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Testicular Development and Spermatogenesis: Harvesting the Postgenomics Bounty

  • Antoine D. Rolland
  • Bernard Jégou
  • Charles PineauEmail author
Part of the Advances in Experimental Medicine and Biology book series (volume 636)

Abstract

Spermatogenesis is a sophisticated process facilitating transmission of the genetic patrimony and, thus, perpetuation of the species. Mammalian spermatogenesis is classically divided into three 3 phases. In the first—the proliferative or mitotic phase—primitive germ cells or spermatogonia undergo a series of mitotic divisions. In the second—the meiotic phase—the spermatocytes undergo two consecutive divisions to produce the haploid spermatids. In the third—spermiogenesis—spermatids differentiate into spermatozoa. The entire process is regulated by paracrine, autocrine and endocrine pathways, an array of structural elements and chemical factors modulating somatic and germ cell activity (for reviews, see refs. 1–4). The communication network linking the various cellular activities during spermatogenesis is highly complex and sophisticated5, 6.

Keywords

Germ Cell Androgen Receptor Sertoli Cell Leydig Cell Spermatogonial Stem Cell 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. 1.
    Jégou B. The Sertoli-germ cell communication network in mammals. Int Rev Cytol 1993; 147:25–96.PubMedCrossRefGoogle Scholar
  2. 2.
    Jégou B, Sharpe RM. Paracrine mechanisms in testicular control. In: deKretser DM, ed. Molecular Biology of the Male Reproduction System. New York: Academic Press, 1993:271–310.Google Scholar
  3. 3.
    Sharpe RM. Regulation of spermatogenesis. In: Knobil E, Neill JD, eds. The Physiology of Reproduction. 2nd ed. New York: Lippincott Williams & Wilkins, 1994:1363–1436.Google Scholar
  4. 4.
    Zhao GQ, Garbers DL. Male germ cell specification and differentiation. Dev Cell 2002; 2:537–547.PubMedCrossRefGoogle Scholar
  5. 5.
    Gnessi L, Fabbri A, Spera G. Gonadal peptides as mediators of development and functional control of the testis: An integrated system with hormones and local environment. Endocr Rev 1997; 18:541–609.PubMedCrossRefGoogle Scholar
  6. 6.
    Jégou B, Pineau C, Dupaix A. Paracrine control of testis function. In: Wang C, ed. Male Reproductive Function. Endocrine Update Series. Berlin: Kluwer Academic, 1999:41–64.CrossRefGoogle Scholar
  7. 7.
    Matzuk MM, Lamb DJ. Genetic dissection of mammalian fertility pathways. Nat Cell Biol 2002; 4:s41–49.CrossRefGoogle Scholar
  8. 8.
    de Rooij DG, de Boer P. Specific arrests of spermatogenesis in genetically modified and mutant mice. Cytogenet Genome Res 2003; 103:267–276.PubMedCrossRefGoogle Scholar
  9. 9.
    Wrobel G, Primig M. Mammalian male germ cells are fertile ground for expression profiling of sexual reproduction. Reproduction 2005; 129:1–7.PubMedCrossRefGoogle Scholar
  10. 10.
    Huang SY, Lin JH, Chen YH et al. A reference map and identification of porcine testis proteins using 2-DE and MS. Proteomics 2005; 5:4205–4212.PubMedCrossRefGoogle Scholar
  11. 11.
    Com E, Evrard B, Roepstorff P et al. New insights into the rat spermatogonial proteome: Identification of 156 additional proteins. Mol Cell Proteomics 2003; 2:248–261.PubMedGoogle Scholar
  12. 12.
    Essader AS, Cargile BJ, Bundy JL et al. A comparison of immobilized pH gradient isoelectric focusing and strong-cation-exchange chromatography as a first dimension in shotgun proteomics. Proteomics 2005; 5:24–34.PubMedCrossRefGoogle Scholar
  13. 13.
    Rolland AD, Evrard B, Guitton N et al. Two-dimensional fluorescence difference gel electrophoresis analysis of spermatogenesis in the rat. J Proteome Res 2007; 6:683–697.PubMedCrossRefGoogle Scholar
  14. 14.
