基于转录组学筛选与哺乳动物睾丸发育相关基因及调控网络的研究进展
|
摘要
睾丸正常发育是雄性哺乳动物精子发生及有效繁殖力的先决条件,其发育过程极其精细和复杂,受到许多因素的影响及调控,但遗传调控占主导地位。哺乳动物睾丸的发育首先会受到大量蛋白编码基因的严格调控,非编码RNA(miRNA、lncRNA和piRNA)也在睾丸发育及精子发生过程扮演重要角色。近年来,以mRNA、miRNA、lncRNA、piRNA为主的转录组学在解析哺乳动物睾丸发育以及精子发生分子机制得到充分应用,并且取得了很大进展。本文从睾丸发育相关mRNA、miRNA、lncRNA、piRNA等方面对哺乳动物睾丸发育研究现状进行介绍与阐述,旨在为深入挖掘睾丸发育基因组变化以及畜牧业中动物育种提供重要理论依据。
Testis maturation and development are a prerequisite for spermatogenesis and effective reproduction in mammals,the process of maturation is extremely complex,which was affected by multiple factors,especially genetic factors.Testis development process was strictly regulated by lots of protein-coding genes,while growing evidences showed that non-coding RNAs(miRNAs,lncRNAs and piRNAs)also played an important roles in testicular development and spermatogenesis.In recent years,the study of transcriptome based on mRNA,miRNA,lncRNA and piRNA have been successfully applied in exploring molecular mechanism of mammalian testicular development and spermatogenesis,and have made great progress.In this review,we summarized the current status of testis development research in mammals from the aspect of testicular developmental-related genes,miRNAs,lncRNAs and piRNA in order to provide reference and theoretical basis for understanding global genome expression change in testicular development and betterguide in animal breeding in the livestock industry.
Testis maturation and development are a prerequisite for spermatogenesis and effective reproduction in mammals,the process of maturation is extremely complex,which was affected by multiple factors,especially genetic factors.Testis development process was strictly regulated by lots of protein-coding genes,while growing evidences showed that non-coding RNAs(miRNAs,lncRNAs and piRNAs)also played an important roles in testicular development and spermatogenesis.In recent years,the study of transcriptome based on mRNA,miRNA,lncRNA and piRNA have been successfully applied in exploring molecular mechanism of mammalian testicular development and spermatogenesis,and have made great progress.In this review,we summarized the current status of testis development research in mammals from the aspect of testicular developmental-related genes,miRNAs,lncRNAs and piRNA in order to provide reference and theoretical basis for understanding global genome expression change in testicular development and betterguide in animal breeding in the livestock industry.
引文
[1]JACYNO E,KAW CKA M,PIETRUSZKA A,et al.Phenotypic correlations of testes size with semen traits and the productive traits of young boars[J].Reprod Domest Anim,2015,50(6):926-930.
[2]GONZALEZ-PENA D,KNOX R V,MACNEIL M D,et al.Genetic gain and economic values of selection strategies including semen traits in three-and fourway crossbreeding systems for swine production[J].J Anim Sci,2015,93(3):879-891.
[3]YTOURNEL F,BRUNET E,DERKS P,et al.Testes size as predictor for semen production of boars and relation to female reproductive traits[C]//Proceedings of 10th World Congress on Genetics Applied To Livestock Production.Vancouver BC:American Society of Animal Science,2014.
[4]ALMAGUER Y,FONT H,CABRERA S,et al.Relationship between body and testicular measurements in young buffalo bulls in Cuba[J].Rev Colomb Cienc Pec,2017,30(2):138-146.
[5]HAGIYA K,HANAMURE T,HAYAKAWA H,et al.Genetic correlations between yield traits or days open measured in cows and semen production traits measured in bulls[J].Animal,2017:1-5,doi:10.1017/S1751731117003470.
[6]COULTER G H,FOOTE R H.Bovine testicular measurements as indicators of reproductive performance and their relationship to productive traits in cattle:A review[J].Theriogenology,1979,11(4):297-311.
[7]PARK S Y,JAMESON J L.Minireview:Transcriptional regulation of gonadal development and differentiation[J].Endocrinology,2005,146(3):1035-1042.
[8]LIU C,ZHANG Y H,DENG Q,et al.Cancer-related triplets of mRNA-lncRNA-miRNA revealed by integrative network in uterine corpus endometrial carcinoma[J].Biomed Res Int,2017,2017:3859582.
[9]SHARPE R M,MCKINNELL C,KIVLIN C,et al.Proliferation and functional maturation of Sertoli cells,and their relevance to disorders of testis function in adulthood[J].Reproduction,2003,125(6):769-784.
