Identification of skin-expressed genes possibly associated with wool growth regulation of Aohan fine wool sheep

BMC Genetics

Jinshan Zhao¹  Guangling He³  Jifeng Liu⁴  Wei De²  Ming Cheng⁵  Ran Bu⁴  Juanjuan Yu⁴  Kaidong Liu⁵  Hegang Li⁵  Nan Liu⁴ 

[1] China Agricultural University, Beijing 100193, China;Nanjing Medical University, Nanjing 210002, China;State key Laboratory of Hydroscience and Engineering, Beijing 100084, China;Qingdao Agricultural University, Qingdao 266109, China;Qingdao Institute of Animal Science and Veterinary Medicine, Qingdao 266100, China

关键词: Differential expression;    Wool growth;    Proteomic technology;    Microarray;   

Others  :  1084974
DOI  :  10.1186/s12863-014-0144-1

 received in 2013-11-19, accepted in 2014-12-03,  发布年份 2014

【 摘 要 】

Background

Sheep are valuable resources for the animal fibre industry. Therefore, identifying genes which regulate wool growth would offer strategies for improving the quality of fine wool. In this study, we employed Agilent sheep gene expression microarray and proteomic technology to compare the gene expression patterns of the body side (hair-rich) and groin (hairless) skins of Aohan fine wool sheep (a Chinese indigenous breed).

Results

Comparing the body side to the groin skins (S/G) of Aohan fine wool sheep, the microarray study revealed that 1494 probes were differentially expressed, including 602 more highly expressed and 892 less highly expressed probes. The microarray results were verified by means of quantitative PCR. Cluster analysis could distinguish the body side skin and the groin skin. Based on the Database for Annotation, Visualization and Integrated Discovery (DAVID), 38 of the differentially expressed genes were classified into four categories, namely regulation of receptor binding, multicellular organismal process, protein binding and macromolecular complex. Proteomic study revealed that 187 protein spots showed significant (p < 0.05) differences in their respective expression levels. Among them, 46 protein entries were further identified by MALDI-TOF/MS analyses.

Conclusions

Microarray analysis revealed thousands of differentially expressed genes, many of which were possibly associated with wool growth. Several potential gene families might participate in hair growth regulation. Proteomic analysis also indentified hundreds of differentially expressed proteins.

