Sex-Specific Differences in the Control of Mammalian Gametogenesis: Vive la Difference!

  • D. J. Wolgemuth
Conference paper
Part of the Ernst Schering Research Foundation Workshop book series (SCHERING FOUND, volume 9)


The notion that the highly differentiated mammalian gametes would have gamete-specific genes that are important for their differentiation and function is almost self-evident. The structural components of these specialized cells, such as proteins in the acrosome, flagellum, and zona pellucida would be expected to and indeed do exhibit sexually dimorphic expression and function. This class of sex-specific genes is excluded from the following discussion. Rather, we will explore the roles of genes that by virtue of their common expression in both oocytes and spermatocytes or their conserved function in gametes across species might be expected to be important to germ cell function in mammals — yet have proven to defy our best predictions!


Germ Cell Meiotic Division Meiotic Prophase Seminiferous Epithelium Female Germ Cell 
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  1. Aaltonen LA, Peltomaki P, Leach FS, Sistonen P, Pylkkanen L, Mecklin JP, Jarvinen H, Powell SM, Jen J and Hamilton SR (1993) Clues to the pathogenesis of familial colorectal cancer. Science 260: 812–6.PubMedCrossRefGoogle Scholar
  2. Albert B, Bray D, Lewis J, Raff M, Roberts K and Watson JD (1983) Molecular Biology of The Cell. Garland Publishing, Inc.Google Scholar
  3. Alani E, Reenan RA and Kolodner RD (1994) Interaction between mismatch repair and genetic recombination in Saccharomyces cerevisiae. Genetics 137: 19–39.PubMedGoogle Scholar
  4. Bachvarova R (1985) Gene expression during oogenesis and oocyte development in mammals. In: Developmental Biology. Eds. L. W. Browder. New York, pp 453–524.Google Scholar
  5. Baker SM, Bronner CE, Zhang L, Plug AW, Robatzek M, Warren G, Elliott EA, Yu J, Ashley T and Arnheim N (1995) Male mice defective in the DNA mismatch repair gene PMS2 exhibit abnormal chromosome synapsis in meiosis. Cell 82: 309–19.PubMedCrossRefGoogle Scholar
  6. Bellve AR, Cavicchia JC, Millette CF, O’Brien DA, Bhatnagar YM and Dym M (1977) Spermatogenic cells of the prepuberal mouse. Isolation and morphological characterization. J Cell Biol 741: 68–85Google Scholar
  7. Bronner CE, Baker SM, Morrison PT, Warren G, Smith LG, Lescoe MK, Kane M, Earabino C, Lipford J and Lindblom A (1994) Mutation in the DNA mismatch repair gene homologue hMLH1 is associated with hereditary non-polyposis colon cancer. Nature 368: 258–61.PubMedCrossRefGoogle Scholar
  8. Colledge WH, Carlton MB, Udy GB and Evans MJ (1994) Disruption of cmos causes parthenogenetic development of unfertilized mouse eggs. Nature 370: 65–8PubMedCrossRefGoogle Scholar
  9. Eddy EM, Welch JE and O’Brian DA (1993) Gene expression during spermatogenesis. In: Mol Biol of the Reprod Syst. Eds. D. d. Kretser. San Diego, pp 181–232Google Scholar
  10. Ge RS and Hardy MP (1997) Decreased cyclin A2 and increased cyclin G1 levels coincide with loss of proliferative capacity in rat Leydig cells during pubertal development. Endocrinology 138: 3719–3726PubMedCrossRefGoogle Scholar
  11. Goldman DS, Kiessling AA, Millette CF and Cooper GM (1987) Expression of c-mos RNA in germ cells of male and female mice. Proc Natl Acad Sci USA 84: 4509–4513PubMedCrossRefGoogle Scholar
  12. Hashimoto N, Watanabe N, Furuta Y, Tamemoto H, Sagata N, Yokoyama M, Okazaki K, Nagayoshi M, Takeda N and Ikawa Y (1994) Parthenogenetic activation of oocytes in c-mos-deficient mice. Nature 370: 68–71PubMedCrossRefGoogle Scholar
