Dmrt7低表达水平与犏牛精子发生阻滞相关性研究
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摘要
犏牛是牦牛和普通牛的杂交后代,杂种F1代犏牛具有很强的杂交优势,生产性能明显提高,但是F,代公犏牛不能正常产生精子,无法稳定遗传杂种优势,这成为牦牛杂交改良的一大难题,至今仍未能阐明犏牛雄性不育的分子机理。近年来的研究发现,Dmrt7作为Dmrt (doublesex and mab-3related transcriptional factor)基因家族的一员,在雄性特有的性染色体联会过程中扮演着关键角色。在本研究中,我们采用生物信息学方法对Dmrt7基因及其编码蛋白的功能位点和二级结构等方面进行了预测和分析,发现牦牛和犏牛Dmrt7基因编码区序列一致,编码370个氨基酸,具有完整的DM功能域；利用半定量PCR技术检测出Dmrt7mRNA仅在成年牛睾丸组织中表达,而未见于其它组织器官中；通过实时荧光定量PCR和Western Blot检测Dmrt7基因mRNA和蛋白在黄牛、牦牛和犏牛睾丸组织中的表达水平,发现mRNA与蛋白表达水平相一致,且犏牛睾丸组织中Dmrt7mRNA和蛋白的表达水平显著低于黄牛和牦牛(P<0.01)；同时我们通过H.E染色、免疫组织化学染色等手段对黄牛、牦牛和犏牛睾丸组织形态进行观察和比较,发现Fl代犏牛曲细精管高度滤泡化,仅含有少量生殖细胞,缺乏精子细胞,呈现明显的退化形态,减数分裂后期的生殖细胞出现明显缺失,犏牛的生殖细胞出现大量凋亡情况,生精过程被阻滞在粗线期后期。这些结果表明,Dmrt7作为减数分裂粗线期和双线期之间雄性特有的性染色体联会过渡中的一个关键因子,其表达水平的低下很有可能是犏牛染色体减数分裂障碍的原因之一。
Cattle-yak, the first hybrid generation of cattle and yak, shows obvious heterosis. However, F1male cattle-yak cannot produce sperm, which prevents the heterosis from being inherited. The inability of cattle-yak to produce sperm has become a major problem in the crossbreeding of yak, and the molecular mechanism for male cattle-yak sterility is not clear. Dmrt7, a member of the Dmrt (doublesex and mab-3related transcriptional factor) family of genes, plays an important role in male sex chromosome synapsis. In our study, the coding region sequence of yak and cattle-yak Dmrt7was cloned by molecular cloning techniques, and the sequence, conserved domains, functional sites, and secondary and tertiary structures of the Dmrt7-encoded protein were predicted and analyzed°using bioinformatics methods. The coding region sequences of the Dmrt7gene, encoding370amino acids, were consistent in yak and cattle-yak. The protein encoded by yak and cattle-yak Dmrt7contains a DM domain. We detected Dmrt7mRNA expression in the testis, but not in any other tissue tested. Dmrt7mRNA and protein expression was significantly higher in testis of cattle and yak than that in cattle-yak (P<0.01). Histological analysis indicated that seminiferous tubules in male cattle-yak were highly vacuolated and contained primarily Sertoli cells and spermatogonia, while those of cattle and yak contained abundant primary spermatocytes. The male cattle-yak testis contained a significantly larger number of apoptotic cells than those of cattle and yak, as assessed by TUNEL analysis. The accumulation of SCP3-positive spermatocytes indicated the arrest of spermatogenesis at the pachytene stage in the cattle-yak. These results suggest that low levels of Dmrt7expression lead to male sterility in cattle-yak.
Cattle-yak, the first hybrid generation of cattle and yak, shows obvious heterosis. However, F1male cattle-yak cannot produce sperm, which prevents the heterosis from being inherited. The inability of cattle-yak to produce sperm has become a major problem in the crossbreeding of yak, and the molecular mechanism for male cattle-yak sterility is not clear. Dmrt7, a member of the Dmrt (doublesex and mab-3related transcriptional factor) family of genes, plays an important role in male sex chromosome synapsis. In our study, the coding region sequence of yak and cattle-yak Dmrt7was cloned by molecular cloning techniques, and the sequence, conserved domains, functional sites, and secondary and tertiary structures of the Dmrt7-encoded protein were predicted and analyzed°using bioinformatics methods. The coding region sequences of the Dmrt7gene, encoding370amino acids, were consistent in yak and cattle-yak. The protein encoded by yak and cattle-yak Dmrt7contains a DM domain. We detected Dmrt7mRNA expression in the testis, but not in any other tissue tested. Dmrt7mRNA and protein expression was significantly higher in testis of cattle and yak than that in cattle-yak (P<0.01). Histological analysis indicated that seminiferous tubules in male cattle-yak were highly vacuolated and contained primarily Sertoli cells and spermatogonia, while those of cattle and yak contained abundant primary spermatocytes. The male cattle-yak testis contained a significantly larger number of apoptotic cells than those of cattle and yak, as assessed by TUNEL analysis. The accumulation of SCP3-positive spermatocytes indicated the arrest of spermatogenesis at the pachytene stage in the cattle-yak. These results suggest that low levels of Dmrt7expression lead to male sterility in cattle-yak.