[10]GONG W,PAN L L,LIN Q,et al.Transcriptome profiling of the developing postnatal mouse testis using next-generation sequencing[J].Sci China Life Sci,2013,56(1):1-12.
[11]MRUK D D,CHENG C Y.Sertoli-sertoli and sertoligerm cell interactions and their significance in germ cell movement in the seminiferous epithelium during spermatogenesis[J].Endocr Rev,2004,25(5):747-806.
[12]SOZUBIR S,BARBER T,WANG Y,et al.Loss of Insl3:A potential predisposing factor for testicular torsion[J].J Urol,2010,183(6):2373-2379.
[13]PITIA A M,UCHIYAMA K,SANO H,et al.Functional insulin‐like factor 3(INSL3)hormone-receptor system in the testes and spermatozoa of domestic ruminants and its potential as a predictor of sire fertility[J].Anim Sci J,2017,88(4):678-690.
[14]RAN M L,CHEN B,WU M S,et al.Integrated analysis of miRNA and mRNA expression profiles in development of porcine testes[J].RSC Adv,2015,5(78):63439-63449.
[15]SONG H B,ZHU L H,LI Y,et al.Exploiting RNAsequencing data from the porcine testes to identify the key genes involved in spermatogenesis in Large White pigs[J].Gene,2015,573(2):303-309.
[16]SUN Z,LI Z,ZHANG Y.Adult testicular dysgenesis of Inhba conditional knockout mice may also be caused by disruption of cross-talk between Leydig cells and germ cells[J].Proc Natl Acad Sci U S A,2010,107(35):E135.
[17]PARKER C C,GOPALAKRISHNAN S,CARBONETTO P,et al.Genome-wide association study of behavioral,physiological and gene expression traits in outbred CFW mice[J].Nat Genet,2016,48(8):919-926.
[18]SCHUBERT C.Scaffold for splicing[J].Biol Reprod,2015,92(3):59.
[19]LI Y,LI J L,FANG C C,et al.Genome-wide differential expression of genes and small RNAs in testis of two different porcine breeds and at two different ages[J].Sci Rep,2016,6:26852.
[20]萨初拉,孔群芳,吴应积.哺乳动物睾丸中c-kit基因表达对生精细胞发育的影响[J].中国细胞生物学学报,2013,35(5):703-711.SACHLA,KONG Q F,WU Y J.The effects of c-kit on development of male germ cells in the mammal's testis[J].Chinese Journal of Cell Biology,2013,35(5):703-711.(in Chinese)
[21]孙兆贵,顾正,王健.KiSS-1/GPR54系统的生殖内分泌功能研究进展[J].生殖与避孕,2009,29(6):374-384.SUN Z G,GU Z,WANG J.Research advances in functions of Kiss-1/GPR54 system in reproductive endocrinology[J].Reproduction&Contraception,2009,29(6):374-384.(in Chinese)
[22]钟金城,姬秋梅,柴志欣,等.基于转录组测序对犏牛和牦牛睾丸组织的分析研究[C]//中国遗传学会第9次全国会员代表大会暨学术研讨会论文集.哈尔滨:中国遗传学会,2013.ZHONG J C,JI Q M,CHAI Z X,et al.Analysis of Yak and Yak testicles based on transcriptome sequencing[C]//Proceedings of the 9th National Member Congress and Academic Seminar of the Chinese Society of Genetics.Harbin:Genetics Society of China,2013.(in Chinese)
[23]郭芳,罗国静,鞠志花,等.SPEF2基因可变剪切体和功能性SNP鉴定及其与公牛精液性状的相关性研究[J].南京农业大学学报,2014,37(3):119-125.GUO F,LUO G J,JU Z H,et al.Association of SPEF2gene splices variant and functional SNP with semen quality traits in Chinese Holstein bulls[J].Journal of Nanjing Agricultural University,2014,37(3):119-125.(in Chinese)
[24]白井岩,吴洁,蒋小强,等.公牛MBL2基因多态性与精液品质及后裔生产性能的相关性研究[J].畜牧兽医学报,2013,44(10):1561-1568.BAI J Y,WU J,JIANG X Q,et al.Association of polymorphisms of MBL2gene with semen quality and progeny performance of bulls[J].Acta Veterinaria et Zootechnica Sinica,2013,44(10):1561-1568.(in Chinese)
[25]CHANG T C,YANG Y,RETZEL E F,et al.Malespecific region of the bovine Y chromosome is gene rich with a high transcriptomic activity in testis development[J].Proc Natl Acad Sci U S A,2013,110(30):12373-12378.
