Restricted accessResearch articleFirst published online 2016-11
Transcriptome-Wide Comparative Analysis of microRNA Profiles in the Telogen Skins of Liaoning Cashmere Goats ( Capra hircus ) and Fine-Wool Sheep ( Ovis aries ) by Solexa Deep Sequencing
Compare the microRNA (miRNA) trancriptomes of goat and sheep skin using Solexa sequencing to understand the development of skin and hair follicles (HFs). miRNA expression patterns vary in the two small RNA libraries from goat (G library) and sheep (S library) telogen skin samples. Analysis of the size distribution of 25.32 million clean reads revealed that most are 21–23 nucleotides. A total of 1910 known miRNAs and 2261 novel mature miRNAs were identified in this study. Among them, 107 novel miRNAs and 1246 known miRNAs were differentially expressed in the two libraries; 10 of the known miRNAs were identified using stem-loop quantitative real-time PCR. Furthermore, GO and KEGG pathway analysis of predicted miRNA targets illustrated the roles of these differentially expressed miRNAs in telogen HF development and growth. This study provides important information about the role of miRNAs in the regulation of HF development and their function in the telogen phase. This observation may help future investigations of the regulation of miRNAs during wool quality improvement.
Get full access to this article
View all access options for this article.
References
1.
AhmedM.I., MardaryevA.N., LewisC.J., SharovA.A., and BotchkarevaN.V. (2011). MicroRNA-21 is an important downstream component of BMP signalling in epidermal keratinocytes. J Cell Sci, 124, 3399–3404.
2.
AllenE., XieZ., GustafsonA.I., and CarringtonJ.C. (2007). microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell, 131, 74–88.
3.
AndlT., MurchisonE.P., LiuF., ZhangY., Yunta-GonzalezM., TobiasJ.W., et al. (2006). The miRNA-processing enzyme dicer is essential for the morphogenesis and maintenance of hair follicles. Curr Biol, 16, 1041–1049.
4.
AndlT., ReddyS.T., GaddaparaT., and MillarS.E. (2002). WNT signals are required for the initiation of hair follicle development. Dev Cell, 2, 643–653.
5.
Aubin-HouzelsteinG. (2012). Notch signaling and the developing hair follicle. Adv Exp Med Biol, 727, 142–160.
6.
BlaszczykJ., TropeaJ.E., BubunenkoM., RoutzahnK.M., WaughD.S., CourtD.L., et al. (2001). Crystallographic and modeling studies of RNase III suggest a mechanism for double-stranded RNA cleavage. Structure, 9, 1225–1236.
7.
DengL., BlancoF.J., StevensH., LuR., CaudrillierA., McBrideM., et al. (2015). MicroRNA-143 activation regulates smooth muscle and endothelial cell crosstalk in pulmonary arterial hypertension. Circ Res, 117, 870–883.
8.
DeppeJ., SteinritzD., SantovitoD., EgeaV., SchmidtA., WeberC., et al. (2016). Upregulation of miR-203 and miR-210 affect growth and differentiation of keratinocytes after exposure to sulfur mustard in normoxia and hypoxia. Toxicol Lett, 244, 81–87.
9.
DickinsonS.E., OlsonE.R., ZhangJ., CooperS.J., MeltonT., CriswellP.J., et al. (2011). p38 MAP kinase plays a functional role in UVB-induced mouse skin carcinogenesis. Mol Carcinog, 50, 469–478.
10.
EzrattyE.J., StokesN., ChaiS., ShahA.S., WilliamsS.E., and FuchsE. (2011). A role for the primary cilium in notch signaling and epidermal differentiation during skin development. Cell, 145, 1129–1141.
11.
GhelaniH.S., RachchhM.A., and GokaniR.H. (2012). MicroRNAs as newer therapeutic targets: a big hope from a tiny player. J Pharmacol Pharmacother, 3, 217–227.
12.
GilesK.M., BrownRAM, EpisM.R., KalinowskiF.C., and LeedmanP.J. (2013). miRNA-7-5p inhibits melanoma cell migration and invasion. Biochem Biophys Res Commun, 430, 706–710.
13.
HardyM.H. (1992). The secret life of the hair follicle. Trends Genet, 8, 55–61.
14.
JamoraC., LeeP., KocieniewskiP., AzharM., HosokawaR., ChaiY., et al. (2004). A signaling pathway involving TGF-β2 and snail in hair follicle morphogenesis. Plos Biol, 3, e11.
15.
JoyceC.E., ZhouX., XiaJ., RyanC., ThrashB., MenterA., et al. (2011). Deep sequencing of small RNAs from human skin reveals major alterations in the psoriasis miRNAome. Hum Mol Genet, 20, 4025–4040.
16.
KramerM.F. (2011). Stem-loop RT-qPCR for miRNAs. Curr Protoc Mol Biol. Chapter 15, Unit 15.10. DOI: 10.1002/0471142727.mb1510s95.
17.
LiR., LiY., KristiansenK., and WangJ. (2008). SOAP: short oligonucleotide alignment program. Bioinformatics, 24, 713–714.
18.
LiW., LuZ.-F., ManX.-Y., LiC.-M., ZhouJ., ChenJ.-Q., et al. (2012a). VEGF upregulates VEGF receptor-2 on human outer root sheath cells and stimulates proliferation through ERK pathway. Mol Biol Rep, 39, 8687–8694.
19.
LiW., ManX.-Y., LiC.-M., ChenJ.-Q., ZhouJ., CaiS.-Q., et al. (2012b). VEGF induces proliferation of human hair follicle dermal papilla cells through VEGFR-2-mediated activation of ERK. Exp Cell Res, 318, 1633–1640.
20.