引文
[1]Wiener G, Jianlin H, Ruijun L. The yak[M].FAO Regional Office for Asia and the Pacific,2003.
[2]阎萍,郭宪,梁春年等.牦牛的精子发生规律及繁殖特性[C].中国畜牧兽医学会动物繁殖学分会第15届学术研讨会论文集(下册),2010.
[3]郭宪,杨博辉,李勇生等.牦牛的生理生态特性.中国畜牧杂志,2006,42(1)：56-57.
[4]屈旭光,李齐发,刘振山等.牦牛、犏牛睾九组织中SYCP3基因mRNA表达水平研究.畜牧兽医学报,2008,39(8)：1132-1136.
[5]董丽艳,李齐发,屈旭光等.黄牛、牦牛和犏牛睾丸组织中Cdc2. Cdc25A基因mRNA表达水平.遗传,2009,31(5)：495-499.
[61李贤,李齐发,赵兴波等.牦牛和犏牛Dmcl基因序列分析及睾丸组织转录水平研究.中国农业科学,2010,43(15)：3221-3229.
[7]潘增祥,刘振山,李隐侠等.犏牛及其亲本睾丸组织中印记基因SNRPN DMR甲基化与mRNA表达差异研究.中国农业科学,2010,43(22)：4709-4716.
[8]李明桂,徐洪涛,李隐侠等.b-Boule基因5’调控序列的克隆与睾丸组织DMR甲基化分析.中国农业科学,2011,44(18)：3859-3867.
[9]胡欧明,钟金城,陈智华等.犏牛精母细胞联会复合体与雄性不育关系的研究.西南民族学院学报：自然科学版,2000,26(1)：61-66.
[10]Erdman S E, Burtis K C. The Drosophila doublesex proteins share a novel zinc finger related DNA binding domain. The Embo Journal,1993,12(2):527-535.
[11]Raymond C S, Shamu C E, Shen M M, et al. Evidence for evolutionary conservation of sex-determining genes. Nature,1998,391(6668):691-695.
[12]Zarkower D. Establishing sexual dimorphism:conservation amidst diversity? Nat Rev Genet,2001, 2(3):175-185.
[13]Lints R, Emmons S W. Regulation of sex-specific differentiation and mating behavior in C. elegans by a new member of the DM domain transcription factor family. Genes Dev,2002,16(18):2390-2402。
[14]Kondo M, Froschauer A, Kitano A, et al. Molecular cloning and characterization of DMRT genes from the medaka oryzias latipes and the platyfish xiphophorus maculatus. Gene,2002,295(2):213-222.
[15]Volff J N, Zarkower D, Bardwell V J, et al. Evolutionary dynamics of the DM domain gene family in metazoans. J Mol Evol,2003,57(Suppl.1):S241-S249.
[16]Brunner B, Hornung U, Shan Z, et al. Genomic organization and expression of the doublesex-related gene cluster in vertebrates and detection of putative regulatory regions for DMRT1. Genomics,2001, 77(1/2):8-17.
[17]Ottolenghi C, Fellous M, Barbieri M, et al. Novel paralogy relations among human chromosomes support a link between the phylogeny of doublesex-related genes and the evolution of sex determination. Genomics,2002,79(3):333-343.
[18]Kim S, Kettlewell J R, Anderson R C, et al. Sexually dimorphic expression of multiple doublesex-related genes in the embryonic mouse gonad. Gene Expr Patterns,2003,3(1):77-82.
[19]Veith A M, Klattig J, Dettai A, et al. Male-biased expression of X-chromosomal DM domain-less Dmrt8 genes in the mouse. Genomics,2006,88(2):185-195.