    Wilkins MR, Sanchez JC, Gooley AA et al. Progress in proteome projects: Why all proteins expressed by a genome should be identified and how to do it. Biotechnol Genet Eng Rev 1995; 13:19–50.Google Scholar
  15. 15.
    Aebersold R, Mann M. Mass spectrometry-based proteomics. Nature 2003; 422:198–207.PubMedCrossRefGoogle Scholar
  16. 16.
    Waterston RH, Lindblad-Toh K, Birney E et al. Initial sequencing and comparative analysis of the mouse genome. Nature 2002; 420:520–562.PubMedCrossRefGoogle Scholar
  17. 17.
    Lander ES, Linton LM, Birren B et al. Initial sequencing and analysis of the human genome. Nature 2001; 409:860–921.PubMedCrossRefGoogle Scholar
  18. 18.
    Venter JC, Adams MD, Myers EW et al. The sequence of the human genome. Science 2001; 291:1304–1351.PubMedCrossRefGoogle Scholar
  19. 19.
    Hubbard TJ, Aken BL, Beal K et al. Ensembl 2007. Nucleic Acids Res 2007; 35:D610–617.PubMedCrossRefGoogle Scholar
  20. 20.
    Modrek B, Resch A, Grasso C et al. Genome-wide detection of alternative splicing in expressed sequences of human genes. Nucleic Acids Res 2001; 29:2850–2859.PubMedCrossRefGoogle Scholar
  21. 21.
    Johnson JM, Castle J, Garrett-Engele P et al. Genome-wide survey of human alternative pre-mRNA splicing with exon junction microarrays. Science 2003; 302:2141–2144.PubMedCrossRefGoogle Scholar
  22. 22.
    Mann M, Jensen ON. Proteomic analysis of post-translational modifications. Nat Biotechnol 2003; 21:255–261.PubMedCrossRefGoogle Scholar
  23. 23.
    Kettman JR, Coleclough C, Frey JR et al. Clonal proteomics: One gene—Family of proteins. Proteomics 2002; 2:624–631.PubMedCrossRefGoogle Scholar
  24. 24.
    Humphery-Smith I. A human proteome project with a beginning and an end. Proteomics 2004; 4:2519–2521.PubMedCrossRefGoogle Scholar
  25. 25.
    Mueller M, Martens L, Apweiler R. Annotating the human proteome: Beyond establishing a parts list. Biochim Biophys Acta 2007; 1774:175–191.PubMedGoogle Scholar
  26. 26.
    Conrads KA, Yi M, Simpson KA et al. A combined proteome and microarray investigation of inorganic phosphate-induced preosteoblast cells. Mol Cell Proteomics 2005; 4:1284–1296.PubMedCrossRefGoogle Scholar
  27. 27.
    Chen G, Gharib TG, Huang CC et al. Discordant protein and mRNA expression in lung adenocarcinomas. Mol Cell Proteomics 2002; 1:304–313.PubMedCrossRefGoogle Scholar
  28. 28.
    Gygi SP, Rochon Y, Franza BR et al. Correlation between protein and mRNA abundance in yeast. Mol Cell Biol 1999; 19:1720–1730.PubMedGoogle Scholar
  29. 29.
    Small CL, Shima JE, Uzumcu M et al. Profiling gene expression during the differentiation and development of the murine embryonic gonad. Biol Reprod 2005; 72:492–501.PubMedCrossRefGoogle Scholar
  30. 30.
    Nef S, Schaad O, Stallings NR et al. Gene expression during sex determination reveals a robust female genetic program at the onset of ovarian development. Dev Biol 2005; 287:361–377.PubMedCrossRefGoogle Scholar
  31. 31.
    Beverdam A, Koopman P. Expression profiling of purified mouse gonadal somatic cells during the critical time window of sex determination reveals novel candidate genes for human sexual dysgenesis syndromes. Hum Mol Genet 2006; 15:417–431.PubMedCrossRefGoogle Scholar
  32. 32.
