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Long noncoding RNA and gene expression analysis of melatonin-exposed Liaoning cashmere goat fibroblasts indicating cashmere growth

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Abstract

Cashmere produced from Liaoning cashmere goat is highly valuable. Melatonin is an important factor affecting cashmere growth and can regulate the growth cycle via effects on gene expression. Long noncoding RNAs (lncRNAs) regulate gene expression, but detailed studies of their effect on hair growth are lacking. To explore how lncRNA mediates the effects of melatonin on cashmere growth, we used RNA-Seq including a control condition (C) and three melatonin treatments (1.0 g/L 24 h (M1_24H), 0.2 g/L 24 h (M2_24H), 0.2 g/L 72 h (M2_72H)). M1_24H, M2_24H, and M2_72H had 32, 10, and 113 differentially expressed lncRNAs, respectively. Gene ontology (GO) and pathway analyses results showed that melatonin was most beneficial to cashmere growth at 0.2 g/L 72 h, and nuclear factor (NF)-κB signaling corresponding to an effect of LncRNA MTC was involved in hair follicle development. We found that melatonin upregulated XLOC_005914 lncRNA (LncRNA MTC). Proliferation increased in the 0.2 g/L 72 h condition and cells with high LncRNA MTC expression, but it was reduced in fibroblasts with knocked down LncRNA MTC expression. This is the first report that LncRNA MTC promotes fibroblast proliferation and regulates hair follicle development and cashmere growth by activating NF-κB signaling.

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References

  • Au PC, Zhu QH, Dennis ES, Wang MB (2011) Long non-coding RNA-mediated mechanisms independent of the RNAi pathway in animals and plants. RNA Biol 8:404–414

    Article  CAS  Google Scholar 

  • Bawden CS, Powell BC, Walker SK, Rogers GE, Bawden CS (1998) Expression of a wool intermediate filament keratin transgene in sheep fibre alters structure. Transgenic Res 7:273–287

    Article  CAS  Google Scholar 

  • Chu M, Jia L, Zhang Y, Jin M, Chen H, Fang L, Di R, Cao G, Feng T, Tang Q, Ma Y, Li K (2011) Polymorphisms of coding region of BMPR-IB gene and their relationship with litter size in sheep. Mol Biol Rep 38:4071–4076

    Article  CAS  Google Scholar 

  • Fan YX, Wu RB, Qiao X, Wang RJ, Su R, Wu JH, Dong Y, Li JQ (2015) Hair follicle transcriptome profiles during the transition from anagen to catagen in Cashmere goat (Capra hircus). Genet Mol Res 14:17904–17915

    Article  CAS  Google Scholar 

  • Fischer TW, Sweatman TW, Semak I, Sayre RM, Wortsman J, Slominski A (2006) Constitutive and UV-induced metabolism of melatonin in keratinocytes and cell-free systems. FASEB J 20:1564–1566

    Article  CAS  Google Scholar 

  • Fischer TW, Slominski A, Tobin DJ, Paus R (2008) Melatonin and the hair follicle. J Pineal Res 44:1–15

    Article  CAS  Google Scholar 

  • Fujimoto S, Takase T, Kadono N, Maekubo K, Hirai Y (2014) Krtap11-1, a hair keratin-associated protein, as a possible crucial element for the physical properties of hair shafts. J Dermatol Sci 74:39–47

    Article  CAS  Google Scholar 

  • Guttman M, Garber M, Levin JZ, Donaghey J, Robinson J, Adiconis X, Fan L, Koziol MJ, Gnirke A, Nusbaum C, Rinn JL, Lander ES, Regev A (2010) Ab initio reconstruction of cell type-specific transcriptomes in mouse reveals the conserved multi-exonic structure of lincRNAs. Nat Biotechnol 28:503–510

    Article  CAS  Google Scholar 

  • Heyninck K, Kreike MM, Beyaert R (2003) Structure function analysis of the A20-binding inhibitor of NF-κB activation ABIN-1. FEBS Lett 536:135–140

    Article  CAS  Google Scholar 

  • Houdek P, Nováková M, Polidarová L, Sládek M, Sumová A (2016) Melatonin is a redundant entraining signal in the rat circadian system. Horm Behav 83:1–5

    Article  CAS  Google Scholar 

  • Jia J, Zhang H, Wang L, Zhao Z, Liu M, Lai L, Lu Y (2014) A method for primary culture of pulmonary microvascular endothelial cells. Xi Bao Yu Fen Zi Mian Yi Xue Za Zhi 30:763–766

    CAS  PubMed  Google Scholar 

  • Jin M, Wang L, Li S, Xing MX, Zhang X (2011) Characterization and expression analysis of KAP7.1, KAP8.2 gene in Liaoning new-breeding cashmere goat hair follicle. Mol Biol Rep 38:3023–3028