[26]GUO Z W,XIE C,YANG J R,et al.MtiBase:A database for decoding microRNA target sites located within CDS and 5′UTR regions from CLIP-Seq and expression profile datasets[J].Database,2015,2015.pii:bav102.
[27]LIN Y H,BUNDSCHUH R.RNA structure generates natural cooperativity between single-stranded RNA binding proteins targeting 5′and 3′UTRs[J].Nucleic Acids Res,2015,43(2):1160-1169.
[28]WONGFIENG W,JUMNAINSONG A,CHAMGRAMOL Y,et al.5′-UTR and 3′-UTR regulation of MICB expression in human cancer cells by novel microRNAs[J].Genes,2017,8(9):213.
[29]王天宇,董园园,李海燕,等.microRNAs的分子进化与调控机制[J].遗传,2010,32(9):874-880.WANG T Y,DONG Y Y,LI H Y,et al.Molecular evolution and regulatory mechanism of microRNAs[J].Hereditas,2010,32(9):874-880.(in Chinese)
[30]SREE S,RADHAKRISHNAN K,INDU S,et al.Dramatic changes in 67miRNAs during initiation of first wave of spermatogenesis in Mus musculus testis:Global regulatory insights generated by miRNAmRNA network analysis[J].Biol Reprod,2014,91(3):69.
[31]李东伟,屈长青,刘洪瑜.miR-34c在哺乳动物生殖发育过程中的功能探讨[J].阜阳师范学院学报:自然科学版,2014,31(4):58-61.LI D W,QU C Q,LIU H Y.Function of miR-34cin process of mammalian reproductive development[J].Journal of Fuyang Teachers College:Natural Science,2014,31(4):58-61.(in Chinese)
[32]LI M Z,YU M,LIU C,et al.Expression of miR-34c in response to overexpression of Boule and Stra8in dairy goat male germ line stem cells(mGSCs)[J].Cell Biochem Funct,2013,31(4):281-288.
[33]LI M,YU M,LIU C,et al.miR-34c works downstream of p53leading to dairy goat male germline stem-cell(mGSCs)apoptosis[J].Cell Prolif,2013,46(2):223-231.
[34]YANG Q E,RACICOT K E,KAUCHER A V,et al.microRNAs 221and 222regulate the undifferentiated state in mammalian male germ cells[J].Development,2013,140(2):280-290.
[35]HE Z P,JIANG J J,KOKKINAKI M,et al.miRNA-20 and miRNA-106aregulate spermatogonial stem cell renewal at the post-transcriptional level via targeting STAT3and Ccnd1[J].Stem Cells,2013,31(10):2205-2217.
[36]HUANG L Z,MA J,SUN Y K,et al.Altered splenic miRNA expression profile in H1N1swine influenza[J].Arch Virol,2015,160(4):979-985.
[37]张晓军,李传民,赵伟,等.猪睾丸组织中miR-375的表达及靶基因预测[J].中国兽医学报,2014,34(11):1846-1849.ZHANG X J,LI C M,ZHAO W,et al.The expression of miR-375and its target genes prediction in testicular tissue of junmu No.1white pig[J].Chinese Journal of Veterinary Science,2014,34(11):1846-1849.(in Chinese)
[38]ZHANG X J,LI C M,LIU X,et al.Differential expression of miR-499and validation of predicted target genes in the testicular tissue of swine at different developmental stages[J].DNA Cell Biol,2015,34(7):464-469.
[39]WENG B,RAN M L,CHEN B,et al.Systematic identification and characterization of miRNAs and piRNAs from porcine testes[J].Genes Genom,2017,39(10):1047-1057.
[40]LIAN C J,SUN B X,NIU S L,et al.A comparative profile of the microRNA transcriptome in immature and mature porcine testes using Solexa deep sequencing[J].FEBS J,2012,279(6):964-975.
[41]BJORK J K,SANDQVIST A,ELSING A N,et al.miR-18,a member of Oncomir-1,targets heat shock transcription factor 2in spermatogenesis[J].Development,2010,137(19):3177-3184.
[42]MORITOKI Y,KOJIMA Y,MIZUNO K,et al.260the role of mir-135avia regulation of foxo1gene expression in maintenance of spermatogonial stem cells[J].J Urol,2013,189(4):e106-e107.
[43]EO J,SONG H,LIM H J.Etv5,a transcription factor with versatile functions in male reproduction[J].Clin Exp Reprod Med,2012,39(2):41-45.
