STRA8-deficient spermatocytes initiate, but fail to complete, meiosis and undergo premature chromosome condensation

Journal of Cell Science

Volumn 121, Issue 19, 2008, Pages 3233-3242

  Mark, Manuel ^a   Jacobs, Hugues ^a   Oulad Abdelghani, Mustapha ^a   Dennefeld, Christine ^a   Féret, Betty ^a   Vernet, Nadège ^a   Codreanu, Carmen Alina ^a   Chambon, Pierre ^a   Ghyselinck, Norbert B ^a  

^a INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

Chromosome pairing; Mouse; Preleptonema; Premature chromosome condensation; Synaptonemal complex

Indexed keywords

NUCLEAR PROTEIN; PROTEIN STRA8; STIMULATED BY RETINOIC ACID 8; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL CYCLE S PHASE; CHROMOSOME ABERRATION; CHROMOSOME CONDENSATION; CHROMOSOME PAIRING; CONTROLLED STUDY; GENE EXPRESSION; GENOME ANALYSIS; MALE; MEIOSIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM; SPERMATOCYTE;

ALLELES; ANIMALS; CHROMOSOME PAIRING; CHROMOSOMES, MAMMALIAN; GENE TARGETING; MALE; MEIOSIS; MEIOTIC PROPHASE I; METAPHASE; MICE; MUTATION; PROTEINS; S PHASE; SPERMATOCYTES; SPERMATOGENESIS; SYNAPTONEMAL COMPLEX; TESTIS;

EID: 55449103543     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.035071     Document Type: Article

References (48)