    Article  CAS  Google Scholar 

  • Kloepper JE, Ernst N, Krieger K, Bodó E, Bíró T, Haslam IS, Schmidt-Ullrich R, Paus R (2014) NF-κB activity is required for anagen maintenance in human hair follicles in vitro. J Investig Dermatol 134:2036–2038

    Article  CAS  Google Scholar 

  • Langbein L, Rogers MA, Praetzel-Wunder S, Helmke B, Schirmacher P, Schweizer J (2006) K25 (K25irs1), K26 (K25irs2), K27 (K25irs3), and K28(K25irs4) represent the type I inner root sheath keratins of the human hair follicle. J Investig Dermatol 126:2377–2386

    Article  CAS  Google Scholar 

  • Laurikkala J, Pispa J (2002) Regulation of hair follicle development by the TNF signal ectodysplasin and its receptor Edar. Development 129:2541–2553

    CAS  PubMed  Google Scholar 

  • Laurikkala J, Pispa J, Jung HS, Nieminen P, Mikkola M, Wang X, Saarialho-Kere U, Galceran J, Grosschedl R, Thesleff I (2014) Regulation of hair follicle development by the TNF signal ectodysplasin and its receptor Edar. Development 129:2541–2553

    Google Scholar 

  • Lin CM, Liu Y, Huang K, Chen XC, Cai BZ, Li HH, Yuan YP, Zhang H, Li Y (2013) Long noncoding RNA expression in dermal papilla cells contributes to hairy gene regulation. Biochem Biophys Res Commun 453:508–514

    Article  Google Scholar 

  • Maung SC, El Sara A, Chapman C, Cohen D, Cukor D (2016) Sleep disorders and chronic kidney disease. World J Nephrol 5:224–232

    Article  Google Scholar 

  • Mercer TR, Dinger ME, Mattick JS (2009) Long non-coding RNAs: insights into functions. Nat Rev Genet 10:155–159

    Article  CAS  Google Scholar 

  • Michal G, Noa S, Shulamit C, Uri G (2008) Transcriptional activation of a subset of hair keratin genes by the NF-κB effector p65/RelA. Differention 76:518–530

    Article  Google Scholar 

  • Mikkola ML (2008) TNF superfamily in skin appendage development. Cytokine Growth Factor Rev 19:219–230

    Article  CAS  Google Scholar 

  • Müller-Röver S, Handjiski B, van der Veen C, Eichmüller S, Foitzik K, McKay IA, Stenn KS, Paus R (2001) A comprehensive guide for the accurate classification of murine hair follicles in distinct hair cycle stages. J Investig Dermatol 117:3–15

    Article  Google Scholar 

  • Nixon AJ, Choy VJ, Parry AL, Pearson AJ (1993) Fiber growth initiation in hair follicles of goats treated with melatonin. J Exp Zool 267:47–56

    Article  CAS  Google Scholar 

  • Persons YM, Cooper DW (1994) Evidence of linkage between high-glycine-tyrosine gene loci and wool fibre diameter in a Merina half-sib family. Anim Genet 25:105–108

    Article  Google Scholar 

  • Powell BC, Rogers GE (1997) The role of keratin proteins and their genes in the growth, structure and properties of hair. EXS 78:59–148

    CAS  PubMed  Google Scholar 

  • Ren H, Wang G, Chen L, Jiang J, Liu L, Li N, Zhao J, Sun X, Zhou P (2016) Genome-wide analysis of long non-coding RNAs at early stage of skin pigmentation in goats (Capra hircus). BMC Genomics 17. https://doi.org/10.1186/s12864-016-2365-3

  • Rogers MA, Langbein L, Winter H, Beckmann I, Praetzel S, Schweizer J (2004) Hair keratin associated proteins: characterization of a second high sulfur KAP gene domain on human chromosome 21. J Investig Dermatol 122:147–158

    Article  CAS  Google Scholar 

  • Rogers MA, Winter H, Langbein L, Wollschläger A, Praetzel-Wunder S, Jave-Suarez LF, Schweizer J (2007) Characterization of human KAP24.1, a cuticular hair keratin-associated protein with unusual amino-acid composition and repeat structure. J Investig Dermatol 127:1197–1204

    Article  CAS  Google Scholar 

  • Rogers MA, Langbein L, Praetzel-Wunder S, Giehl K (2008) Characterization and expression analysis of the hair keratin associated protein KAP26.1. Br J Dermatol 159:725–729

    Article  CAS  Google Scholar 

  • Rust CC, Meyer RK (1969) Hair color, meif and testis size in male, short-tailed weasels treated with melatonin. Science 165:921–922