【 授权许可】

   
2014 Liu et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

【 参考文献 】

• [1]Purvis IW, Franklin IR: Major genes and QTL influencing wool production and quality: a review. Genet Sel Evol 2005, 37(S1):S97-S107. BioMed Central Full Text
• [2]Beh KJ, Callaghan MJ, Leish Z, Hulme DJ, Lenane I, Maddox JF: A genome scan for QTL affecting fleece and wool traits in Merino sheep. Wool Technol Sheep Breed 2001, 49:88-89.
• [3]Bidinost F, Roldan DL, Dodero AM, Cano EM, Taddeo HR, Mueller JP, Poli MA: Wool quantitative trait loci in Merino sheep. Small Ruminant Res 2008, 74:113-118.
• [4]Cano EM, Marrube G, Roldan DL, Bidinost F, Abad M, Allain D, Vaiman D, Taddeo H, Poli MA, Bray AR: QTL affecting fleece traits in Angora goats. Small Ruminant Res 2007, 71:158-164.
• [5]Itenge TO, Hickford JG, Forrest RH, McKenzie GW, Frampton CM: Improving the quality of wool through the use of gene markers. South Afr J Animal Sci 2009, 39:219-223.
• [6]Galbraith H: Fundamental hair follicle biology and fine fibre production in animals. Animal 2010, 4:1490-1509.
• [7]Schmidt-Ullrich R, Paus R: Molecular principles of hair follicle induction and morphogenesis. Bioessays 2005, 27:247-261.
• [8]McGrice HA: Molecular Characterisation of Primary Wool Follicle Initiation in Merino Sheep. University of Adelaide, School of agriculture, food and wine, ᅟ; 2010.
• [9]Janich P, Pascual G, Merlos-Suarez A, Batlle E, Ripperger J, Albrecht U, Obrietan K, Di Croce L, Benitah SA: The circadian molecular clock creates epidermal stem cell heterogeneity. Nature 2011, 480:209-214.
• [10]Rhee H, Polak L, Fuchs E: Lhx2 maintains stem cell character in hair follicles. Science 2006, 312:1946-1949.
• [11]Cotsarelis G: Gene expression profiling gets to the root of human hair follicle stem cells. J Clin Invest 2006, 116:19-22.
• [12]Ohyama M, Terunuma A, Tock CL, Radonovich MF, Pise-Masison CA, Hopping SB, Brady JN, Udey MC, Vogel JC: Characterization and isolation of stem cell-enriched human hair follicle bulge cells. J Clin Invest 2006, 116:249-260.
• [13]Keane OM, Zadissa A, Wilson T, Hyndman DL, Greer GJ, Baird DB, McCulloch AF, Crawford AM, McEwan JC: Gene expression profiling of naive sheep genetically resistant and susceptible to gastrointestinal nematodes. BMC Genomics 2006, 7:42. BioMed Central Full Text
• [14]MacKinnon KM, Burton JL, Zajac AM, Notter DR: Microarray analysis reveals difference in gene expression profiles of hair and wool sheep infected with Haemonchus contortus. Vet Immunol Immunopathol 2009, 130:210-220.
• [15]Bongiorni S, Chillemi G, Prosperini G, Bueno S, Valentini A, Pariset L: A tool for sheep product quality: custom microarrays from public databases. Nutrients 2009, 1:235-250.
• [16]Faucon F, Rebours E, Bevilacqua C, Helbling JC, Aubert J, Makhzami S, Dhorne-Pollet S, Robin S, Martin P: Terminal differentiation of goat mammary tissue during pregnancy requires the expression of genes involved in immune functions. Physiol Genomics 2009, 40:61-82.
• [17]Ollier S, Robert-Granie C, Bernard L, Chilliard Y, Leroux C: Mammary transcriptome analysis of food-deprived lactating goats highlights genes involved in milk secretion and programmed cell death. J Nutr 2007, 137:560-567.
• [18]Norris BJ, Bower NI, Smith WJ, Cam GR, Reverter A: Gene expression profiling of ovine skin and wool follicle development using a combined ovine-bovine skin cDNA microarray. Aust J Exp Agr 2005, 45:867-877.
• [19]Smith WJ, Li Y, Ingham A, Collis E, McWilliam SM, Dixon TJ, Norris BJ, Mortimer SI, Moore RJ, Reverter A: A genomics-informed, SNP association study reveals FBLN1 and FABP4 as contributing to resistance to fleece rot in Australian Merino sheep. BMC Vet Res 2010, 6:27. BioMed Central Full Text
• [20]Penagaricano F, Zorrilla P, Naya H, Robello C, Urioste JI: Gene expression analysis identifies new candidate genes associated with the development of black skin spots in Corriedale sheep. J Appl Genet 2012, 53:99-106.
