Bat3 deficiency accelerates the degradation of Hsp70-2/HspA2 during spermatogenesis

Journal of Cell Biology

Volumn 182, Issue 3, 2008, Pages 449-458

  Sasaki, Toru ^a   Marcon, Edyta ^c   McQuire, Tracy ^a   Arai, Yoichi ^d   Moens, Peter B ^c   Okada, Hitoshi ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c YORK UNIVERSITY   (Canada)

^d TOHOKU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 70 2; HEAT SHOCK PROTEIN A2; HISTONE H2AX; PROTEIN; PROTEIN BAT3; RAD51 PROTEIN; REPLICATION FACTOR A;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; GERM CELL; HUMAN; HUMAN CELL; MALE; MALE INFERTILITY; MEIOSIS; MOUSE; NONHUMAN; PACHYTENE; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; SPERMATOCYTE; SPERMATOGENESIS; STAINING; SYNAPTONEMAL COMPLEX;

ANIMALS; APOPTOSIS; CARRIER PROTEINS; CELL LINE; HSP70 HEAT-SHOCK PROTEINS; HUMANS; MALE; MICE; NUCLEAR PROTEINS; ORGAN SPECIFICITY; POLYUBIQUITIN; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; SPERMATOGENESIS; SPERMATOZOA; SYNAPTONEMAL COMPLEX; THERMODYNAMICS;

MUS;

EID: 49749130037     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200802113     Document Type: Article

References (40)