    Wilhelm D, Huang E, Svingen T et al. Comparative proteomic analysis to study molecular events during gonad development in mice. Genesis 2006; 44:168–176.PubMedCrossRefGoogle Scholar
  33. 33.
    Han BK, Kim JN, Shin JH et al. Proteome analysis of chicken embryonic gonads: Identification of major proteins from cultured gonadal primordial germ cells. Mol Reprod Dev 2005; 72:521–529.PubMedCrossRefGoogle Scholar
  34. 34.
    Guillaume E, Dupaix A, Moertz E et al. Proteome analysis of spermatogonia: Identification of a first set of 53 spermatogonial proteins. Proteome 2000, in press.Google Scholar
  35. 35.
    Ito T, Chiba T, Ozawa R et al. A comprehensive two-hybrid analysis to explore the yeast protein interactome. Proc Natl Acad Sci USA 2001; 98:4569–4574.PubMedCrossRefGoogle Scholar
  36. 36.
    Hamra FK, Schultz N, Chapman KM et al. Defining the spermatogonial stem cell. Dev Biol 2004; 269:393–410.PubMedCrossRefGoogle Scholar
  37. 37.
    Oatley JM, Avarbock MR, Telaranta AI et al. Identifying genes important for spermatogonial stem cell self-renewal and survival. Proc Natl Acad Sci USA 2006; 103:9524–9529.PubMedCrossRefGoogle Scholar
  38. 38.
    Costoya JA, Hobbs RM, Barna M et al. Essential role of Plzf in maintenance of spermatogonial stem cells. Nat Genet 2004; 36:653–659.PubMedCrossRefGoogle Scholar
  39. 39.
    Chen C, Ouyang W, Grigura V et al. ERM is required for transcriptional control of the spermatogonial stem cell niche. Nature 2005; 436:1030–1034.PubMedCrossRefGoogle Scholar
  40. 40.
    Hofmann MC, Braydich-Stolle L, Dym M. Isolation of male germ-line stem cells; influence of GDNF. Dev Biol 2005; 279:114–124.PubMedCrossRefGoogle Scholar
  41. 41.
    Chu DS, Liu H, Nix P et al. Sperm chromatin proteomics identifies evolutionarily conserved fertility factors. Nature 2006; 443:101–105.PubMedCrossRefGoogle Scholar
  42. 42.
    Govin J, Caron C, Escoffier E et al. Post-meiotic shifts in HSPA2/HSP70.2 chaperone activity during mouse spermatogenesis. J Biol Chem 2006; 281:37888–37892.PubMedCrossRefGoogle Scholar
  43. 43.
    Zhu YF, Cui YG, Guo XJ et al. Proteomic analysis of effect of hyperthermia on spermatogenesis in adult male mice. J Proteome Res 2006; 5:2217–2225.PubMedCrossRefGoogle Scholar
  44. 44.
    Reinke V, Smith HE, Nance J et al. A global profile of germline gene expression in C. elegans. Mol Cell 2000; 6:605–616.PubMedCrossRefGoogle Scholar
  45. 45.
    Divina P, Vlcek C, Strnad P et al. Global transcriptome analysis of the C57BL/6J mouse testis by SAGE: Evidence for nonrandom gene order. BMC Genomics 2005; 6:29.PubMedCrossRefGoogle Scholar
  46. 46.
    Yao J, Chiba T, Sakai J et al. Mouse testis transcriptome revealed using serial analysis of gene expression. Mamm Genome 2004; 15:433–451.PubMedCrossRefGoogle Scholar
  47. 47.
    Fox MS, Ares VX, Turek PJ et al. Feasibility of global gene expression analysis in testicular biopsies from infertile men. Mol Reprod Dev 2003; 66:403–421.PubMedCrossRefGoogle Scholar
  48. 48.
    Wu SM, Baxendale V, Chen Y et al. Analysis of mouse germ-cell transcriptome at different stages of spermatogenesis by SAGE: Biological significance. Genomics 2004; 84:971–981.PubMedCrossRefGoogle Scholar
  49. 49.
    Shima JE, McLean DJ, McCarrey JR et al. The murine testicular transcriptome: Characterizing gene expression in the testis during the progression of spermatogenesis. Biol Reprod 2004; 71:319–330.PubMedCrossRefGoogle Scholar
  50. 50.
