Abstract
Dmrt7 is a member of the DM domain family of genes. Dmrt7 deficiency is also a strong candidate as a cause for male cattle-yak infertility, as it is regarded as essential for male spermatogenesis, between the pachynema and diplonema stages. In our study, the coding region sequence of yak and cattle-yak Dmrt7 was 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 Dmrt7 gene, encoding 370 amino acids, were consistent in yak and cattle-yak. The protein encoded by yak and cattle-yak Dmrt7 contains a DM domain. We detected Dmrt7 mRNA expression in testis, but not in any other tissue. Dmrt7 mRNA 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. Male cattle-yak testis contained a significantly larger number of apoptotic cells than those in cattle and yak assessed by terminal deoxynucleotidyl transferase dUTP nick end-labeling (TUNEL) analysis. The accumulation of SCP3-positive spermatocytes indicated the arrest of spermatogenesis at the pachynema stage in the cattle-yak. These results suggest low levels of Dmrt7 expression lead to male sterility in cattle-yak. The molecular function of Dmrt7 and the regulation of its expression warrant need to be examined in future studies.
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Fernandez-Capetillo O, Mahadevaiah SK, Celeste A, Romanienko PJ, Camerini-Otero RD, Bonner WM et al (2003) H2AX is required for chromatin remodeling and inactivation of sex chromosomes in male mouse meiosis. Dev Cell 4:497–508
Erdman SE, Burtis KC (1993) The Drosophila doublesex proteins share a novel zinc finger related DNA binding domain. EMBO J 12:527–535
Raymond CS, Shamu CE, Shen MM, Seifert KJ, Hirsch B, Hodgkin J et al (1998) Evidence for evolutionary conservation of sex-determining genes. Nature 391:691–695
Zarkower D (2001) Establishing sexual dimorphism: conservation amidst diversity? Nat Rev Genet 2:175–185
Kim S, Kettlewell JR, Anderson RC, Bardwell VJ, Zarkower D (2003) Sexually dimorphic expression of multiple doublesex-related genes in the embryonic mouse gonad. Gene Expr Patterns 3:77–82
Volff JN, Zarkower D, Bardwell VJ, Schartl M (2003) Evolutionary dynamics of the DM domain gene family in metazoans. J Mol Evol 57(Suppl 1):S241–S249
Veith AM, Klattig J, Dettai A, Schmidt C, Englert C, Volff JN (2006) Male-biased expression of X-chromosomal DM domain-less Dmrt8 genes in the mouse. Genomics 88:185–195
Raymond CS, Kettlewell JR, Hirsch B, Bardwell VJ, Zarkower D (1999) Expression of Dmrt1 in the genital ridge of mouse and chicken embryos suggests a role in vertebrate sexual development. Dev Biol 215:208–220
Smith CA, McClive PJ, Western PS, Reed KJ, Sinclair AH (1999) Conservation of a sex-determining gene. Nature 402:601–602
Kettlewell JR, Raymond CS, Zarkower D (2000) Temperature-dependent expression of turtle Dmrt1 prior to sexual differentiation. Genesis 26:174–178
Nanda I, Kondo M, Hornung U, Asakawa S, Winkler C, Shimizu A et al (2002) A duplicated copy of DMRT1 in the sex-determining region of the Y chromosome of the medaka, Oryzias latipes. Proc Natl Acad Sci USA 99:11778–11783
Matsuda M, Nagahama Y, Shinomiya A, Sato T, Matsuda C, Kobayashi T et al (2002) DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature 417:559–563
Meng A, Moore B, Tang H, Yuan B, Lin S (1999) A Drosophila doublesex-related gene, terra, is involved in somitogenesis in vertebrates. Development 126:1259–1268
Smith CA, Hurley TM, McClive PJ, Sinclair AH (2002) Restricted expression of DMRT3 in chicken and mouse embryos. Gene Expr Patterns 2:69–72
Liu S, Li Z, Gui JF (2009) Fish-specific duplicated dmrt2b contributes to a divergent function through Hedgehog pathway and maintains left–right asymmetry establishment function. PLoS One 4:e7261
Saude L, Lourenco R, Goncalves A, Palmeirim I (2005) Terra is a left–right asymmetry gene required for left–right synchronization of the segmentation clock. Nat Cell Biol 7:918–920
Huang X, Hong CS, O’Donnell M, Saint-Jeannet JP (2005) The doublesex-related gene, XDmrt4, is required for neurogenesis in the olfactory system. Proc Natl Acad Sci USA 102:11349–11354
Kawamata M, Nishimori K (2006) Mice deficient in Dmrt7 show infertility with spermatogenic arrest at pachytene stage. FEBS Lett 580:6442–6446
Kawamata M, Inoue H, Nishimori K (2007) Male-specific function of Dmrt7 by sexually dimorphic translation in mouse testis. Sex Dev 1:297–304
Kim S, Namekawa SH, Niswander LM, Ward JO, Lee JT, Bardwell VJ et al (2007) A mammal-specific doublesex homolog associates with male sex chromatin and is required for male meiosis. PLoS Genet 3:e62
Hou Y, Zhou X, Liu J, Yuan J, Cheng H, Zhou R (2010) 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 6:655–664
Moens PB, Kolas NK, Tarsounas M, Marcon E, Cohen PE, Spyropoulos B (2002) 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 115:1611–1622
Dobson MJ, Pearlman RE, Karaiskakis A, Spyropoulos B, Moens PB (1994) Synaptonemal complex proteins: occurrence, epitope mapping and chromosome disjunction. J Cell Sci 107(Pt 10):2749–2760
Wu S, Wolgemuth DJ (1995) The distinct and developmentally regulated patterns of expression of members of the mouse Cdc25 gene family suggest differential functions during gametogenesis. Dev Biol 170:195–206
Behringer RR, Crotty DA, Tennyson VM, Brinster RL, Palmiter RD, Wolgemuth DJ (1993) Sequences 5′ of the homeobox of the Hox-1.4 gene direct tissue-specific expression of lacZ during mouse development. Development 117:823–833
Rubin MR, Toth LE, Patel MD, D’Eustachio P, Nguyen-Huu MC (1986) A mouse homeo box gene is expressed in spermatocytes and embryos. Science 233:663–667
Zhang Q, Li J, Li Q, Li X, Liu Z, Song D et al (2009) Cloning and characterization of the gene encoding the bovine BOULE protein. Mol Genet Genomics 281:67–75
Date S, Nozawa O, Inoue H, Hidema S, Nishimori K (2012) Impairment of pachytene spermatogenesis in Dmrt7 deficient mice, possibly causing meiotic arrest. Biosci Biotechnol Biochem 76:1621–1626
Cohen PE, Pollack SE, Pollard JW (2006) Genetic analysis of chromosome pairing, recombination, and cell cycle control during first meiotic prophase in mammals. Endocr Rev 27:398–426
Acknowledgments
This research was supported by the Special Scientific Research Fund of Agriculture (201203008), Great Project of Science and Technology of Gansu Province in China (1102NKDA027) and Key Laboratory of Yak Breeding Engineering, Lanzhou Gansu Province (1106RTSA015).
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The authors declare that they have no conflict of interest.
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Ping Yan and Lin Xiang have contributed equally to this study.
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Yan, P., Xiang, L., Guo, X. et al. The low expression of Dmrt7 is associated with spermatogenic arrest in cattle-yak. Mol Biol Rep 41, 7255–7263 (2014). https://doi.org/10.1007/s11033-014-3611-x
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DOI: https://doi.org/10.1007/s11033-014-3611-x