[20]Heard E, Disteche C M. Dosage compensation in mammals:fine-tuning the expression of the X chromosome. Genes Dev,2006,20(14):1848-1867.
[21]Huynh K D, Lee J T. X-chromosome inactivation:a hypothesis linking ontogeny and phylogeny. Nat Rev Genet,2005,6(5):410-418.
[22]McK.ee B D, Handel M A. Sex chromosomes, recombination, and chromatin conformation. Chromosoma,1993,102(2):71-80.
[23]Mahadevaiah S K, Turner J M, Baudat F, et al. Recombinational DNA double-strand breaks in mice precede synapsis. Nat Genet,2001,27(3):271-276.
[24]Jablonka E, Lamb M J. Meiotic pairing constraints and the activity of sex chromosomes. J Theor Biol, 1988,133(1):23-36.
[25]Odorisio T, Rodriguez T A, Evans E P, et al. The meiotic checkpoint monitoring synapsis eliminates spermatocytes via p53-independent apoptosis. Nat Genet,1998,18(3):257-261.
[26]Hoyer-Fender S. Molecular aspects of XY body formation. Cytogenet Genome Res,2003,103(3/4): 245-25.
[27]Fernandez-Capetillo O, Mahadevaiah S K, Celeste A, et al. H2AX is required for chromatin remodeling and inactivation of sex chromosomes in male mouse meiosis. Dev Cell,2003,4(4):497-508.
[28]Kim S, Namekawa S H, Niswander L M, et al. A mammal-specific doublesex homolog associates with male sex chromatin and is required for male meiosis. PLoS Genetics,2007,3(4):e62.
[29]Kawamata M, Nishimori K. Mice deficient in Dmrt7 show infertility with spermatogenic arrest at pachytene stage. FEBS Lett,2006,580(27):6442-6446.
[30]Zhang Q, Li J, Li Q, et al. Cloning and characterization of the gene encoding the bovine BOULE protein. Mol Genet Genomics,2009,281(1):67-75.
[31]Moens P B, Kolas N K, Tarsounas M, et al. The time course and chromosomal localization of recombination-related proteins at meiosis in the mouse are compatible with models that can resolve the early DNA-DNA interactions without reciprocal recombination. J Cell Sci,2002,115:1611-1622.
[32]Dobson M J, Pearlman R E, Karaiskakis A, et al. Synaptonemal complex proteins:occurrence, epitope mapping and chromosome disjunction. J Cell Sci,1994,107 (Pt 10):2749-2760.
[33]Wu S, Wolgemuth D J. The distinct and developmentally regulated patterns of expression of members of the mouse Cdc25 gene family suggest differential functions during gametogenesis. Dev Biol, 1995,170:195-206
[34]Behringer R R, Crotty D A, Tennyson V M, et al. Sequences 5' of the homeobox of the Hox-1.4 gene direct tissue-specific expression of lacZ during mouse development. Development,1993,117:823-833.
[35]Cohen P E, Pollack S E, Pollard J W. Genetic analysis of chromosome pairing, recombination, and cell cycle control during first meiotic prophase in mammals. Endocr Rev,2006,27(4):398-426.
[36]Roeder G S, Bailis J M. The pachytene checkpoint. Trends Genet,2000,16(9):395-403.
[37]Date S, Nozawa O, Inoue H, et al. Impairment of pachytene spermatogenesis in Dmrt7 deficient mice, possibly causing meiotic arrest. Biosci Biotechnol Biochem,2012,76:1621-1626.
[38]Hou Y, Zhou X, Liu J, et al. Nuclear factor-Y (NF-Y) regulates transcription of mouse Dmrt7 gene by binding to tandem CCAAT boxes in its proximal promoter. Int J Biol Sci,2010,6(7):655-664.
[1]Erdman S E, Burtis K C. The Drosophila doublesex proteins share a novel zinc finger related DNA binding domain. EMBO J,1993,12(2):527-535.
[2]Raymond C S, Shamu C E, Shen M M, et al. Evidence for evolutionary conservation of sex-determining genes. Nature,1998,391(6668):691-695.
[3]Zarkower D. Establishing sexual dimorphism:conservation amidst diversity? Nature Reviews Genetics,2001,2(3):175-185.
[4]Matsuda M, Nagahama Y, Shinomiya A, et al. DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature,2002,417(6888):559-563.
[5]Raymond C S, Kettlewell J R, Hirsch B, et al. Expression of Dmrtl in the genital ridge of mouse and chicken embryos suggests a role in vertebrate sexual development. Dev Biol,1999,215(2):208-220.