    Article  CAS  Google Scholar 

  • Santiago-Moreno J, López-Sebastián A, del Campo A, González-Bulnes A, Picazo R, Gómez-Brunet A (2004) Effect of constant-release melatonin implants and prolonged exposure to a long day photoperiod on prolactin secretion and hair growth in mouflon (Ovis gmelini musimon). Domest Anim Endocrinol 26:303–314

    Article  CAS  Google Scholar 

  • Scaife J, Galbraith H, Scaife J, Ewen S (1994) Growth of secondary hair follicles of the Cashmere goat in vitro and their response to prolactin and melatonin. J Anat 185:135–142

    PubMed  PubMed Central  Google Scholar 

  • Slominski A, Pisarchik A, Zbytek B, Tobin DJ, Kauser S, Wortsman J (2003) Functional activity of serotoninergic and melatoniner gicsystem expressed in the skin. J Cell Physiol 196:144–153

    Article  CAS  Google Scholar 

  • Tong X, Coulombe PA (2006a) Keratin 17 modulates hair follicle cycling in a TNF alpha dependent fashion. Genes Dev 20:1353–1364

    Article  CAS  Google Scholar 

  • Tong X, Coulombe PA (2006b) Keratin 17 modulates hair follicle cycling in a TNFα-dependent fashion. Genes Dev 20:1353–1364

    Article  CAS  Google Scholar 

  • Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L (2010) Transcript assembly and quantification by RNA-seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:511–515

    Article  CAS  Google Scholar 

  • Ulitsky I, Bartel DP (2013) lincRNAs: genomics, evolution, and mechanisms. Cell 154:26–46

    Article  CAS  Google Scholar 

  • Weikard R, Hadlich F, Kuehn C (2013) Identification of novel transcripts and noncoding RNAs in bovine skin by deep next generation sequencing. BMC Genomics 14:789. https://doi.org/10.1186/1471-2164-14-789

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Woods JL, Orwin DF (1987) Wool proteins of New Zealand Romney sheep. Aust J Biol Sci 40:1–14

    CAS  PubMed  Google Scholar 

  • Zhao J, Ren Y, Yue W (2007) Analysis of polymorphism on KAP8 gene in three goat breeds with PCR-SSCP. Biotechnology 17:3–6

    CAS  Google Scholar 

  • Zhao YH, Liu ZH, Wang L, Xiao HM, Du CG, Zhang YJ, Su R, Li JQ (2015) Expression of the RORα gene in Inner Mongolian cashmere goat hair follicles. Genet Mol Res 14:380–388

    Article  CAS  Google Scholar 

Download references

Funding

This work was supported by the National Natural Science Foundation of China (grant number 31772557; 31172188) and Liaoning Natural Science Foundation of China (grant number 20170540577).

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Authors and Affiliations

  1. Liaoning Provincial Key Laboratory of Biotechnology and Drug Discovery, Department of Life Sciences, Liaoning Normal University, Dalian, 116000, China

    Mei Jin, Ming Cao, Qian Cao, Jun Piao, Fengqin Zhao & Jing’ai Piao

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  1. Mei Jin
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  2. Ming Cao
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  3. Qian Cao
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  4. Jun Piao
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  5. Fengqin Zhao
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  6. Jing’ai Piao
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Correspondence to Mei Jin.

Ethics declarations

The research protocols in this study were approved by the Animal Experiment and Care Committee of Liaoning Normal University.

Conflict of interest

All co-authors have contributed significantly and agreed with the contents of the manuscript. We certify that the submission is an original work and is not under review at any other publication. The authors declare that they have no conflict of interest.

Ethical approval

The research has been approved by the Liaoning Normal University Ethics Committee. The permission for the Liaoning cashmere goats was obtained prior to the study. The Liaoning Provincial Key Laboratory of Biotechnology and Drug Discovery is responsible for ensuring the protection and care of vertebrate animals used in research studies. We must ensure that animal research is conducted according to long-standing ethical principles and federal, state, and university regulations. In addition to the Animal Care and Use guidelines and regulatory information, this site provides access to tools needed to successfully prepare.

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Informed consent was obtained from all individual participants included in the study. Additional informed consent was obtained from all individual participants for whom identifying information is included in this article.

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Communicated by: Sven Thatje

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Jin, M., Cao, M., Cao, Q. et al. Long noncoding RNA and gene expression analysis of melatonin-exposed Liaoning cashmere goat fibroblasts indicating cashmere growth. Sci Nat 105, 60 (2018). https://doi.org/10.1007/s00114-018-1585-6

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  • DOI: https://doi.org/10.1007/s00114-018-1585-6

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