HSP70-2 is required for desynapsis of synaptonemal complexes during meiotic prophase in juvenile and adult mouse spermatocytes

Development

Volumn 124, Issue 22, 1997, Pages 4595-4603

  Dix, David J ^a   Allen, James W ^a   Collins, Barbara W ^a   Poorman Allen, Patricia ^b   Mori, Chisato ^c   Blizard, Deborah R ^d   Brown, Paula R ^d   Goulding, Eugenia H ^d   Strong, Bradley D ^d   Eddy, E M ^d  

^a U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

^b GLAXOSMITHKLINE   (United States)

^c KYOTO UNIVERSITY   (Japan)

^d NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

Author keywords

Heat shock protein; HSP70; Meiosis; Mouse; Spermatogenesis; Synaptonemal complex

Indexed keywords

ANTIGEN; HEAT SHOCK PROTEIN 70; MESSENGER RNA;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CHROMOSOME; GERM CELL; MALE; MEIOSIS; METAPHASE; MOUSE; NONHUMAN; PACHYTENE; PRIORITY JOURNAL; PROPHASE; PROTEIN SYNTHESIS; SPERMATOCYTE; SYNAPTONEMAL COMPLEX; TISSUE SECTION;

ANIMALS; APOPTOSIS; BASE SEQUENCE; CELL DIFFERENTIATION; DNA PRIMERS; HSP70 HEAT-SHOCK PROTEINS; MALE; MEIOSIS; MICE; MICE, KNOCKOUT; POLYMERASE CHAIN REACTION; SEMINIFEROUS TUBULES; SPERMATOCYTES; SPERMATOGENESIS; SYNAPTONEMAL COMPLEX; TESTIS;

EID: 0030721027     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (54)