  13. Howe JA, Howell M, Hunt T and Newport JW (1995) Identification of a developmental timer regulating the stability of embryonic cyclin A and a new somatic A-type cyclin at gastrulation. Genes Dev 9: 1164–76PubMedCrossRefGoogle Scholar
  14. Kastner P, Mark M, Leid M, Gansmuller A, Chin W, Grondona JM, Decimo D, Krezel W, Dierich A and Chambon P (1996) Abnormal spermatogenesis in RXR beta mutant mice. Genes Dev 10: 80–92PubMedCrossRefGoogle Scholar
  15. Lewandoski M, Wassarman KM and Martin GR (1997) Zp3-cre, a transgenic mouse line for the activation or inactivation of loxP-flanked target genes specifically in the female germ line. Curr Biol 72: 148–51CrossRefGoogle Scholar
  16. Liao C, Ravnik S, Zhang Q, Muhlrad S and Wolgemuth D (In preparation) Differential Expression of the A-type Cyclins during Cell Cycles in the Mouse Ovary.Google Scholar
  17. Liu D, Liao C and Wolgemuth DJ (2000) A Role for Cyclin Al in the Activation of MPF and G2-M Transition during Meiosis of Male Germ Cells in Mice. Dev Biol 224: 388–400PubMedCrossRefGoogle Scholar
  18. Liu D, Matzuk MM, Sung WK, Guo Q, Wang P and Wolgemuth DJ (1998) Cyclin Al is required for meiosis in the male mouse. Nat Genet 20: 377–380PubMedCrossRefGoogle Scholar
  19. Lufkin T, Lohnes D, Mark M, Dierich A, Gorry P, Gaub MP, LeMeur M and Chambon P (1993) High postnatal lethality and testis degeneration in reti-Google Scholar
  20. noic acid receptor alpha mutant mice. Proc Natl Acad Sci U S A 90: 7225–7229Google Scholar
  21. Mendelsohn C, Lohnes D, Decimo D, Lufkin T, LeMeur M, Chambon P and Mark M (1994) Function of the retinoic acid receptors (RARs) during development (II). Multiple abnormalities at various stages of organogenesis in RAR double mutants. Development 120: 2749–2771Google Scholar
  22. Morita Y and Tilly JL (1999) Segregation of retinoic acid effects on fetal ovarian germ cell mitosis versus apoptosis by requirement for new macro-molecular synthesis. Endocrinology 140: 2696–2703PubMedCrossRefGoogle Scholar
  23. Murphy M, Stinnakre MG, Senamaud-Beaufort C, Winston NJ, Sweeney C, Kubelka M, Carrington M, Brechot C and Sobczak-Thepot J (1997) Delayed early embryonic lethality following disruption of the murine cyclin A2 gene [published erratum appeared in Nat Genet 1999 Dec;23(4):481]. Nat Genet 15: 83–86CrossRefGoogle Scholar
  24. Mutter GL, Grills GS and Wolgemuth DJ (1988) Evidence for the involvement of the proto-oncogene c-mos in mammalian meiotic maturation and possibly very early embryogenesis. Embo J 7: 683–689PubMedGoogle Scholar
  25. Mutter GL, Stacey A and Wolgemuth DJ (1987) Differential expression in murine somatic and germinal tissues of transcripts homologous to an abundant embryonal-carcinoma-cell mRNA. Differentiation 34: 126–130PubMedCrossRefGoogle Scholar
  26. Nebel BR, Amarosa AP and Hackett EA (1961) Calendar of gametogenic development in the prepubertal male mouse. Science 134: 832–833PubMedCrossRefGoogle Scholar
  27. Oakberg EF (1956a) Duration of spermatogenesis in the mouse and timing of stages of the cycle of the seminiferous epithelium. Am J Anat 99: 507–516PubMedCrossRefGoogle Scholar
  28. Oakberg EF (1956b) A description of spermiogenesis in the mouse and its use in analysis of the cycle of the seminiferous epithelium and germ cell renewal. Am J Anat 99: 391–409PubMedCrossRefGoogle Scholar