[44]廖珂.牦牛、普通牛和犏牛睾丸组织microRNA的比较研究[D].成都:西南民族大学,2016.LIAO K.Comparative analysis of microRNA in yak,ordinary cattle and cattle-yak testis tissue[D].Chengdu:Southwest Minzu University,2016.(in Chinese)
[45]REN H X,WANG G F,LEI C,et al.Genome-wide analysis of long non-coding RNAs at early stage of skin pigmentation in goats(Capra hircus)[J].BMC Genomics,2016,17:67.
[46]NISHANT K T,RAVISHANKAR H,RAO M R S.Characterization of a mouse recombination hot spot locus encoding a novel non-protein-coding RNA[J].Mol Cell Biol,2004,24(12):5620-5634.
[47]ANGUERA M C,MA W Y,CLIFT D,et al.Tsxproduces a long noncoding RNA and has general functions in the germline,stem cells,and brain[J].PLoS Genet,2011,7(9):e1002248.
[48]SUN J,LIN Y,WU J.Long non-coding RNA expression profiling of mouse testis during postnatal development[J].PLoS One,2013,8(10):e75750.
[49]RAN M,CHEN B,LI Z,et al.Systematic identification of long noncoding RNAs in immature and mature porcine testes[J].Biol Reprod,2016,94(4):77.
[50]韩聪.山羊生精细胞发育及睾丸组织lncRNA差异表达分析[D].杨凌:西北农林科技大学,2017.HAN C.The development of spermatogenic cells and the analysis of lncRNA differential expression in goats[D].Yangling:Northwest A&F University,2017.(in Chinese)
[51]PARALKAR V R,MISHRA T,LUAN J,et al.Lineage and species-specific long noncoding RNAs during erythro-megakaryocytic development[J].Blood,2014,123(12):1927-1937.
[52]ZHAO W M,MU Y L,MA L,et al.Systematic identification and characterization of long intergenic noncoding RNAs in fetal porcine skeletal muscle development[J].Sci Rep,2015,5:8957.
[53]ZHAO J,SUN B K,ERWIN J A,et al.Polycomb proteins targeted by a short repeat RNA to the mouse X chromosome[J].Science,2008,322(5902):750-756.
[54]BISCHOFF S R,TSAI S Q,HARDISON N E,et al.Differences in X-chromosome transcriptional activity and cholesterol metabolism between placentae from swine breeds from Asian and Western origins[J].PLoS One,2013,8(1):e55345.
[55]SLEUTELS F,ZWART R,BARLOW D P.The noncoding Air RNA is required for silencing autosomal imprinted genes[J].Nature,2002,415(6873):810-813.
[56]ZHOU Y,WU K,JIANG J P,et al.Integrative analysis reveals enhanced regulatory effects of human long intergenic non-coding RNAs in lung adenocarcinoma[J].J Genet Genomics,2015,42(8):423-436.
[57]CUI W R,QIAN Y L,ZHOU X K,et al.Discovery and characterization of long intergenic non-coding RNAs(lincRNA)module biomarkers in prostate cancer:An integrative analysis of RNA-Seq data[J].BMC Genomics,2015,16:S3.
[58]毛军,张贤生.piRNA通路与精子发生的研究进展[J].中华男科学杂志,2016,22(10):923-927.MAO J,ZHANG X S.The piRNA pathway and spermatogenesis:Advances in studies[J].National Journal of Andrology,2016,22(10):923-927.(in Chinese)
[59]李春艳,任春环,刘秋月,等.piRNA的形成及其在雌性动物中生物学功能研究进展[J].畜牧兽医学报,2017,48(10):1785-1795.LI C Y,REN C H,LIU Q Y,et al.Research progress on piRNA formation and function in female animals[J].Acta Veterinaria et Zootechnica Sinica,2017,48(10):1785-1795.(in Chinese)
[60]YANG Q L,HUA J,WANG L,et al.microRNA and piRNA profiles in normal human testis detected by next generation sequencing[J].PLoS One,2013,8(6):e66809.
[61]JIANG X Z,LI D J,YANG J F,et al.Characterization of a novel human testis-specific gene:Testis developmental related gene 1(TDRG1)[J].Tohoku J Exp Med,2011,225(4):311-318.
[62]LAZAROS L,XITA N,KAPONIS A,et al.The association of aromatase(CYP19)gene variants with sperm concentration and motility[J].Asian J Androl,2011,13(2):292-297.
[63]YAO L,LI J L,FANG C C,et al.Genome-wide differential expression of genes and small RNAs in testis of two different porcine breeds and at two different ages[J].Sci Rep,2016,6:26852.
[64]LIU G,LEI B,LI Y,et al.Discovery of potential piRNAs from next generation sequences of the sexually mature porcine testes[J].PLoS One,2012,7(4):e34770.