1. Allen, J.W., D.J. Dix, B.W. Collins, B.A. Merrick, C. He, J.K. Selkirk, P. Poorman-Allen, M.E. Dresser, and E.M. Eddy. 1996. HSP70-2 is part of the synaptonemal complex in mouse and hamster spermatocytes. Chromosoma. 104:414-421.
2. Anway, M.D., J. Folmer, W.W. Wright, and B.R. Zirkin. 2003. Isolation of sertoli cells from adult rat testes: an approach to ex vivo studies of Sertoli cell function. Biol. Reprod. 68:996-1002.
3. Arndt, V., C. Daniel, W. Nastainczyk, S. Alberti, and J. Hohfeld. 2005. BAG-2 acts as an inhibitor of the chaperone-associated ubiquitin ligase CHIP. Mol. Biol. Cell. 16:5891-5900.
4. Boer, P.H., C.N. Adra, Y.F. Lau, and M.W. McBurney. 1987. The testis-specific phosphoglycerate kinase gene pgk-2 is a recruited retroposon. Mol. Cell. Biol. 7:3107-3112.
5. Bolcun-Filas, E., Y. Costa, R. Speed, M. Taggart, R. Benavente, D.G. De Rooij, and H.J. Cooke. 2007. SYCE2 is required for synaptonemal complex assembly, double strand break repair, and homologous recombination. J. Cell Biol. 176:741-747.
6. Briknarova, K., S. Takayama, L. Brive, M.L. Havert, D.A. Knee, J. Velasco, S. Homma, E. Cabezas, J. Stuart, D.W. Hoyt, et al. 2001. Structural analysis of BAG1 cochaperone and its interactions with Hsc70 heat shock protein. Nat. Struct. Biol. 8:349-352.
7. Buaas, F.W., A.L. Kirsh, M. Sharma, D.J. McLean, J.L. Morris, M.D. Griswold, D.G. de Rooij, and R.E. Braun. 2004. Plzf is required in adult male germ cells for stem cell self-renewal. Nat. Genet. 36:647-652.
8. Costa, Y., and H.J. Cooke. 2007. Dissecting the mammalian synaptonemal complex using targeted mutations. Chromosome Res. 15:579-589.
9. Costa, Y., R. Speed, R. Ollinger, M. Alsheimer, C.A. Semple, P. Gautier, K. Maratou, I. Novak, C. Hoog, R. Benavente, and H.J. Cooke. 2005. Two novel proteins recruited by synaptonemal complex protein 1 (SYCP1) are at the centre of meiosis. J. Cell Sci. 118:2755-2762.
10. Dai, Q., S.B. Qian, H.H. Li, H. McDonough, C. Borchers, D. Huang, S. Takayama, J.M. Younger, H.Y. Ren, D.M. Cyr, and C. Patterson. 2005. Regulation of the cytoplasmic quality control protein degradation pathway by BAG2. J. Biol. Chem. 280:38673-38681.
11. Daugaard, M., T. Kirkegaard-Sorensen, M.S. Ostenfeld, M. Aaboe, M. Hoyer-Hansen, T.F. Orntoft, M. Rohde, and M. Jaattela. 2007. Lens epithelium-derived growth factor is an Hsp70-2 regulated guardian of lysosomal stability in human cancer. Cancer Res. 67:2559-2567.
12. de Kretser, D.M. 1997. Male infertility. Lancet. 349:787-790.
13. Demand, J., S. Alberti, C. Patterson, and J. Hohfeld. 2001. Cooperation of a ubiquitin domain protein and an E3 ubiquitin ligase during chaperone/proteasome coupling. Curr. Biol. 11:1569-1577.
14. Desmots, F., H.R. Russell, Y. Lee, K. Boyd, and P.J. McKinnon. 2005. The reaper-binding protein scythe modulates apoptosis and proliferation during mammalian development. Mol. Cell. Biol. 25:10329-10337.
15. Desmots, F., H.R. Russell, D. Michel, and P.J. McKinnon. 2007. Scythe regulates apoptosis inducing factor stability during endoplasmic reticulum stress induced apoptosis. J. Biol. Chem. 283:3264-3271.
16. Dix, D.J., J.W. Allen, B.W. Collins, C. Mori, N. Nakamura, P. Poorman-Allen, E.H. Goulding, and E.M. Eddy. 1996. Targeted gene disruption of Hsp70-2 results in failed meiosis, germ cell apoptosis, and male infertility. Proc. Natl. Acad. Sci. USA. 93:3264-3268.
17. Dobson, M.J., R.E. Pearlman, A. Karaiskakis, B. Spyropoulos, and P.B. Moens. 1994. Synaptonemal complex proteins: occurrence, epitope mapping and chromosome disjunction. J. Cell Sci. 107:2749-2760.
18. Fawcett, D.W. 1956. The fine structure of chromosomes in the meiotic prophase of vertebrate spermatocytes. J. Biophys. Biochem. Cytol. 2:403-406.
19. Govin, J., C. Caron, E. Escoffier, M. Ferro, L. Kuhn, S. Rousseaux, E.M. Eddy, J. Garin, and S. Khochbin. 2006. Post-meiotic shifts in HSPA2/HSP70.2 chaperone activity during mouse spermatogenesis. J. Biol. Chem. 281:37888-37892.
20. Hamer, G., K. Gell, A. Kouznetsova, I. Novak, R. Benavente, and C. Hoog. 2006. Characterization of a novel meiosis-specific protein within the central element of the synaptonemal complex. J. Cell Sci. 119:4025-4032.
21. Kleene, K.C., R.J. Distel, and N.B. Hecht. 1984. Translational regulation and deadenylation of a protamine mRNA during spermiogenesis in the mouse. Dev. Biol. 105:71-79.
22. Maratou, K., T. Forster, Y. Costa, M. Taggart, R.M. Speed, J. Ireland, P. Teague, D. Roy, and H.J. Cooke. 2004. Expression profiling of the developing testis in wild-type and Dazl knockout mice. Mol. Reprod. Dev. 67:26-54.
23. Moens, P.B. 1994. Molecular perspectives of chromosome pairing at meiosis. Bioessays. 16:101-106.
24. Moens, P.B., N.K. Kolas, M. Tarsounas, E. Marcon, P.E. Cohen, and B. Spyropoulos. 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.
25. Moses, M.J. 1956. Chromosomal structures in crayfish spermatocytes. J. Biophys. Biochem. Cytol. 2:215-218.
26. Moses, M.J. 1969. Structure and function of the synaptonemal complex. Genetics. 61:41-51.
27. Pogge von Strandmann, E., V.R. Simhadri, B. von Tresckow, S. Sasse, K.S. Reiners, H.P. H ansen, A. Rothe, B. Boll, V.L. Simhadri, P. Borchmann, et al. 2007. Human leukocyte antigen-B-associated transcript 3 is released from tumor cells and engages the NKp30 receptor on natural killer cells. Immunity. 27:965-974.
28. Rohde, M., M. Daugaard, M.H. Jensen, K. Helin, J. Nylandsted, and M. Jaattela. 2005. Members of the heat-shock protein 70 family promote cancer cell growth by distinct mechanisms. Genes Dev. 19:570-582.
29. Sasaki, T., E.C. Gan, A. Wakeham, S. Kornbluth, T.W. Mak, and H. Okada. 2007. HLA-B-associated transcript 3 (Bat3)/Scythe is essential for p300-mediated acetylation of p53. Genes Dev. 21:848-861.
30. Sassone-Corsi, P. 2002. Unique chromatin remodeling and transcriptional regulation in spermatogenesis. Science. 296:2176-2178.
31. Schrans-Stassen, B.H., P.T. Saunders, H.J. Cooke, and D.G. de Rooij. 2001. Nature of the spermatogenic arrest in Dazl-/- mice. Biol. Reprod. 65:771-776.
32. Sigurdsson, S., K. Trujillo, B. Song, S. Stratton, and P. Sung. 2001. Basis for avid homologous DNA strand exchange by human Rad51 and RPA. J. Biol. Chem. 276:8798-8806.
33. Thress, K., W. Henzel, W. Shillinglaw, and S. Kornbluth. 1998. Scythe: a novel reaper-binding apoptotic regulator. EMBO J. 17:6135-6143.
34. Thress, K., E.K. Evans, and S. Kornbluth. 1999a. Reaper-induced dissociation of a Scythe-sequestered cytochrome c-releasing activity. EMBO J. 18:5486-5493.
35. Thress, K., S. Kornbluth, and J.J. Smith. 1999b. Mitochondria at the crossroad of apoptotic cell death. J. Bioenerg. Biomembr. 31:321-326.
36. Thress, K., J. Song, R.I. Morimoto, and S. Kornbluth. 2001. Reversible inhibition of Hsp70 chaperone function by Scythe and Reaper. EMBO J. 20:1033-1041.
37. Toure, A., E.J. Clemente, P. Ellis, S.K. Mahadevaiah, O.A. Ojarikre, P.A. Ball, L. Reynard, K.L. Loveland, P.S. Burgoyne, and N.A. Affara. 2005. Identification of novel Y chromosome encoded transcripts by testis transcriptome analysis of mice with deletions of the Y chromosome long arm. Genome Biol. 6:R102.
38. Wang, P.J., J.R. McCarrey, F. Yang, and D.C. Page. 2001. An abundance of X-linked genes expressed in spermatogonia. Nat. Genet. 27:422-426.
39. Wang, R., and C.C. Liew. 1994. The human BAT3 ortholog in rodents is predominantly and developmentally expressed in testis. Mol. Cell. Biochem. 136:49-57.
40. Zickler, D., and N. Kleckner. 1999. Meiotic chromosomes: integrating structure and function. Annu. Rev. Genet. 33:603-754.