    Namekawa SH, Park PJ, Zhang LF et al. Postmeiotic sex chromatin in the male germline of mice. Curr Biol 2006; 16:660–667.PubMedCrossRefGoogle Scholar
  51. 51.
    Chalmel F, Rolland AD, Niederhauser-Wiederkehr C et al. The conserved transcriptome in human and rodent male gametogenesis. Proc Natl Acad Sci USA 2007; 104:8346–8351.PubMedCrossRefGoogle Scholar
  52. 52.
    Schlecht U, Demougin P, Koch R et al. Expression profiling of mammalian male meiosis and gametogenesis identifies novel candidate genes for roles in the regulation of fertility. Mol Biol Cell 2004; 15:1031–1043.PubMedCrossRefGoogle Scholar
  53. 53.
    Almstrup K, Nielsen JE, Hansen MA et al. Analysis of cell-type-specific gene expression during mouse spermatogenesis. Biol Reprod 2004; 70:1751–1761.PubMedCrossRefGoogle Scholar
  54. 54.
    Ellis PJ, Furlong RA, Wilson A et al. Modulation of the mouse testis transcriptome during postnatal development and in selected models of male infertility. Mol Hum Reprod 2004; 10:271–281.PubMedCrossRefGoogle Scholar
  55. 55.
    Clemente EJ, Furlong RA, Loveland KL et al. Gene expression study in the juvenile mouse testis: Identification of stage-specific molecular pathways during spermatogenesis. Mamm Genome 2006; 17:956–975.PubMedCrossRefGoogle Scholar
  56. 56.
    Schultz N, Hamra FK, Garbers DL. A multitude of genes expressed solely in meiotic or postmeiotic spermatogenic cells offers a myriad of contraceptive targets. Proc Natl Acad Sci USA 2003; 100:12201–12206.PubMedCrossRefGoogle Scholar
  57. 57.
    O’Shaughnessy PJ, Fleming L, Baker PJ et al. Identification of developmentally regulated genes in the somatic cells of the mouse testis using serial analysis of gene expression. Biol Reprod 2003; 69:797–808.PubMedCrossRefGoogle Scholar
  58. 58.
    Ge RS, Dong Q, Sottas CM et al. Gene expression in rat leydig cells during development from the progenitor to adult stage: A cluster analysis. Biol Reprod 2005; 72:1405–1415.PubMedCrossRefGoogle Scholar
  59. 59.
    Ellis PJ, Clemente EJ, Ball P et al. Deletions, on mouse Yq lead to upregulation of multiple X-and Y-linked transcripts in spermatids. Hum Mol Genet 2005; 14:2705–2715.PubMedCrossRefGoogle Scholar
  60. 60.
    Toure A, Clemente EJ, Ellis P et al. Identification of novel Y chromosome encoded transcripts by testis transcriptome analysis of mice with deletions of the Y chromosome long arm. Genome Biol 2005; 6:R102.PubMedCrossRefGoogle Scholar
  61. 61.
    Beissbarth T, Borisevich I, Horlein A et al. Analysis of CREM-dependent gene expression during mouse spermatogenesis. Mol Cell Endocrinol 2003; 212:29–39.PubMedCrossRefGoogle Scholar
  62. 62.
    Chaudhary J, Sadler-Riggleman I, Ague JM et al. The helix-loop-helix inhibitor of differentiation (ID) proteins induce post-mitotic terminally differentiated Sertoli cells to reenter the cell cycle and proliferate. Biol Reprod 2005; 72:1205–1217.PubMedCrossRefGoogle Scholar
  63. 63.
    Cheng Y, Buffone MG, Kouadio M et al. Abnormal sperm in mice lacking the Taf71 gene. Mol Cell Biol 2007; 27:2582–9.PubMedCrossRefGoogle Scholar
  64. 64.
    Cagney G, Park S, Chung C et al. Human tissue profiling with multidimensional protein identification technology. J Proteome Res 2005; 4:1757–1767.PubMedCrossRefGoogle Scholar
  65. 65.