[65]道楞.蒙古马睾丸发育及精子生成相关piRNA的鉴定及表达调控研究[D].呼和浩特:内蒙古农业大学,2017.DAO L.Identification and expression regulation of piRNA in Mongolian horse testis development and spermatogenesis[D].Hohhot:Inner Mongolia Agricultural University,2017.(in Chinese)
[66]PILLAI R S,CHUMA S.piRNAs and their involvement in male germline development in mice[J].Dev Growth Differ,2012,54(1):78-92.
[67]STALKER L,RUSSELL S J,CO C,et al.PIWIL1is expressed in the Canine testis,increases with sexual maturity,and binds small RNAs[J].Biol Reprod,2016,94(1):17.
[68]李玥,赵少志,江雪,等.恒河猴piwil1基因的表达[J].应用与环境生物学报,2012,18(1):60-64.LI Y,ZHAO S Z,JIANG X,et al.Expression of piwil1gene in Macaca mulatta[J].Chinese Journal of Applied&Environmental Biology,2012,18(1):60-64.(in Chinese)
[69]顾垚.黄牛、犏牛Piwi通路相关基因以及睾丸组织基因组甲基化分析[D].南京:南京农业大学,2012.GU Y.Methylation status of Piwi genes and genome in testis of cattle and cattle yaks[D].Nanjing:Nanjing Agricultural University,2012.(in Chinese)
[2]GONZALEZ-PENA D,KNOX R V,MACNEIL M D,et al.Genetic gain and economic values of selection strategies including semen traits in three-and fourway crossbreeding systems for swine production[J].J Anim Sci,2015,93(3):879-891.
[3]YTOURNEL F,BRUNET E,DERKS P,et al.Testes size as predictor for semen production of boars and relation to female reproductive traits[C]//Proceedings of 10th World Congress on Genetics Applied To Livestock Production.Vancouver BC:American Society of Animal Science,2014.
[4]ALMAGUER Y,FONT H,CABRERA S,et al.Relationship between body and testicular measurements in young buffalo bulls in Cuba[J].Rev Colomb Cienc Pec,2017,30(2):138-146.
[5]HAGIYA K,HANAMURE T,HAYAKAWA H,et al.Genetic correlations between yield traits or days open measured in cows and semen production traits measured in bulls[J].Animal,2017:1-5,doi:10.1017/S1751731117003470.
[6]COULTER G H,FOOTE R H.Bovine testicular measurements as indicators of reproductive performance and their relationship to productive traits in cattle:A review[J].Theriogenology,1979,11(4):297-311.
[7]PARK S Y,JAMESON J L.Minireview:Transcriptional regulation of gonadal development and differentiation[J].Endocrinology,2005,146(3):1035-1042.
[8]LIU C,ZHANG Y H,DENG Q,et al.Cancer-related triplets of mRNA-lncRNA-miRNA revealed by integrative network in uterine corpus endometrial carcinoma[J].Biomed Res Int,2017,2017:3859582.
[9]SHARPE R M,MCKINNELL C,KIVLIN C,et al.Proliferation and functional maturation of Sertoli cells,and their relevance to disorders of testis function in adulthood[J].Reproduction,2003,125(6):769-784.
[10]GONG W,PAN L L,LIN Q,et al.Transcriptome profiling of the developing postnatal mouse testis using next-generation sequencing[J].Sci China Life Sci,2013,56(1):1-12.
[11]MRUK D D,CHENG C Y.Sertoli-sertoli and sertoligerm cell interactions and their significance in germ cell movement in the seminiferous epithelium during spermatogenesis[J].Endocr Rev,2004,25(5):747-806.
[12]SOZUBIR S,BARBER T,WANG Y,et al.Loss of Insl3:A potential predisposing factor for testicular torsion[J].J Urol,2010,183(6):2373-2379.
[13]PITIA A M,UCHIYAMA K,SANO H,et al.Functional insulin‐like factor 3(INSL3)hormone-receptor system in the testes and spermatozoa of domestic ruminants and its potential as a predictor of sire fertility[J].Anim Sci J,2017,88(4):678-690.
[14]RAN M L,CHEN B,WU M S,et al.Integrated analysis of miRNA and mRNA expression profiles in development of porcine testes[J].RSC Adv,2015,5(78):63439-63449.
[15]SONG H B,ZHU L H,LI Y,et al.Exploiting RNAsequencing data from the porcine testes to identify the key genes involved in spermatogenesis in Large White pigs[J].Gene,2015,573(2):303-309.