LinH.-Y., KaoC.-H., LinK.M.-C., KaartinenV., and YangL.-T. (2011). Notch signaling regulates late-stage epidermal differentiation and maintains postnatal hair cycle homeostasis. PLoS One 6,e15842.
21.
LinH.-Y., and YangL.-T. (2013). Differential response of epithelial stem cell populations in hair follicles to TGF-beta signaling. Dev Biol, 373, 394–406.
22.
LiuZ., XiaoH., LiH., ZhaoY., LaiS., YuX., et al. (2012). Identification of conserved and novel microRNAs in cashmere goat skin by deep sequencing. PLoS One, 7, e50001.
23.
LivakK.J., and SchmittgenT.D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods, 25, 402–408.
24.
MahS.M., BuskeC., HumphriesR.K., and KuchenbauerF. (2010). miRNA*: a passenger stranded in RNA-induced silencing complex?. Crit Rev Eukaryot Gene Expr, 20, 141–148.
25.
MaloneC., BrenneckeJ., CzechB., AravinA., and HannonG.J. (2012). Preparation of small RNA libraries for high-throughput sequencing. Cold Spring Harbor Protoc, 2012, 1067–1077.
26.
MardaryevA.N., AhmedM.I., VlahovN.V., FessingM.Y., GillJ.H., SharovA.A., et al. (2010). Micro-RNA-31 controls hair cycle-associated changes in gene expression programs of the skin and hair follicle. FASEB J, 24, 3869–3881.
27.
MeyersB.C., AxtellM.J., BartelB., BartelD.P., BaulcombeD., BowmanJ.L., et al. (2008). Criteria for annotation of plant microRNAs. Plant Cell, 20, 3186–3190.
28.
MikkolaM.L., and MillarS.E. (2006). The mammary bud as a skin appendage: unique and shared aspects of development. J Mammary Gland Biol Neoplasia, 11, 187–203.
NiY., ZhangK., LiuX., YangT., WangB., FuL., et al. (2014). miR-21 promotes the differentiation of hair follicle-derived neural crest stem cells into Schwann cells. Neural Regen Res, 9, 828–836.
31.
NingM.S., and AndlT. (2013). Control by a hair's breadth: the role of microRNAs in the skin. Cell Mol Life Sci, 70, 1149–1169.
32.
NishioH., MatsuiK., TsujiH., TamuraA., and SuzukiK. (2001). Immunolocalisation of the janus kinases (JAK) - signal transducers and activators of transcription (STAT) pathway in human epidermis. J Anat, 198, 581–589.
33.
OhyamaM., ZhengY., PausR., and StennK.S. (2010). The mesenchymal component of hair follicle neogenesis: background, methods and molecular characterization. Exp Dermatol, 19, 89–99.
34.
PausR., Muller-RoverS., van der VeenC., MaurerM., EichmullerS., LingG., et al. (1999). A comprehensive guide for the recognition and classification of distinct stages of hair follicle morphogenesis. J Invest Dermatol, 113, 523–532.
35.
Schmidt-UllrichR., and PausR. (2005). Molecular principles of hair follicle induction and morphogenesis. Bioessays, 27, 247–261.
36.
SchmittM.J., PhilippidouD., ReinsbachS.E., MargueC., Wienecke-BaldacchinoA., NashanD., et al. (2012). Interferon-γ-induced activation of signal transducer and activator of transcription 1 (STAT1) up-regulates the tumor suppressing microRNA-29 family in melanoma cells. Cell Commun Signal 10,41.
37.
SchwabR., PalatnikJ.F., RiesterM., SchommerC., SchmidM., and WeigelD. (2005). Specific effects of MicroRNAs on the plant transcriptome. Dev Cell, 8, 517–527.
38.
SperlingL.C. (1991). Hair anatomy for the clinician. J Am Acad Dermatol, 25, 1–17.
39.
StennK.S., and PausR. (2001). Controls of hair follicle cycling. Physiol Rev, 81, 449–494.
40.
WeiY., ChenS., YangP., MaZ., and KangL. (2009). Characterization and comparative profiling of the small RNA transcriptomes in two phases of locust. Genome Biol 10,R6.
41.
WenguangZ., JianghongW., JinquanL., and YashizawaM. (2007). A subset of skin-expressed microRNAs with possible roles in goat and sheep hair growth based on expression profiling of mammalian microRNAs. OMICS, 11, 385–396.
42.
WieduwiltM.J., and MoasserM.M. (2008). The epidermal growth factor receptor family: biology driving targeted therapeutics. Cell Mol Life Sci, 65, 1566–1584.
43.
XieS.-S., LiX.-Y., LiuT., CaoJ.-H., ZhongQ., and ZhaoS.-H. (2011). Discovery of porcine microRNAs in multiple tissues by a solexa deep sequencing approach. PLoS One, 6, e16235.
44.
YiR., and FuchsE. (2010). MicroRNA-mediated control in the skin. Cell Death Differ, 17, 229–235.
45.
YiR., PoyM.N., StoffelM., and FuchsE. (2008). A skin microRNA promotes differentiation by repressing 'stemness'. Nature, 452, 225–229.
46.
ZhangS., ZhaoF., WeiC., ShengX., RenH., XuL., et al. (2013a). Identification and characterization of the miRNA transcriptome of Ovis aries. PLoS One, 8, e58905.
47.
ZhangX.-D., ZhangY.-H., LingY.-H., LiuY., CaoH.-G., YinZ.-J., et al. (2013b). Characterization and differential expression of microRNAs in the ovaries of pregnant and non-pregnant goats (Capra hircus). BMC Genomics, 14, 157.
Supplementary Material
Please find the following supplemental material available below.
For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.
For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.