    Iguchi N, Tobias JW, Hecht NB. Expression profiling reveals meiotic male germ cell mRNAs that are translationally up-and down-regulated. Proc Natl Acad Sci USA 2006; 103:7712–7717.PubMedCrossRefGoogle Scholar
  66. 66.
    Ostermeier GC, Dix DJ, Miller D et al. Spermatozoal RNA profiles of normal fertile men. Lancer 2002; 360:772–777.CrossRefGoogle Scholar
  67. 67.
    Ostermeier GC, Goodrich RJ, Moldenhauer JS et al. A suite of novel human spermatozoal RNAs. J Androl 2005; 26:70–74.PubMedGoogle Scholar
  68. 68.
    Wang H, Zhou Z, Xu M et al. A spermatogenesis-related gene expression profile in human spermatozoa and its potential clinical applications. J Mol Med 2004; 82:317–324.PubMedCrossRefGoogle Scholar
  69. 69.
    Zhao Y, Li Q, Yao C et al. Characterization and quantification of mRNA transcripts in ejaculated spermatozoa of fertile men by serial analysis of gene expression. Hum Reprod 2006; 21:1583–1590.PubMedCrossRefGoogle Scholar
  70. 70.
    Martinez-Heredia J, Estanyol JM, Ballesca JL et al. Proteomic identification of human sperm proteins. Proteomics 2006; 6:4356–4369.PubMedCrossRefGoogle Scholar
  71. 71.
    Johnston DS, Wooters J, Kopf GS et al. Analysis of the human sperm proteome. Ann NY Acad Sci 2005; 1061:190–202.PubMedCrossRefGoogle Scholar
  72. 72.
    Dorus S, Busby SA, Gerike U et al. Genomic and functional evolution of the Drosophila melanogaster sperm proteome. Nat Genet 2006; 38:1440–1445.PubMedCrossRefGoogle Scholar
  73. 73.
    Anderson NL, Anderson NG. Proteome and proteomics: New technologies, new concepts, and new words. Electrophoresis 1998; 19:1853–1861.PubMedCrossRefGoogle Scholar
  74. 74.
    Cao W, Gerton GL, Moss SB. Proteomic profiling of accessory structures from the mouse sperm flagellum. Mol Cell Proteomics 2006; 5:801–810.PubMedCrossRefGoogle Scholar
  75. 75.
    Kim YH, Haidl G, Schaefer M et al. Compartmentalization of a unique ADP/ATP carrier protein SFEC (Sperm Flagellar Energy Carrier, AAC4) with glycolytic enzymes in the fibrous sheath of the human sperm flagellar principal piece. Dev Biol 2007; 302:463–476.PubMedCrossRefGoogle Scholar
  76. 76.
    Stein KK, Go JC, Lane WS et al. Proteomic analysis of sperm regions that mediate sperm-egg interactions. Proteomics 2006; 6:3533–3543.PubMedCrossRefGoogle Scholar
  77. 77.
    Baker MA, Witherdin R, Hetherington L et al. Identification of post-translational modifications that occur during sperm maturation using difference in two-dimensional gel electrophoresis. Proteomics 2005; 5:1003–1012.PubMedCrossRefGoogle Scholar
  78. 78.
    Sleight SB, Miranda PV, Plaskett NW et al. Isolation and proteomic analysis of mouse sperm detergent-resistant membrane fractions: Evidence for dissociation of lipid rafts during capacitation. Biol Reprod 2005; 73:721–729.PubMedCrossRefGoogle Scholar
  79. 79.
    Ficarro S, Chertihin O, Westbrook VA et al. Phosphoproteome analysis of capacitated human sperm: Evidence of tyrosine phosphorylation of a kinase-anchoring protein 3 and valosin-containing protein/p97 during capacitation. J Biol Chem 2003; 278:11579–11589.PubMedCrossRefGoogle Scholar
  80. 80.
    Lalancette C, Faure RL, Leclerc P. Identification of the proteins present in the bull sperm cytosolic fraction enriched in tyrosine kinase activity: A proteomic approach. Proteomics 2006; 6:4523–4540.PubMedCrossRefGoogle Scholar
  81. 81.