[16]SUN Z,LI Z,ZHANG Y.Adult testicular dysgenesis of Inhba conditional knockout mice may also be caused by disruption of cross-talk between Leydig cells and germ cells[J].Proc Natl Acad Sci U S A,2010,107(35):E135.
[17]PARKER C C,GOPALAKRISHNAN S,CARBONETTO P,et al.Genome-wide association study of behavioral,physiological and gene expression traits in outbred CFW mice[J].Nat Genet,2016,48(8):919-926.
[18]SCHUBERT C.Scaffold for splicing[J].Biol Reprod,2015,92(3):59.
[19]LI Y,LI J L,FANG C C,et al.Genome-wide differential expression of genes and small RNAs in testis of two different porcine breeds and at two different ages[J].Sci Rep,2016,6:26852.
[20]萨初拉,孔群芳,吴应积.哺乳动物睾丸中c-kit基因表达对生精细胞发育的影响[J].中国细胞生物学学报,2013,35(5):703-711.SACHLA,KONG Q F,WU Y J.The effects of c-kit on development of male germ cells in the mammal's testis[J].Chinese Journal of Cell Biology,2013,35(5):703-711.(in Chinese)
[21]孙兆贵,顾正,王健.KiSS-1/GPR54系统的生殖内分泌功能研究进展[J].生殖与避孕,2009,29(6):374-384.SUN Z G,GU Z,WANG J.Research advances in functions of Kiss-1/GPR54 system in reproductive endocrinology[J].Reproduction&Contraception,2009,29(6):374-384.(in Chinese)
[22]钟金城,姬秋梅,柴志欣,等.基于转录组测序对犏牛和牦牛睾丸组织的分析研究[C]//中国遗传学会第9次全国会员代表大会暨学术研讨会论文集.哈尔滨:中国遗传学会,2013.ZHONG J C,JI Q M,CHAI Z X,et al.Analysis of Yak and Yak testicles based on transcriptome sequencing[C]//Proceedings of the 9th National Member Congress and Academic Seminar of the Chinese Society of Genetics.Harbin:Genetics Society of China,2013.(in Chinese)
[23]郭芳,罗国静,鞠志花,等.SPEF2基因可变剪切体和功能性SNP鉴定及其与公牛精液性状的相关性研究[J].南京农业大学学报,2014,37(3):119-125.GUO F,LUO G J,JU Z H,et al.Association of SPEF2gene splices variant and functional SNP with semen quality traits in Chinese Holstein bulls[J].Journal of Nanjing Agricultural University,2014,37(3):119-125.(in Chinese)
[24]白井岩,吴洁,蒋小强,等.公牛MBL2基因多态性与精液品质及后裔生产性能的相关性研究[J].畜牧兽医学报,2013,44(10):1561-1568.BAI J Y,WU J,JIANG X Q,et al.Association of polymorphisms of MBL2gene with semen quality and progeny performance of bulls[J].Acta Veterinaria et Zootechnica Sinica,2013,44(10):1561-1568.(in Chinese)
[25]CHANG T C,YANG Y,RETZEL E F,et al.Malespecific region of the bovine Y chromosome is gene rich with a high transcriptomic activity in testis development[J].Proc Natl Acad Sci U S A,2013,110(30):12373-12378.
[26]GUO Z W,XIE C,YANG J R,et al.MtiBase:A database for decoding microRNA target sites located within CDS and 5′UTR regions from CLIP-Seq and expression profile datasets[J].Database,2015,2015.pii:bav102.
[27]LIN Y H,BUNDSCHUH R.RNA structure generates natural cooperativity between single-stranded RNA binding proteins targeting 5′and 3′UTRs[J].Nucleic Acids Res,2015,43(2):1160-1169.
[28]WONGFIENG W,JUMNAINSONG A,CHAMGRAMOL Y,et al.5′-UTR and 3′-UTR regulation of MICB expression in human cancer cells by novel microRNAs[J].Genes,2017,8(9):213.
[29]王天宇,董园园,李海燕,等.microRNAs的分子进化与调控机制[J].遗传,2010,32(9):874-880.WANG T Y,DONG Y Y,LI H Y,et al.Molecular evolution and regulatory mechanism of microRNAs[J].Hereditas,2010,32(9):874-880.(in Chinese)
[30]SREE S,RADHAKRISHNAN K,INDU S,et al.Dramatic changes in 67miRNAs during initiation of first wave of spermatogenesis in Mus musculus testis:Global regulatory insights generated by miRNAmRNA network analysis[J].Biol Reprod,2014,91(3):69.