[6]Raymond C S, Murphy M W, O'Sullivan, et al. Dmrtl, a gene related to worm and fly sexual regulators, is required for mammalian testis differentiation. Genes Dev,2000,14(20):2587-2595.
[7]Seo, K W, Wang Y, Kokubo H, et al. Targeted disruption of the DM domain containing transcription factor Dmrt2 reveals an essential role in somite patterning. Dev Biol,2006,290(1):200-210.
[8]Smith C A, Hurley T M, McClive P J, et al. Restricted expression of DMRT3 in chicken and mouse embryos. Gene Expr Patterns,2002,2(1-2):69-72.
[9]Li Q, Zhou X, Guo Y, et al. Nuclear localization, DNA binding and restricted expression in neural and germ cells of zebrafish Dmrt3. Biol Cell,2008,100(8):453-463.
[10]Huang X, Hong C S, O'Donnell M, et al. The doublesex-related gene, XDmrt4, is required for neurogenesis in the olfactory system. Proc Natl Acad Sci U S A,2005,102(32):11349-11354.
[11]Kim S, Kettlewell J R, Anderson R C, et al. Sexually dimorphic expression of multiple doublesex-related genes in the embryonic mouse gonad. Gene Expr Patterns,2003,3(1):77-82.
[12]Guo Y, Li Q, Gao S, et al. Molecular cloning, characterization, and expression in brain and gonad of Dmrt5 of zebrafish. Biochem Biophys Res Commun,2004,324(2):569-575.
[13]Veith A M, Klattig J, Dettai A, et al. Male-biased expression of X-chromosomal DM domain-less Dmrt8 genes in the mouse. Genomics,2006,88(2):185-195.
[14]Cohen P E, Pollack S E, Pollard J W. Genetic analysis of chromosome pairing, recombination, and cell cycle control during first meiotic prophase in mammals. Endocr Rev,2006,27(4):398-426.
[15]Kim S, Namekawa S H, Niswander L M, et al. A mammal-specific doublesex homolog associates with male sex chromatin and is required for male meiosis. PLoS Genetics,2007,3(4):e62.
[16]McKee B D, Handel M A. Sex chromosomes, recombination, and chromatin conformation. Chromosoma,1993,102(2):71-80.
[17]Mahadevaiah S K, Turner J M, Baudat F, et al. Recombinational DNA double-strand breaks in mice precede synapsis. Nat Genet,2001,27(3):271-276.
[18]Jablonka E, Lamb M J. Meiotic pairing constraints and the activity of sex chromosomes. J Theor Biol, 1988,133(1):23-36.
[19]Odorisio T, Rodriguez T A, Evans E P, et al. The meiotic checkpoint monitoring synapsis eliminates spermatocytes via p53-independent apoptosis. Nat Genet,1998,18(3):257-261.
[20]Hoyer-Fender S. Molecular aspects of XY body formation. Cytogenet Genome Res,2003,103(3/4): 245-255.
[21]Fernandez-Capetillo O. Mahadevaiah S K, Celeste A, et al. H2AX is required for chromatin remodeling and inactivation of sex chromosomes in male mouse meiosis. Dev Cell,2003,4(4): 497-508.
[22]Hou Y, Zhou X, Liu J, et al. Nuclear factor-Y (NF-Y) regulates transcription of mouse Dmrt7 gene by binding to tandem CCAAT boxes in its proximal promoter. Int J Biol Sci,2010,6(7):655-664.
[2]阎萍,郭宪,梁春年等.牦牛的精子发生规律及繁殖特性[C].中国畜牧兽医学会动物繁殖学分会第15届学术研讨会论文集(下册),2010.
[3]郭宪,杨博辉,李勇生等.牦牛的生理生态特性.中国畜牧杂志,2006,42(1)：56-57.
[4]屈旭光,李齐发,刘振山等.牦牛、犏牛睾九组织中SYCP3基因mRNA表达水平研究.畜牧兽医学报,2008,39(8)：1132-1136.
[5]董丽艳,李齐发,屈旭光等.黄牛、牦牛和犏牛睾丸组织中Cdc2. Cdc25A基因mRNA表达水平.遗传,2009,31(5)：495-499.
[61李贤,李齐发,赵兴波等.牦牛和犏牛Dmcl基因序列分析及睾丸组织转录水平研究.中国农业科学,2010,43(15)：3221-3229.