  29. O’Keefe SJ, Wolfes H, Kiessling AA and Cooper GM (1989) Microinjection of antisense c-mos oligonucleotides prevents meiosis II in the maturing mouse egg. Proc Natl Acad Sci U S A 86: 7038–7042.PubMedCrossRefGoogle Scholar
  30. Packer AI and Wolgemuth DJ (1999) Genetic and Molecular Approaches to Understanding the Role of Retinoids in Mammalian Spermatogenesis. Handbook of Experimental Pharmacology 139: 347–368CrossRefGoogle Scholar
  31. Paules RS, Buccione R, Moschel RC, Vande Woude GF and Eppig JJ (1989) Mouse Mos protooncogene product is present and functions during oogenesis. Proc Natl Acad Sci U S A 86: 5395–5399.PubMedCrossRefGoogle Scholar
  32. Propst F, Rosenberg MP, Jyer A, Kaul K and Vande Woude GF (1987) c-mos proto-oncogene RNA transcripts in mouse tissues: structural features, developmental regulation, and localization in specific cell types. Mol Cell Biol 7: 1629–1637.Google Scholar
  33. Ravnik SE and Wolgemuth DJ (1996) The developmentally restricted pattern of expression in the male germ line of a murine cyclin A, cyclin A2, suggests roles in both mitotic and meiotic cell cycles. Dev Biol 173: 69–78PubMedCrossRefGoogle Scholar
  34. Ravnik SE and Wolgemuth DJ (1999) Regulation of meiosis during mammalian spermatogenesis: the A-type cyclins and their associated cyclin-dependent kinases are differentially expressed in the germ-cell lineage. Dev Biol 207: 408–418PubMedCrossRefGoogle Scholar
  35. Russel LD, Ettlin R, Sinha Hikim AP and Clegg ED (1990) Histological and Histopathological Evaluation of the Testis. Cache River Press.Google Scholar
  36. Schultz RM (1986) Molecular aspects of mammalian oocytes growth and maturation. In: Experimental Approaches to Mammalian Embryonic Development. Eds. J. R. a. R. A. Pedersen. New York, Cambridge University Press, pp 195–237Google Scholar
  37. Setchell BP (1982) The flow and composition of lymph from the testes of pigs with some observations on the effect of raised venous pressure. Comp Bioch Physiol A 73: 201–205CrossRefGoogle Scholar
  38. Svoboda P, Stein P, Hayashi H and Schultz RM (2000) Selective reduction of dormant maternal mRNAs in mouse oocytes by RNA interference. Development 127: 4147–4156.PubMedGoogle Scholar
  39. Sweeney C, Murphy M, Kubelka M, Ravnik SE, Hawkins CF, Wolgemuth DJ and Carrington M (1996) A distinct cyclin A is expressed in germ cells in the mouse. Development 122: 53–64PubMedGoogle Scholar
  40. Wiltshire T, Park C, Caldwell KA and Handel MA (1995) Induced premature G2/M-phase transition in pachytene spermatocytes includes events unique to meiosis. Dev Biol 169: 557–567PubMedCrossRefGoogle Scholar
  41. Winston N, Bourgain-Guglielmetti F, Ciemerych MA, Kubiak JZ, SenamaudBeaufort C, Carrington M, Brechot C and Sobczak-Thepot J (2000) Early development of mouse embryos null mutant for the cyclin A2 gene occurs in the absence of maternally derived cyclin A2 gene products. Dev Biol 223: 139–153.PubMedCrossRefGoogle Scholar
  42. Wolgemuth DJ, Rhee K, Wu S and Ravnik SE (1995) Genetic control of mitosis, meiosis and cellular differentiation during mammalian spermatogenesis. Reprod Fertil Dev 7: 669–683PubMedCrossRefGoogle Scholar
  43. Yang R, Morosetti R and Koeffler HP (1997) Characterization of a second human cyclin A that is highly expressed in testis and in several leukemic cell lines. Cancer Res 57: 913–920PubMedGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2002

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  • D. J. Wolgemuth

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