, Zhang Y, Li X, et al. An anti-sense lncRNA of the A-FABP gene regulates the proliferation of hair follicle stem cells via the chi-miR-335-5p/DKK1/β-catenin axis. Int J Biol Macromol 2024;283:137511. https://doi.org/10.1016/j.ijbiomac.2024.137511
  12. Zhang Y, Li F, Shi Y, Zhang T, Wang X. Comprehensive transcriptome analysis of hair follicle morphogenesis reveals that lncRNA-H19 promotes dermal papilla cell proliferation through the chi-miR-214-3p/β-catenin axis in cashmere goats. Int J Mol Sci 2022;23:10006. https://doi.org/10.3390/ijms231710006
  13. Ma R, Shang F, Rong Y, et al. Expression profile of long noncoding RNA in inner Mongolian cashmere goat with putative roles in hair follicles development. Front Vet Sci 2022;9:995604. https://doi.org/10.3389/fvets.2022.995604
  14. Cao Z, Pan X, Yang Y, Huang Y, Shen HB. The lncLocator: a subcellular localization predictor for long non-coding RNAs based on a stacked ensemble classifier. Bioinformatics 2018;34:2185-94. https://doi.org/10.1093/bioinformatics/bty085
  15. Agarwal V, Bell GW, Nam JW, Bartel DP. Predicting effective microRNA target sites in mammalian mRNAs. eLife 2015;4:e05005. https://doi.org/10.7554/eLife.05005
  16. Betel D, Wilson M, Gabow A, Marks DS, Sander C. The microRNA.org resource: targets and expression. Nucleic Acids Res 2008;36:D149-53. https://doi.org/10.1093/nar/gkm995
  17. Kang YJ, Yang DC, Kong L, et al. CPC2: a fast and accurate coding potential calculator based on sequence intrinsic features. Nucleic Acids Res 2017;45:W12-6. https://doi.org/10.1093/nar/gkx428
  18. Sun L, Luo H, Bu D, et al. Utilizing sequence intrinsic composition to classify protein-coding and long non-coding transcripts. Nucleic Acids Res 2013;41:e166. https://doi.org/10.1093/nar/gkt646
  19. Ma R, Du H, Cao Y, et al. Research progress on the regulatory mechanisms of follicle morphogenesis and development in mammals. J China Agric Univ 2024;29:40-55. https://doi.org/10.11841/j.issn.1007-4333.2024.05.04
  20. Salmena L, Poliseno L, Tay Y, Kats L, Pandolfi PP. A ceRNA hypothesis: the Rosetta Stone of a hidden RNA language? Cell 2011;146:353-8. https://doi.org/10.1016/j.cell.2011.07.014