[7]潘增祥,刘振山,李隐侠等.犏牛及其亲本睾丸组织中印记基因SNRPN DMR甲基化与mRNA表达差异研究.中国农业科学,2010,43(22)：4709-4716.
[8]李明桂,徐洪涛,李隐侠等.b-Boule基因5’调控序列的克隆与睾丸组织DMR甲基化分析.中国农业科学,2011,44(18)：3859-3867.
[9]胡欧明,钟金城,陈智华等.犏牛精母细胞联会复合体与雄性不育关系的研究.西南民族学院学报：自然科学版,2000,26(1)：61-66.
[10]Erdman S E, Burtis K C. The Drosophila doublesex proteins share a novel zinc finger related DNA binding domain. The Embo Journal,1993,12(2):527-535.
[11]Raymond C S, Shamu C E, Shen M M, et al. Evidence for evolutionary conservation of sex-determining genes. Nature,1998,391(6668):691-695.
[12]Zarkower D. Establishing sexual dimorphism:conservation amidst diversity? Nat Rev Genet,2001, 2(3):175-185.
[13]Lints R, Emmons S W. Regulation of sex-specific differentiation and mating behavior in C. elegans by a new member of the DM domain transcription factor family. Genes Dev,2002,16(18):2390-2402。
[14]Kondo M, Froschauer A, Kitano A, et al. Molecular cloning and characterization of DMRT genes from the medaka oryzias latipes and the platyfish xiphophorus maculatus. Gene,2002,295(2):213-222.
[15]Volff J N, Zarkower D, Bardwell V J, et al. Evolutionary dynamics of the DM domain gene family in metazoans. J Mol Evol,2003,57(Suppl.1):S241-S249.
[16]Brunner B, Hornung U, Shan Z, et al. Genomic organization and expression of the doublesex-related gene cluster in vertebrates and detection of putative regulatory regions for DMRT1. Genomics,2001, 77(1/2):8-17.
[17]Ottolenghi C, Fellous M, Barbieri M, et al. Novel paralogy relations among human chromosomes support a link between the phylogeny of doublesex-related genes and the evolution of sex determination. Genomics,2002,79(3):333-343.
[18]Kim S, Kettlewell J R, Anderson R C, et al. Sexually dimorphic expression of multiple doublesex-related genes in the embryonic mouse gonad. Gene Expr Patterns,2003,3(1):77-82.
[19]Veith A M, Klattig J, Dettai A, et al. Male-biased expression of X-chromosomal DM domain-less Dmrt8 genes in the mouse. Genomics,2006,88(2):185-195.
[20]Heard E, Disteche C M. Dosage compensation in mammals:fine-tuning the expression of the X chromosome. Genes Dev,2006,20(14):1848-1867.
[21]Huynh K D, Lee J T. X-chromosome inactivation:a hypothesis linking ontogeny and phylogeny. Nat Rev Genet,2005,6(5):410-418.
[22]McK.ee B D, Handel M A. Sex chromosomes, recombination, and chromatin conformation. Chromosoma,1993,102(2):71-80.
[23]Mahadevaiah S K, Turner J M, Baudat F, et al. Recombinational DNA double-strand breaks in mice precede synapsis. Nat Genet,2001,27(3):271-276.
[24]Jablonka E, Lamb M J. Meiotic pairing constraints and the activity of sex chromosomes. J Theor Biol, 1988,133(1):23-36.
[25]Odorisio T, Rodriguez T A, Evans E P, et al. The meiotic checkpoint monitoring synapsis eliminates spermatocytes via p53-independent apoptosis. Nat Genet,1998,18(3):257-261.
[26]Hoyer-Fender S. Molecular aspects of XY body formation. Cytogenet Genome Res,2003,103(3/4): 245-25.
[27]Fernandez-Capetillo O, Mahadevaiah S K, Celeste A, et al. H2AX is required for chromatin remodeling and inactivation of sex chromosomes in male mouse meiosis. Dev Cell,2003,4(4):497-508.
[28]Kim S, Namekawa S H, Niswander L M, et al. A mammal-specific doublesex homolog associates with male sex chromatin and is required for male meiosis. PLoS Genetics,2007,3(4):e62.
[29]Kawamata M, Nishimori K. Mice deficient in Dmrt7 show infertility with spermatogenic arrest at pachytene stage. FEBS Lett,2006,580(27):6442-6446.
[30]Zhang Q, Li J, Li Q, et al. Cloning and characterization of the gene encoding the bovine BOULE protein. Mol Genet Genomics,2009,281(1):67-75.