1. Allen, J. W., Dix, D. J., Collins, B. W., Merrick, B. A., He, C., Selkirk, J. K., Poorman-Allen, R. Dresser, M. E. and Eddy, E. M. (1996) HSP70-2 is part of the synaptonemal complex in mouse and hamster spermatocytes. Chromosoma 104, 414-21.
2. Allen, R. L., O'Brien, D. A., Jones, C. C., Rockett, D. L. and Eddy, E. M. (1988). Expression of heat shock proteins by isolated mouse spermatogenic cells. Mol. Cell Biol. 8, 3260-6.
3. Anderson, B., Pearse III, R. V., Schlegel, P. N., Cichon, Z., Schonemann, M. D., Bardin, C. W. and Rosenfeld, M. A. (1993) Sperm 1: a POU-domain gene transiently expressed immediately before meiosis 1 in the male germ cell. Proc. Natl Acad. Sci. USA 90, 11084-11088.
4. Baker, S. M., Bronner, C. E., Zhang, L., Plug, A. W., Robatzek, M., Warren, G., Elliott, E. A., Yu, J., Ashley, T., Arnheim, N., Flavell, R. A. and Liskay, R. M. (1995). Male mice defective in the DNA mismatch repair gene PMS2 exhibit abnormal chromosome synapsis in meiosis. Cell 82, 309-19.
5. Baker, S. M., Plug, A. W., Prolla, T. A., Bronner, C. E., Harris, A. C., Yao, X., Christie, D-M, Monell, C., Arnheim, N., Bradley, A., Ashley, T. and Liskay, R.M. (1996). Involvement of mouse Mlh1 in DNA mismatch repair and meiotic crossing over. Nature Genetics 13, 336-342.
6. Bellvé, A. R., Cavicchia, J. C., Millette, C. F., and O'Brien, D. A., Bhatnagar, Y. M. and Dym, M. (1977). Spermatogenic cells of the prepuberal mouse. J. Cell. Biol. 74, 68-85
7. Bonnycastle, L. L. C., Yu, C., Hunt, C. R., Trask, B. J., Clancy, K. P., Weber, J. L., Patterson, D. and Schellenberg, G. D. (1994). Cloning, sequencing, and mapping of the human chromosome 14 heat shock protein gene (HSPA2). Genomics 23, 85-93.
8. Chen, Q., Pearlman, R. E. And Moens, P. B. (1992) Isolation and characterization of a gene encoding a protein of the rat synaptonemal complex. Biochem. Cell Biol. 70, 1030-1038.
9. Clarke, A. R., Gledhill, S., Hooper, M. L., Bird, C. C., and Wyllie, A. H. (1994). p53 dependence of early apoptotic and proliterative responses within the mouse intestinal epithelium following gamma-irradiation. Oncogene 9, 1767-1773.
10. Cobb, J., Reddy, R. K., Park, C. and Handel, M. A. (1997). Analysis of expression and function of topoisomerases I and II during meiosis in male mice. Molec. Reprod. Dev. 46, 489-498.
11. Dix, D. J. (1997). Hsp70 expression and function during gametogenesis. Cell Stres & Chaperones 2, 73-77.
12. Dix, D. J., Rosario-Herrle, M. O., Gotoh, H., Mori, C., Goulding, E. H., Voelker, C. R. and Eddy, E. M. (1996a) Developmentally regulated expression of Hsp70-2 and a Hsp70-2/lacZ transgene during spermatogenesis. Dev. Biol. 174, 310-321.
13. Dix, D. J., Allen, J. W., Collins, B. W., Mori, C., Nakamura, N., Poorman-Allen, P., Gouliding, E. H. and Eddy, E. M. (1996b). Targeted gene disruption of Hsp70-2 results in failed meiosis. germ cell apoptosis, and male infertility. Proc. Natl Acad. Sci. USA 93, 3264-8.
14. Dobson, M.J., Pearlman, R.E., Karaiskakis, A., Spyropoulos, B. and Moens, P.B. (1994). Synaptonemal complex proteins: occurrence, epitope mapping and chromosome disjunction. J. Cell Sci. 107, 2749-2760.
15. Drabent B., Bode C., Bramlege B., and Doenecke D. (1996) Expression of the mouse testicular histone gene HIt during spermatogenesis. Histochem. Cell Biol. 106, 247-251.
16. Draetta, G. And Beach, D. (1988). Activation of cdc2 protein kinase during mitosis in human cells: cell cycle-dependent phosphorylation and subunit rearrangement. Cell 54, 17-26.
17. Draetta, G., Piwnica-Worms, H., Morrison, D., Druker, B., Roberts, T. and Beach, D. (1988). Human cdc2 protein kinase is a major cell-cycle regulated tyrosine kinase substrate. Nature 336, 738-744.