[31]李东伟,屈长青,刘洪瑜.miR-34c在哺乳动物生殖发育过程中的功能探讨[J].阜阳师范学院学报:自然科学版,2014,31(4):58-61.LI D W,QU C Q,LIU H Y.Function of miR-34cin process of mammalian reproductive development[J].Journal of Fuyang Teachers College:Natural Science,2014,31(4):58-61.(in Chinese)
[32]LI M Z,YU M,LIU C,et al.Expression of miR-34c in response to overexpression of Boule and Stra8in dairy goat male germ line stem cells(mGSCs)[J].Cell Biochem Funct,2013,31(4):281-288.
[33]LI M,YU M,LIU C,et al.miR-34c works downstream of p53leading to dairy goat male germline stem-cell(mGSCs)apoptosis[J].Cell Prolif,2013,46(2):223-231.
[34]YANG Q E,RACICOT K E,KAUCHER A V,et al.microRNAs 221and 222regulate the undifferentiated state in mammalian male germ cells[J].Development,2013,140(2):280-290.
[35]HE Z P,JIANG J J,KOKKINAKI M,et al.miRNA-20 and miRNA-106aregulate spermatogonial stem cell renewal at the post-transcriptional level via targeting STAT3and Ccnd1[J].Stem Cells,2013,31(10):2205-2217.
[36]HUANG L Z,MA J,SUN Y K,et al.Altered splenic miRNA expression profile in H1N1swine influenza[J].Arch Virol,2015,160(4):979-985.
[37]张晓军,李传民,赵伟,等.猪睾丸组织中miR-375的表达及靶基因预测[J].中国兽医学报,2014,34(11):1846-1849.ZHANG X J,LI C M,ZHAO W,et al.The expression of miR-375and its target genes prediction in testicular tissue of junmu No.1white pig[J].Chinese Journal of Veterinary Science,2014,34(11):1846-1849.(in Chinese)
[38]ZHANG X J,LI C M,LIU X,et al.Differential expression of miR-499and validation of predicted target genes in the testicular tissue of swine at different developmental stages[J].DNA Cell Biol,2015,34(7):464-469.
[39]WENG B,RAN M L,CHEN B,et al.Systematic identification and characterization of miRNAs and piRNAs from porcine testes[J].Genes Genom,2017,39(10):1047-1057.
[40]LIAN C J,SUN B X,NIU S L,et al.A comparative profile of the microRNA transcriptome in immature and mature porcine testes using Solexa deep sequencing[J].FEBS J,2012,279(6):964-975.
[41]BJORK J K,SANDQVIST A,ELSING A N,et al.miR-18,a member of Oncomir-1,targets heat shock transcription factor 2in spermatogenesis[J].Development,2010,137(19):3177-3184.
[42]MORITOKI Y,KOJIMA Y,MIZUNO K,et al.260the role of mir-135avia regulation of foxo1gene expression in maintenance of spermatogonial stem cells[J].J Urol,2013,189(4):e106-e107.
[43]EO J,SONG H,LIM H J.Etv5,a transcription factor with versatile functions in male reproduction[J].Clin Exp Reprod Med,2012,39(2):41-45.
[44]廖珂.牦牛、普通牛和犏牛睾丸组织microRNA的比较研究[D].成都:西南民族大学,2016.LIAO K.Comparative analysis of microRNA in yak,ordinary cattle and cattle-yak testis tissue[D].Chengdu:Southwest Minzu University,2016.(in Chinese)
[45]REN H X,WANG G F,LEI C,et al.Genome-wide analysis of long non-coding RNAs at early stage of skin pigmentation in goats(Capra hircus)[J].BMC Genomics,2016,17:67.
[46]NISHANT K T,RAVISHANKAR H,RAO M R S.Characterization of a mouse recombination hot spot locus encoding a novel non-protein-coding RNA[J].Mol Cell Biol,2004,24(12):5620-5634.
[47]ANGUERA M C,MA W Y,CLIFT D,et al.Tsxproduces a long noncoding RNA and has general functions in the germline,stem cells,and brain[J].PLoS Genet,2011,7(9):e1002248.
[48]SUN J,LIN Y,WU J.Long non-coding RNA expression profiling of mouse testis during postnatal development[J].PLoS One,2013,8(10):e75750.
[49]RAN M,CHEN B,LI Z,et al.Systematic identification of long noncoding RNAs in immature and mature porcine testes[J].Biol Reprod,2016,94(4):77.
[50]韩聪.山羊生精细胞发育及睾丸组织lncRNA差异表达分析[D].杨凌:西北农林科技大学,2017.HAN C.The development of spermatogenic cells and the analysis of lncRNA differential expression in goats[D].Yangling:Northwest A&F University,2017.(in Chinese)
[51]PARALKAR V R,MISHRA T,LUAN J,et al.Lineage and species-specific long noncoding RNAs during erythro-megakaryocytic development[J].Blood,2014,123(12):1927-1937.