• [21]Wenguang Z, Jianghong W, Jinquan L, Yashizawa M: A subset of skin-expressed microRNAs with possible roles in goat and sheep hair growth based on expression profiling of mammalian microRNAs. OMICS 2007, 11:385-396.
• [22]Yu Z-D, Bawden CS, Henderson HV, Nixon AJ, Gordon SW, Pearson AJ: Micro-arrays as a discovery tool for wool genomics. Proc New Zeal SocAnimal Prod 2006, 66:129-133.
• [23]Yu Z-D, Gordon SW, Pearson AJ, Henderson HV, Craven AJ, Nixon AJ: Gene expression profiling of wool follicle growth cycles by cDNA microarray. Proc New Zeal SocAnimal Prod 2008, 68:39-42.
• [24]Liu N, Li H, Liu K, Yu J, Cheng M, De W, Liu J, Shi S, He Y, Zhao J: Differential expression of genes and proteins associated with wool follicle cycling.Mol Biol Rep 2014, published online in advance of the print edition.
• [25]Jiang Y, Xie M, Chen W, Talbot R, Maddox JF, Faraut T, Wu C, Muzny DM, Li Y, Zhang W, Stanton JA, Brauning R, Barris WC, Hourlier T, Aken BL, Searle SM, Adelson DL, Bian C, Cam GR, Chen Y, Cheng S, DeSilva U, Dixen K, Dong Y, Fan G, Franklin IR, Fu S, Fuentes-Utrilla P, Guan R, Highland MA, et al.: The sheep genome illuminates biology of the rumen and lipid metabolism. Science 2014, 344(6188):1168-1173.
• [26]Wang HR, Feng ZC, Du M, Ren JK, Li HR: Initial research for seasonal variation of wool growth of Aohan fine wool sheep. Inner Mongolia Animal Sci 1994, 3:1-3. (in Chinese)
• [27]Yu JJ, Liu JF, Zhao JS, Cheng M, Liu KD, Liu N: Gene chip analysis of expression pattern of type I Inner Root Sheath (IRS) keratin in AoHan wool sheep. Agr Scie Technol 2012, 13:1171-1174.
• [28]Zhao JS, Li HG, Liu KD, Liu N, Li JQ: Differential expression of immune genes between body side skin and groin skin of Aohan fine wool sheep. Agr Scie Technol 2012, 13:2475-2479.
• [29]McElwee KJ, Sinclair R: Hair Physiology and its Disorders. Drug Discovery Today: Disease Mechanisms. 2008.
• [30]Kawano M, Komi-Kuramochi A: Comprehensive analysis of FGF and FGFR expression in skin. J Invest Dermatol 2005, 124:877-885.
• [31]Stenn KS, Paus R: Controls of hair follicle cycling. Physiol Rev 2001, 81:449-494.
• [32]Sampath H, Flowers MT, Liu X, Paton CM, Sullivan R, Chu K, Zhao M, Ntambi JM: Skin-specific deletion of stearoyl-CoA desaturase-1 alters skin lipid composition and protects mice from high fat diet-induced obesity. J Biol Chem 2009, 284:19961-19973.
• [33]Karelina TV, Bannikov GA, Eisen AZ: Basement membrane zone remodeling during appendageal development in human fetal skin: the absence of type VII collagen is associated with gelatinase-A (MMP2) activity. J Invest Dermatol 2000, 114:371-375.
• [34]Philp D, Nguyen M, Scheremeta B, St-Surin S, Villa AM, Orgel A, Kleinman HK, Elkin M: Thymosin beta4 increases hair growth by activation of hair follicle stem cells. FASEB J 2004, 18:385-387.
• [35]Jones PH, Watt FM: Separation of human epidermal stem cells from transit amplifying cells on the basis of differences in integrin function and expression. Cell 1993, 73:713-724.
• [36]Kloepper JE, Hendrix S, Bodo E, Tiede S, Humphries MJ, Philpott MP, Fassler R, Paus R: Functional role of beta 1 integrin-mediated signalling in the human hair follicle. Exp Cell Res 2008, 314:498-508.
• [37]Brakebusch C, Grose R, Quondamatteo F, Ramirez A, Jorcano JL, Pirro A, Svensson M, Herken R, Sasaki T, Timpl R, Werner S, Fassler R: Skin and hair follicle integrity is crucially dependent on beta 1 integrin expression on keratinocytes. EMBO J 2000, 19:3990-4003.
• [38]Rowe JM, Welsh C, Pena RN, Wolf CR, Brown K, Whitelaw CB: Illuminating role of CYP1A1 in skin function. J Invest Dermatol 2008, 128:1866-1868.
• [39]Ryu K, Yokoyama M, Yamashita M, Hirano T: Induction of excitatory and inhibitory presynaptic differentiation by GluD1. Biochem Biophys Res Commun 2012, 417:157-161.
• [40]Lein ES, Hawrylycz MJ, Ao N, Ayres M, Bensinger A, Bernard A, Boe AF, Boguski MS, Brockway KS, Byrnes EJ, Chen L, Chen TM, Chin MC, Chong J, Crook BE, Czaplinska A, Dang CN, Datta S, Dee NR, Desaki AL, Desta T, Diep E, Dolbeare TA, Donelan MJ, Dong HW, Dougherty JG, Duncan BJ, Ebbert AJ, Eichele G, Estin LK, et al.: Genome-wide atlas of gene expression in the adult mouse brain. Nature 2007, 445:168-176.