[31]Moens P B, Kolas N K, Tarsounas M, et al. The time course and chromosomal localization of recombination-related proteins at meiosis in the mouse are compatible with models that can resolve the early DNA-DNA interactions without reciprocal recombination. J Cell Sci,2002,115:1611-1622.
[32]Dobson M J, Pearlman R E, Karaiskakis A, et al. Synaptonemal complex proteins:occurrence, epitope mapping and chromosome disjunction. J Cell Sci,1994,107 (Pt 10):2749-2760.
[33]Wu S, Wolgemuth D J. The distinct and developmentally regulated patterns of expression of members of the mouse Cdc25 gene family suggest differential functions during gametogenesis. Dev Biol, 1995,170:195-206
[34]Behringer R R, Crotty D A, Tennyson V M, et al. Sequences 5' of the homeobox of the Hox-1.4 gene direct tissue-specific expression of lacZ during mouse development. Development,1993,117:823-833.
[35]Cohen P E, Pollack S E, Pollard J W. Genetic analysis of chromosome pairing, recombination, and cell cycle control during first meiotic prophase in mammals. Endocr Rev,2006,27(4):398-426.
[36]Roeder G S, Bailis J M. The pachytene checkpoint. Trends Genet,2000,16(9):395-403.
[37]Date S, Nozawa O, Inoue H, et al. Impairment of pachytene spermatogenesis in Dmrt7 deficient mice, possibly causing meiotic arrest. Biosci Biotechnol Biochem,2012,76:1621-1626.
[38]Hou Y, Zhou X, Liu J, et al. Nuclear factor-Y (NF-Y) regulates transcription of mouse Dmrt7 gene by binding to tandem CCAAT boxes in its proximal promoter. Int J Biol Sci,2010,6(7):655-664.
[1]Erdman S E, Burtis K C. The Drosophila doublesex proteins share a novel zinc finger related DNA binding domain. EMBO J,1993,12(2):527-535.
[2]Raymond C S, Shamu C E, Shen M M, et al. Evidence for evolutionary conservation of sex-determining genes. Nature,1998,391(6668):691-695.
[3]Zarkower D. Establishing sexual dimorphism:conservation amidst diversity? Nature Reviews Genetics,2001,2(3):175-185.
[4]Matsuda M, Nagahama Y, Shinomiya A, et al. DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature,2002,417(6888):559-563.
[5]Raymond C S, Kettlewell J R, Hirsch B, et al. Expression of Dmrtl in the genital ridge of mouse and chicken embryos suggests a role in vertebrate sexual development. Dev Biol,1999,215(2):208-220.
[6]Raymond C S, Murphy M W, O'Sullivan, et al. Dmrtl, a gene related to worm and fly sexual regulators, is required for mammalian testis differentiation. Genes Dev,2000,14(20):2587-2595.
[7]Seo, K W, Wang Y, Kokubo H, et al. Targeted disruption of the DM domain containing transcription factor Dmrt2 reveals an essential role in somite patterning. Dev Biol,2006,290(1):200-210.
[8]Smith C A, Hurley T M, McClive P J, et al. Restricted expression of DMRT3 in chicken and mouse embryos. Gene Expr Patterns,2002,2(1-2):69-72.
[9]Li Q, Zhou X, Guo Y, et al. Nuclear localization, DNA binding and restricted expression in neural and germ cells of zebrafish Dmrt3. Biol Cell,2008,100(8):453-463.
[10]Huang X, Hong C S, O'Donnell M, et al. The doublesex-related gene, XDmrt4, is required for neurogenesis in the olfactory system. Proc Natl Acad Sci U S A,2005,102(32):11349-11354.
[11]Kim S, Kettlewell J R, Anderson R C, et al. Sexually dimorphic expression of multiple doublesex-related genes in the embryonic mouse gonad. Gene Expr Patterns,2003,3(1):77-82.
[12]Guo Y, Li Q, Gao S, et al. Molecular cloning, characterization, and expression in brain and gonad of Dmrt5 of zebrafish. Biochem Biophys Res Commun,2004,324(2):569-575.
[13]Veith A M, Klattig J, Dettai A, et al. Male-biased expression of X-chromosomal DM domain-less Dmrt8 genes in the mouse. Genomics,2006,88(2):185-195.
[14]Cohen P E, Pollack S E, Pollard J W. Genetic analysis of chromosome pairing, recombination, and cell cycle control during first meiotic prophase in mammals. Endocr Rev,2006,27(4):398-426.
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