18. Dresser, M.E. and Moses, M.J. (1979). Silver staining of synaptonemal complexes in surface spreads for light and electron microscopy. Exp. Cell Res. 121, 416-419.
19. Dunphy, W.G., Brizuela, L., Beach, D. and Newport, J. (1988). The Xenopus homolog of cdc2 is a component of MPF, a cytoplasmic regulator of mitosis. Cell 54, 423-431.
20. Edelmann, W., Cohen, P. E., Kane, M., Lau, K., Morrow, B., Bennett, S., Umar, A., Kunkel, T., Cattoretti, G., Chaganti, R., Pollard, J.W., Kolodner, R. D. and Kucherlapati, R. (1996). Meiotic pachytene arrest in MLH1-deficient mice. Cell 85, 1125-1134.
21. Enders, G. C. and May, J. J. (1994). Developmentally regulated expression of a mouse germ cell nuclear antigen examined from embryonic day 11 to adult in male and female mice. Dev. Biol. 163, 331-340.
22. Fenderson, B. A., O'Brien, D. A., Millette, C. F. and Eddy, E. M. (1984). Stage-specific expression of three cell surface carbohydrate antigens during murine spermatogenesis detected with monoclonal antibodies. Devel. Biol. 103, 117-128.
23. Fenderson, B. A., Toshimori, K., Muller, C. H., Lane, T. F. and Eddy, E. M. (1988). Identification of a protein in the fibrous sheath of the sperm flagellum. Biol. Reprod. 38, 345-357.
24. Fulcher K. D., Mori C., Welch J. E., O'Brien, D. A., Klapper, D. G., and Eddy E. M. (1995). Characterization of Fsc1 cDNA for a mouse sperm fibrous sheath component. Biol. Reprod. 52, 41-49.
25. Georgopoulos, C. and Welch, W. J. (1993). Role of the major heat shock proteins as molecular chaperones. Ann. Rev. Cell Biol. 9, 601-634.
26. Haaf, T., Golub, E. I., Reddy, G., Radding, C. M. and Ward, D. C. (1995). Nuclear foci of mammalian Rad51 recombination protein in somatic cells after DNA damage and its localisation in synaptonemal complexes. Proc. Natl Acad. Sci. USA 92, 2298-302.
27. Kashiwabara, S., Arai, Y., Kodaira, K. and Baba, T. (1990). Acrosin biosynthesis in meiotic and postmeiotic spermatogenic cells. Biochem. Biophys. Res. Commun. 173, 240-245.
28. Keegan, K S., Holtzman, D. A., Plug, A. W., Christenson, E. R., Brainerd, E. E., Flaggs, G., Bentley, N. J., Taylor, E. M., Meyn, M. S., Moss, S. B., Carr, A. M. and Hockstra, M. F. (1996). The Atr and Atm protein kinases associate with different sites along meiotically pairing chromosomes. Genes Dev. 10, 2423-2437.
29. Kovalenko, O. V., Plug, A. W., Haaf, T., Gonda, D. K., Ashley, T., Ward, D. C., Radding, C. M. and Golub, E. I. (1996). Mammalian ubiquitin-conjugating enzyme Ubc9 interacts with Rad 51 recombination protein and localizes in synaptonemal complexes. Proc. Natl. Acad. Sci. USA 93, 2958-2963.
30. Kremling, H., Keime, S., Wilhelm, K., Adham, I. M., Hameister, H. and Engel, W. (1991). Mouse proacrosin gene: nucleotide sequence, diploid expression, and chromosomal localization. Genomics 11, 828-834.
31. Lin, T. Y., Viswanathan, S., Wood, C., Wilson, P. G., Wolf, N. and Fuller, M. T. (1996). Coordinate developmental control of the meiotic cell cycle and spermatid differentiation in Drosophila males. Development 122, 1331-41.
32. Matsumoto, M. and Fujimoto, H. (1990). Cloning of a hsp70-related gene expressed in mouse spermatids. Biochem. Biophys. Res. Commun. 166, 43-49.
33. Meuwissen, R. L., Offenberg, H. H., Dietrich, A. J., Riesewijk, A., Vanlersel, M. and Heyting, C. (1992) A coiled-coil related protein specific for synapsed regions of meiotic prophase chromosomes. EMBO J. 11, 5091-5100.
34. Moens, P. B. (1994). Molecular perspectives of chromosome pairing at meiosis. BioEssays 16, 101-6.
35. Moens, P. B. and Earnshaw, W. C. (1989). Anti-topoisomerase II recognizes meiotic chromosome cores. Chromosoma 98, 317-22.