    Bohring C, Krause E, Habermann B et al. Isolation and identification of sperm membrane antigens recognized by antisperm antibodies, and their possible role in immunological infertility disease. Mol Hum Reprod 2001; 7:113–118.PubMedCrossRefGoogle Scholar
  82. 82.
    Bohring C, Krause W. Characterization of spermatozoa surface antigens by antisperm antibodies and its influence on acrosomal exocytosis. Am J Reprod Immunol 2003; 50:411–419.PubMedCrossRefGoogle Scholar
  83. 83.
    Paradowska A, Bohring C, Krause E et al. Identification of evolutionary conserved mouse sperm surface antigens by human antisperm antibodies (ASA) from infertile patients. Am J Reprod Immunol 2006; 55:321–330.PubMedCrossRefGoogle Scholar
  84. 84.
    Fijak M, Iosub R, Schneider E et al. Identification of immunodominant autoantigens in rat autoimmune orchitis. J Pathol 2005; 207:127–138.PubMedCrossRefGoogle Scholar
  85. 85.
    McLean DJ, Friel PJ, Pouchnik D et al. Oligonucleotide microarray analysis of gene expression in follicle-stimulating hormone-treated rat Sertoli cells. Mol Endocrinol 2002; 16:2780–2792.PubMedCrossRefGoogle Scholar
  86. 86.
    Sadate-Ngatchou PI, Pouchnik DJ, Griswold MD. Follicle-stimulating hormone induced changes in gene expression of murine testis. Mol Endocrinol 2004; 18:2805–2816.PubMedCrossRefGoogle Scholar
  87. 87.
    Meachem SJ, Ruwanpura SM, Ziolkowski J et al. Developmentally distinct in vivo effects of FSH on proliferation and apoptosis during testis maturation. J Endocrinol 2005; 186:429–446.PubMedCrossRefGoogle Scholar
  88. 88.
    Sadate-Ngatchou PI, Pouchnik DJ, Griswold MD. Identification of testosterone-regulated genes in testes of hypogonadal mice using oligonucleotide microarray. Mol Endocrinol 2004; 18:422–433.PubMedCrossRefGoogle Scholar
  89. 89.
    Zhou Q, Shima JE, Nie R et al. Androgen-regulated transcripts in the neonatal mouse testis as determined through microarray analysis. Biol Reprod 2005; 72:1010–1019.PubMedCrossRefGoogle Scholar
  90. 90.
    Petrusz P, Jeyaraj DA, Grossman G. Microarray analysis of androgen-regulated gene expression in testis: The use of the androgen-binding protein (ABP)-transgenic mouse as a model. Reprod Biol Endocrinol 2005; 3:70.PubMedCrossRefGoogle Scholar
  91. 91.
    Meng J, Holdcraft RW, Shima JE et al. Androgens regulate the permeability of the blood-testis barrier. Proc Natl Acad Sci USA 2005; 102:16696–16700.PubMedCrossRefGoogle Scholar
  92. 92.
    Eacker SM, Shima JE, Connolly CM et al. Transcriptional profiling of androgen receptor (AR) mutants suggests instructive and permissive roles of AR signaling in germ cell development. Mol Endocrinol 2007; 21:895–907.PubMedCrossRefGoogle Scholar
  93. 93.
    Denolet E, De Gendt K, Allemeersch J et al. The effect of a sertoli cell-selective knockout of the androgen receptor on testicular gene expression in prepubertal mice. Mol Endocrinol 2006; 20:321–334.PubMedCrossRefGoogle Scholar
  94. 94.
    Khaitovich P, Hellmann I, Enard W et al. Parallel patterns of evolution in the genomes and transcriptomes of humans and chimpanzees. Science 2005; 309:1850–1854.PubMedCrossRefGoogle Scholar
  95. 95.
    Voolstra C, Tautz D, Farbrother P et al. Contrasting evolution of expression differences in the testis between species and subspecies of the house mouse. Genome Res 2007; 17:42–49.PubMedCrossRefGoogle Scholar
  96. 96.