• [41]Magdaleno S, Jensen P, Brumwell CL, Seal A, Lehman K, Asbury A, Cheung T, Cornelius T, Batten DM, Eden C, Norland SM, Rice DS, Dosooye N, Shakya S, Mehta P, Curran T: BGEM: an in situ hybridization database of gene expression in the embryonic and adult mouse nervous system. PLoS Biol 2006, 4:e86.
• [42]Higgins CA, Richardson GD, Ferdinando D, Westgate GE, Jahoda CA: Modelling the hair follicle dermal papilla using spheroid cell cultures. Exp Dermatol 2010, 19:546-548.
• [43]Churko JM, Chan J, Shao Q, Laird DW: The G60S connexin43 mutant regulates hair growth and hair fiber morphology in a mouse model of human oculodentodigital dysplasia. J Invest Dermatol 2011, 131:2197-2204.
• [44]Colombe L, Vindrios A, Michelet JF, Bernard BA: Prostaglandin metabolism in human hair follicle. Exp Dermatol 2007, 16:762-769.
• [45]Johnstone MA, Albert DM: Prostaglandin-induced hair growth. Surv Ophthalmol 2002, 47(S1):S185-S202.
• [46]Umeda-Ikawa A: Time-course expression profiles of hair cycle-associated genes in male mini rats after depilation of telogen-phase hairs. Int J Mol Sci 2009, 10:1967-1977.
• [47]Powell BC, Beltrame JS: Characterization of a hair (wool) keratin intermediate filament gene domain. J Invest Dermatol 1994, 102:171-177.
• [48]Yu Z, Gordon SW, Nixon AJ, Bawden CS, Rogers MA, Wildermoth JE, Maqbool NJ, Pearson AJ: Expression patterns of keratin intermediate filament and keratin associated protein genes in wool follicles. Differentiation 2009, 77:307-316.
• [49]Goh BK, Common JE, Gan WH, Kumarasinghe P: A case of dermatopathia pigmentosa reticularis with wiry scalp hair and digital fibromatosis resulting from a recurrent KRT14 mutation. Clin Exp Dermatol 2009, 34:340-343.
• [50]Lugassy J, Itin P, Ishida-Yamamoto A, Holland K, Huson S, Geiger D, Hennies HC, Margarita I, Dani B, Jouni U, Bergman R, McGrath JA, Richard G, Sprecher E: Naegeli-Franceschetti-Jadassohn syndrome and dermatopathia pigmentosa reticularis: two allelic ectodermal dysplasias caused by dominant mutations in KRT14. Am J Hum Genet 2006, 79:724-730.
• [51]Horner ME, Parkinson KE, Kaye V, Lynch PJ: Dowling-Degos disease involving the vulva and back: case report and review of the literature. Dermatol Online J 2011, 17:1.
• [52]Kizawa K, Takahara H, Troxler H, Kleinert P, Mochida U, Heizmann CW: Specific citrullination causes assembly of a globular S100A3 homotetramer: a putative Ca2+ modulator matures human hair cuticle. J Biol Chem 2008, 283:5004-5013.
• [53]Lueking A, Huber O, Wirths C, Schulte K, Stieler KM, Blume-Peytavi U, Kowald A, Hensel-Wiegel K, Tauber R, Lehrach H, Meyer HE, Cahill DJ: Profiling of alopecia areata autoantigens based on protein microarray technology. Mol Cell Proteomics 2005, 4:1382-1390.
• [54]Rosenquist TA, Martin GR: Fibroblast growth factor signalling in the hair growth cycle: expression of the fibroblast growth factor receptor and ligand genes in the murine hair follicle. Dev Dyn 1996, 205:379-386.
• [55]Nacht M, Dracheva T, Gao Y, Fujii T, Chen Y, Player A, Akmaev V, Cook B, Dufault M, Zhang M, Zhang W, Guo M, Curran J, Han S, Sidransky D, Buetow K, Madden SL, Jen J: Molecular characteristics of non-small cell lung cancer. Proc Natl Acad Sci U S A 2001, 98:15203-15208.
• [56]Tang Z, Li Y, Wan P, Li X, Zhao S, Liu B, Fan B, Zhu M, Yu M, Li K: LongSAGE analysis of skeletal muscle at three prenatal stages in Tongcheng and Landrace pigs. Genome Biol 2007, 8:R115. BioMed Central Full Text
• [57]Dennis G Jr, Sherman BT, Hosack DA, Yang J, Gao W, Lane HC, Lempicki RA: DAVID: database for annotation, visualization, and integrated discovery. Genome Biol 2003, 4:P3. BioMed Central Full Text
• [58]Berndt P, Hobohm U, Langen H: Reliable automatic protein identification from matrix-assisted laser desorption/ionization mass spectrometric peptide fingerprints. Electrophoresis 1999, 20:3521-3526.