1. Baltus, A. E., Menke, D. B., Hu, Y. C., Goodheart, M. L., Carpenter, A. E., de Rooij, D. G. and Page, D. C. (2006). In germ cells of mouse embryonic ovaries, the decision to enter meiosis precedes premeiotic DNA replication. Nat. Genet. 38, 1430-1434.
2. Barlow, A. L., Benson, F. E., West, S. C. and Hultén, M. A. (1997). Distribution of the Rad51 recombinase in human and mouse spermatocytes. EMBO J. 16, 5207-5215.
3. Blagosklonny, M. V. (2007). Mitotic arrest and cell fate: why and how mitotic inhibition of transcription drives mutually exclusive events. Cell Cycle 6, 70-74.
4. Bowles, J., Knight, D., Smith, C., Wilhelm, D., Richman, J., Mamiya, S., Yashiro, K., Chawengsaksophak, K., Wilson, M. J., Rossant, J. et al. (2006). Retinoid signaling determines germ cell fate in mice. Science 312, 596-600.
5. Bucher, N. and Britten, C. D. (2008). G2 checkpoint abrogation and checkpoint kinase-1 targeting in the treatment of cancer. Br. J. Cancer. 98, 523-528.
6. Chiarini-Garcia, H. and Russell, L. D. (2001). High-resolution light microscopic characterization of mouse spermatogonia. Biol. Reprod. 65, 1170-1178.
7. Cobb, J., Cargile, B. and Handel, M. A. (1999a). Acquisition of competence to condense metaphase I chromosomes during spermatogenesis. Dev. Biol. 205, 49-64.
8. Cobb, J., Miyaike, M., Kikuchi, A. and Handel, M. A. (1999b). Meiotic events at the centromeric heterochromatin: histone H3 phosphorylation, topoisomerase II alpha localization and chromosome condensation. Chromosoma 108, 412-425.
9. Cohen, P. E., Pollack, S. E. and Pollard, J. W. (2006). Genetic analysis of chromosome pairing, recombination, and cell cycle control during first meiotic prophase in mammals. Endocr. Rev. 27, 398-426.
10. Eaker, S., Cobb, J., Pyle, A. and Handel, M. A. (2002). Meiotic prophase abnormalities and metaphase cell death in MLH1-deficient mouse spermatocytes: insights into regulation of spermatogenic progress. Dev. Biol. 249, 85-95.
11. Eijpe, M., Offenberg, H., Jessberger, R., Revenkova, E. and Heyting, C. (2003). Meiotic cohesion REC8 marks the axial elements of rat synaptonemal complexes before cohesins SMC1β and SMC3. J. Cell Biol. 160, 657-670.
12. Ghyselinck, N. B., Vernet, N., Dennefeld, C., Giese, N., Nau, H., Chambon, P., Viville, S. and Mark, M. (2006). Retinoids and spermatogenesis: lessons from mutant mice lacking the plasma retinol binding protein. Dev. Dyn. 235, 1608-1622.
13. Hamant, O., Ma, H. and Cande, W. Z. (2006). Genetics of meiotic prophase I in plants. Annu. Rev. Plant Biol. 57, 267-302.
14. Handel, M. A. and Eppig, J. J. (1998). Sexual dimorphism in the regulation of mammalian meiosis. Curr Top. Dev. Biol. 37, 333-358.
15. Harper, L., Golubovskaya, I. and Cande, W. Z. (2004). A bouquet of chromosomes. J. Cell Sci. 117, 4025-4032.
16. Ignat, M., Teletin, M., Tisserand, J., Khetchoumian, K., Dennefeld, C., Chambon, P., Losson, R. and Mark, M. (2008). Arterial calcifications and increased expression of vitamin D receptor targets in mice lacking TIF1alpha. Proc. Natl. Acad. Sci. USA 105, 2598-2603.
17. Kneitz, B., Cohen, P. E., Avdievich, E., Zhu, L., Kane, M. F., Hou, H., Jr, Kolodner, R. D., Kucherlapati, R., Pollard, J. W. and Edelmann, W. (2000). MutS homolog 4 localization to meiotic chromosomes is required for chromosome pairing during meiosis in male and female mice. Genes Dev. 14, 1085-1097.
18. Koubova, J., Menke, D. B., Zhou, Q., Capel, B., Griswold, M. D. and Page, D. C. (2006). Retinoic acid regulates sex-specific timing of meiotic initiation in mice. Proc. Natl. Acad. Sci. USA 103, 2474-2479.
19. Kouznetsova, A., Novak, I., Jessberger, R. and Höög, C. (2005). SYCP2 and SYCP3 are required for cohesin core integrity at diplotene but not for centromere cohesion at the first meiotic division. J. Cell Sci. 118, 2271-2278.
20. Kuroda, M., Sok, J., Webb, L., Baechtold, H., Urano, F., Yin, V., Chung, P., de Rooij, D. G., Akhmedov, A., Ashley, T. et al. (2000). Male sterility and enhanced radiation sensitivity in TLS(-/-) mice. EMBO J. 19, 453-462.
21. Liebe, B., Petukhova, G., Barchi, M., Bellani, M., Braselmann, H., Nakano, T., Pandita, T. K., Jasin, M., Fornace, A., Meistrich, M. L. et al. (2006). Mutations that affect meiosis in male mice influence the dynamics of the mid-preleptotene and bouquet stages. Exp. Cell Res. 312, 3768-3781.
22. Lipkin, S. M., Moens, P. B., Wang, V., Lenzi, M., Shanmugarajah, D., Gilgeous, A., Thomas, J., Cheng, J., Touchman, J. W., Green, E. D. et al. (2002). Meiotic arrest and aneuploidy in MLH3-deficient mice. Nat. Genet. 31, 385-390.
23. Mahadevaiah, S. K., Turner, J. M., Baudat, F., Rogakou, E. P., de Boer, P., Blanco-Rodríguez, J., Jasin, M., Keeney, S., Bonner, W. M. and Burgoyne, P. S. (2001). Recombinational DNA double-strand breaks in mice precede synapsis. Nat. Genet. 27, 271-276.