    Kan Z, Garrett-Engele PW, Johnson JM et al. Evolutionarily conserved and diverged alternative splicing events show different expression and functional profiles. Nucleic Acids Res 2005; 33:5659–5666.PubMedCrossRefGoogle Scholar
  97. 97.
    Xu Q, Modrek B, Lee C. Genome-wide detection of tissue-specific alternative splicing in the human transcriptome. Nucleic Acids Res 2002; 30:3754–3766.PubMedCrossRefGoogle Scholar
  98. 98.
    Yeo G, Holste D, Kreiman G et al. Variation in alternative splicing across human tissues. Genome Biol 2004; 5:R74.PubMedCrossRefGoogle Scholar
  99. 99.
    Khil PP, Smirnova NA, Romanienko PJ et al. The mouse X chromosome is enriched for sex-biased genes not subject to selection by meiotic sex chromosome inactivation. Nat Genet 2004; 36:642–646.PubMedCrossRefGoogle Scholar
  100. 100.
    Li Q, Lee BT, Zhang L. Genome-scale analysis of positional clustering of mouse testis-specific genes. BMC Genomics 2005; 6:7.PubMedCrossRefGoogle Scholar
  101. 101.
    Boutanaev AM, Kalmykova AI, Shevelyov YY et al. Large clusters of coexpressed genes in the Drosophila genome. Nature 2002; 420:666–669.PubMedCrossRefGoogle Scholar
  102. 102.
    Harris MA. The Gene Ontology (GO) project in 2006. Nucleic Acids Res 2006; 34:D322–326.CrossRefGoogle Scholar
  103. 103.
    Chalmel F, Lardenois A, Primig M. Towards understanding the core meiotic transcriptome in mammals and its implications for somatic cancer. Ann NY Acad Sci 2007; 2:2.Google Scholar
  104. 104.
    Liu D, Brockman JM, Dass B et al. Systematic variation in mRNA 3′-processing signals during mouse spermatogenesis. Nucleic Acids Res 2007; 35:234–246.PubMedCrossRefGoogle Scholar
  105. 105.
    Birney E. The ENCODE (ENCyclopedia Of DNA Elements) project. Science 2004; 306:636–640.CrossRefGoogle Scholar
  106. 106.
    Birney E, Stamatoyannopoulos JA, Dutta A et al. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 2007; 447:799–816.PubMedCrossRefGoogle Scholar
  107. 107.
    Primig M, Wiederkehr C, Basavaraj R et al. GermOnline, a new cross-species community annotation database on germ-line development and gametogenesis. Nat Genet 2003; 35:291–292.PubMedCrossRefGoogle Scholar
  108. 108.
    Ivell R. ‘All that glitters is not gold’—Common testis gene transcripts are not always what they seem. Int J Androl 1992; 15:85–92.PubMedCrossRefGoogle Scholar
  109. 109.
    Gandhi TK, Zhong J, Mathivanan S et al. Analysis of the human protein interactome and comparison with yeast, worm and fly interaction datasets. Nat Genet 2006; 38:285–293.PubMedCrossRefGoogle Scholar
  110. 110.
    Cheng J, Kapranov P, Drenkow J et al. Transcriptional maps of 10 human chromosomes at 5-nucleotide resolution. Science 2005; 308:1149–1154.PubMedCrossRefGoogle Scholar
  111. 111.
    Com E, Rolland A, Guerrois M et al. Identification, molecular cloning and cellular distribution of the rat homologue of Minichromosome maintenance protein 7 (MCM7) in the rat testis. Mol Reprod Dev 2006; 73:866–877.PubMedCrossRefGoogle Scholar
  112. 112.
    Leblond CP, Clermont Y. Definition of the stages of the cycle of the seminiferous epithelium in the rat. Ann NY Acad Aci 1952; 55:548–573.CrossRefGoogle Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media 2009

Authors and Affiliations

  • Antoine D. Rolland
    • 1
  • Bernard Jégou
    • 1
  • Charles Pineau
    • 1
    Email author
  1. 1.Inserm, U625, IFR 140University of Rennes IRennesFrance

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