36. Moens, P. B. and Spyropoulos, B. (1995). Immunocytology of chiasmata and chromosomal disjunction at mouse meiosis. Chromosoma 104, 175-82.
37. Mori, C., Nakamura, N., Kimura, S., Irie, H., Takigawa, T. and Shiota, K. (1995). Programmed cell death in the interdigital tissue of the fetal mouse limb is apoptosis with DNA fragmentation. Anatom. Rec. 242, 103-110.
38. Mori, C., Nakamura, N., Dix, D. J., Fujioka, M., Nakagawa, S., Shiota, K. and Eddy, E. M. (1997) Morphological analysis of germ cell apoptosis during postnatal testis development in normal and Hsp70-2 knockout mice. Dev. Dynamics 208, 125-136.
39. Moses, M. J. (1968) Synaptonemal complex. Ann. Rev. Genetics 2, 363-412.
40. Moses, M. J. (1980) New cytogenetic studies on mammalian meiosis. In Animal Models in Human Reproduction (ed. M. Serio, Martini, L.), pp. 169-190. Raven Press, New York.
41. Moses, M. J. (1981) Meiosis, synaptonemal complexes, and cytogenetic analysis. In Bioregulators of Reproduction (ed. G. Jagiello and Vogel. H.), pp 187-206. Academic Press, New York.
42. Moses, M. J., Poorman-Allen, P., Tepperberg, J.H., Gibson, J.B., Backer, L. C. and Allen, J. W. (1990). The synaptonemal complex as an indicator of induced chromosome damage. In Banbury Report 34: Biology of Mammalian Germ Cell Mutagenesis (ed J. W. Allen, B. A. Bridges, M. F. Lyon, M. J. Moses and L. B. Russell), pp. 133-150. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
43. Orr-Weaver, T. (1995). Meiosis in Drosophila : seeing is believing. Proc. Natl Acad. Sci USA 92, 10443-10449.
44. Raab, L. S., Polakoski, K. L., Hancock, L. W. and Hamilton, D. W. (1995) Characterization of the heat shock protein P70 in rat spermatogenic cells. Mol. Reprod. Dev. 40, 186-195.
45. Rosario, M. O., Perkins, S. L., O'Brien, D. A., Allen, R. L. and Eddy, E. M. (1992). Identification of the gene for the developmentally expressed 70 kDa heat-shock protein (P70) of mouse spermatogenic cells. Dev. Biol. 150, 1-11.
46. Scully, R., Chen, J., Plug, A., Xiao, Y., Weaver, D., Feunteun, J., Ashley, T. and Livingston, D.M. (1997). Association of BRCA1 with Rad51in mitotic and meiotic cells. Cell 88, 265-275.
47. Sigrist, S., Ried, G. and Lehner, C. F. (1995). Dmcdc2 kinase is required for both meiotic divisions during Drosophila spermatogenesis and is activated by the Twine/cdc25 phosphatase. Mech. Dev. 53, 247-260.
48. Sweeney, C., Murphy, M., Kubelka, M., Ravnik, S. E., Hawkins, C. F., Wolgemuth, D. J. and Carrington, M. (1996). A distinct cyclin A is expressed in germ cells in the mouse. Development 122, 53-64.
49. Welch J. E., Schatte E. C., O'Brien D. A. and Eddy E. M. (1992) Expression of a glyceraldehyde 3-phosphate dehydrogenase gene specific to mouse spermatogenic cells. Biol. Reprod. 46, 869-878.
50. Wiltshire, T., Park, C., Caldwell, K. A. and Handel, M. A. (1995) Induced premature G2/M-phase transition in pachytene spermatocytes includes events unique to meiosis. Dev. Biol. 169, 557-567.
51. Wisniewski, J., Kordula, T. and Krawczyk, Z. (1990). Isolation and nucleotide sequence analysis of the rat testis-specific major heat-shock protein (HSP70)-related gene. Biochim. Biophys. Acta 1048, 93-99.
52. Wu, S. and Wolgemuth, D. J. (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.
53. Zakeri, Z. F., Wolgemuth, D. J. and Hunt, C. R. (1988). Identification and sequence analysis of a new member of the mouse HSP70 gene family and characterization of its unique cellular and developmental pattern of expression in the male germ line. Mol. Cell. Biol. 8, 2925-2932.
54. Zhu, D., Dix, D. J. and Eddy, E. M. (1997). HSP70-2 is required for CDC2 kinase activity in meiosis I of mouse spermatocytes. Development 124, 3007-3014.