[52]ZHAO W M,MU Y L,MA L,et al.Systematic identification and characterization of long intergenic noncoding RNAs in fetal porcine skeletal muscle development[J].Sci Rep,2015,5:8957.
[53]ZHAO J,SUN B K,ERWIN J A,et al.Polycomb proteins targeted by a short repeat RNA to the mouse X chromosome[J].Science,2008,322(5902):750-756.
[54]BISCHOFF S R,TSAI S Q,HARDISON N E,et al.Differences in X-chromosome transcriptional activity and cholesterol metabolism between placentae from swine breeds from Asian and Western origins[J].PLoS One,2013,8(1):e55345.
[55]SLEUTELS F,ZWART R,BARLOW D P.The noncoding Air RNA is required for silencing autosomal imprinted genes[J].Nature,2002,415(6873):810-813.
[56]ZHOU Y,WU K,JIANG J P,et al.Integrative analysis reveals enhanced regulatory effects of human long intergenic non-coding RNAs in lung adenocarcinoma[J].J Genet Genomics,2015,42(8):423-436.
[57]CUI W R,QIAN Y L,ZHOU X K,et al.Discovery and characterization of long intergenic non-coding RNAs(lincRNA)module biomarkers in prostate cancer:An integrative analysis of RNA-Seq data[J].BMC Genomics,2015,16:S3.
[58]毛军,张贤生.piRNA通路与精子发生的研究进展[J].中华男科学杂志,2016,22(10):923-927.MAO J,ZHANG X S.The piRNA pathway and spermatogenesis:Advances in studies[J].National Journal of Andrology,2016,22(10):923-927.(in Chinese)
[59]李春艳,任春环,刘秋月,等.piRNA的形成及其在雌性动物中生物学功能研究进展[J].畜牧兽医学报,2017,48(10):1785-1795.LI C Y,REN C H,LIU Q Y,et al.Research progress on piRNA formation and function in female animals[J].Acta Veterinaria et Zootechnica Sinica,2017,48(10):1785-1795.(in Chinese)
[60]YANG Q L,HUA J,WANG L,et al.microRNA and piRNA profiles in normal human testis detected by next generation sequencing[J].PLoS One,2013,8(6):e66809.
[61]JIANG X Z,LI D J,YANG J F,et al.Characterization of a novel human testis-specific gene:Testis developmental related gene 1(TDRG1)[J].Tohoku J Exp Med,2011,225(4):311-318.
[62]LAZAROS L,XITA N,KAPONIS A,et al.The association of aromatase(CYP19)gene variants with sperm concentration and motility[J].Asian J Androl,2011,13(2):292-297.
[63]YAO L,LI J L,FANG C C,et al.Genome-wide differential expression of genes and small RNAs in testis of two different porcine breeds and at two different ages[J].Sci Rep,2016,6:26852.
[64]LIU G,LEI B,LI Y,et al.Discovery of potential piRNAs from next generation sequences of the sexually mature porcine testes[J].PLoS One,2012,7(4):e34770.
[65]道楞.蒙古马睾丸发育及精子生成相关piRNA的鉴定及表达调控研究[D].呼和浩特:内蒙古农业大学,2017.DAO L.Identification and expression regulation of piRNA in Mongolian horse testis development and spermatogenesis[D].Hohhot:Inner Mongolia Agricultural University,2017.(in Chinese)
[66]PILLAI R S,CHUMA S.piRNAs and their involvement in male germline development in mice[J].Dev Growth Differ,2012,54(1):78-92.
[67]STALKER L,RUSSELL S J,CO C,et al.PIWIL1is expressed in the Canine testis,increases with sexual maturity,and binds small RNAs[J].Biol Reprod,2016,94(1):17.
[68]李玥,赵少志,江雪,等.恒河猴piwil1基因的表达[J].应用与环境生物学报,2012,18(1):60-64.LI Y,ZHAO S Z,JIANG X,et al.Expression of piwil1gene in Macaca mulatta[J].Chinese Journal of Applied&Environmental Biology,2012,18(1):60-64.(in Chinese)
[69]顾垚.黄牛、犏牛Piwi通路相关基因以及睾丸组织基因组甲基化分析[D].南京:南京农业大学,2012.GU Y.Methylation status of Piwi genes and genome in testis of cattle and cattle yaks[D].Nanjing:Nanjing Agricultural University,2012.(in Chinese)