24. Marcon, E. and Moens, P. (2003). MLH1p and MLH3p localize to precociously induced chiasmata of okadaic-acid-treated mouse spermatocytes. Genetics 165, 2283-2287.
25. Menke, D. B., Koubova, J. and Page, D. C. (2003). Sexual differentiation of germ cells in XX mouse gonads occurs in an anterior-to-posterior wave. Dev. Biol. 262, 303-312.
26. Morelli, M. A. and Cohen, P. E. (2005). Not all germ cells are created equal: aspects of sexual dimorphism in mammalian meiosis. Reproduction 130, 761-781.
27. Nebel, B. R., Amarose, A. P. and Hacket, E. M. (1961). Calendar of gametogenic development in the prepuberal male mouse. Science 134, 832-833.
28. Oakberg, E. F. (1956). Duration of spermatogenesis in the mouse and timing of stages of the cycle of the seminiferous epithelium. Am. J. Anat. 99, 507-516.
29. Oulad-Abdelghani, M., Boulliet, P., Decimo, D., Gansmuller, A., Heyberger, S., Dolle, P., Bronner, S., Lutz, Y. and Chambon, P. (1996). Characterization of a premeiotic germ cell-specific cytoplasmic protein encoded by Stra8, a novel retinoic acid-responsive gene. J. Cell Biol. 135, 469-477.
30. Pandita, T. K., Westphal, C. H., Anger, M., Sawant, S. G., Geard, C. R., Pandita, R. K. and Scherthan, H. (1999). Atm inactivation results in aberrant telomere clustering during meiotic prophase. Mol. Cell. Biol. 19, 5096-5105.
31. Pawlowski, W. P., Sheehan, M. J. and Ronceret, A. (2007). In the beginning: the initiation of meiosis. BioEssays 29, 511-514.
32. Peters, A. H., Plug, A. W., van Vugt, M. J. and de Boer, P. (1997). A drying-down technique for the spreading of mammalian meiocytes from the male and female germline. Chromosome Res. 5, 66-68.
33. Peters, A. H., O'Carroll, D., Scherthan, H., Mechtler, K., Sauer, S., Schöfer, C., Weipoltshammer, K., Pagani, M., Lachner, M., Kohlmaier, A. et al. (2001). Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability. Cell 107, 323-337.
34. Roeder, G. S. and Bailis, J. M. (2000). The pachytene checkpoint. Trends Genet. 16, 395-403.
35. Roninson, I. B., Broude, E. V. and Chang, B. D. (2001). If not apoptosis, then what? Treatment-induced senescence and mitotic catastrophe in tumor cells. Drug Resist. Updat. 4, 303-313.
36. Russell, L. D., Ettlin, A. P. S. and Clegg, R. A. (1990). Histological and Histopathological Evaluation of the Testis. Clearwater, FL: Cache River Press.
37. Scherthan, H. (2007). Telomere attachment and clustering during meiosis. Cell. Mol. Life Sci. 64, 117-124.
38. Scherthan, H., Jerratsch, M., Dhar, S., Wang, Y. A., Goff, S. P. and Pandita, T. K. (2000). Meiotic telomere distribution and Sertoli cell nuclear architecture are altered in Atm- and Atm-p53-deficient mice. Mol. Cell. Biol. 20, 7773-7783.
39. Session, D. R., Fautsch, M. P., Avula, R., Jones, W. R., Nehra, A. and Wieben, E. D. (2001). Cyclin-dependent kinase 5 is expressed in both Sertoli cells and metaphase spermatocytes. Fertil. Steril. 75, 669-673.
40. Shinohara, A., Gasior, S., Ogawa, T., Kleckner, N. and Bishop, D. K. (1997). Saccharomyces cerevisiae recA homologues RAD51 and DMC1 have both distinct and overlapping roles in meiotic recombination. Genes Cells 2, 615-629.
41. Speed, R. M. (1982). Meiosis in the foetal mouse ovary. I. An analysis at the light microscope level using surface-spreading. Chromosoma 85, 427-437.
42. Turner, J. M., Mahadevaiah, S. K., Fernandez-Capetillo, O., Nussenzweig, A., Xu, X., Deng, C. X. and Burgoyne, P. S. (2005). Silencing of unsynapsed meiotic chromosomes in the mouse. Nat. Genet. 37, 41-47.
43. Vernet, N., Dennefeld, C., Guillou, F., Chambon, P., Ghyselinck, N. B. and Mark, M. (2006a). Prepubertal testis development relies on retinoic acid but not rexinoid receptors in Sertoli cells. EMBO J. 25, 5816-5825.
44. Vernet, N., Dennefeld, C., Rochette-Egly, C., Oulad-Abdelghani, M., Chambon, P., Ghyselinck, N. B. and Mark M. (2006b). Retinoic acid metabolism and signaling pathways in the adult and developing mouse testis. Endocrinology 147, 96-110.
45. Wei, K., Clark, A. B., Wong, E., Kane, M. F., Mazur, D. J., Parris, T., Kolas, N. K., Russell, R., Hou, H., Jr, Kneitz, B. et al. (2003). Inactivation of Exonuclease 1 in mice results in DNA mismatch repair defects, increased cancer susceptibility, and male and female sterility. Genes Dev. 17, 603-614.
46. Wolgemuth, D. J. (2006). Making the commitment to meiosis. Nat. Genet. 38, 1362-1363.
47. Xu, H., Beasley, M. D., Warren, W. D., van der Horst, G. T. and McKay, M. J. (2005). Absence of mouse REC8 cohesin promotes synapsis of sister chromatids in meiosis. Dev. Cell 8, 949-961.
48. Zickler, D. (2006). From early homologue recognition to synaptonemal complex formation. Chromosoma 115, 158-174.