Inactivation of the HR6B ubiquitin-conjugating DNA repair enzyme in mice causes male sterility associated with chromatin modification

Cell

Volumn 86, Issue 5, 1996, Pages 799-810

  Roest, H P ^a   Van Klaveren, J ^a   De Wit, J ^a   Van Gurp, C G ^a   Koken, M H M ^a,b   Vermey, M ^a   Van Roijen, J H ^a   Hoogerbrugge, J W ^a   Vreeburg, J T M ^a   Baarends, W M ^a   Bootsma, D ^a   Grootegoed, J A ^a   Hoeijmakers, J H J ^a  

^a ERASMUS UNIVERSITY ROTTERDAM   (Netherlands)

^b SAINT LOUIS HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

UBIQUITIN;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CHROMATIN CONDENSATION; CHROMATIN STRUCTURE; DNA DAMAGE; DNA REPAIR; ENZYME INACTIVATION; GENE MUTATION; MALE STERILITY; MEIOSIS; MOLECULAR INTERACTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SPERMATOGENESIS;

EID: 16044372544     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(00)80154-3     Document Type: Article

References (55)

1. Agell, N., and Mezquita, C. (1988). Cellular content of ubiquitin and formation of ubiquitin conjugates during chicken spermatogenesis. Biochem. J. 250, 883-889.
2. Agell, N., Chiva, M., and Mezquita, C. (1983). Changes in nuclear content of protein conjugate histone H2A-ubiquitin during rooster spermatogenesis. FEBS Lett. 155, 209-212.
3. Aitken, R.J., Baker, H.W.G., and Irvine, D.S. (1995). On the nature of semen quality and infertility. Hum. Reprod. 10, 248-249.
4. Alfonso, P.J., and Kistler, W.S. (1993). Immunohistochemical localization of spermatid nuclear transition protein 2 in the testes of rats and mice. Biol. Reprod. 48, 522-529.
5. Baker, S.M., Bonner, C.E., Zhang, L., Plug, A.W., Robatzek, M., Warren, G., Elliott, E.A., Yu, J., Ashley, T., Arnheim, N., et al. (1995). Male mice defective in the DNA mismatch repair gene PMS2 exhibit abnormal chromosome synapsis in meiosis. Cell 82, 309-319.
6. Balhorn, R. (1989). Mammalian protamines: structure and molecular interactions. In Molecular Biology of Chromosome Function, K.W. Adolph, ed. (New York: Springer), pp. 366-395.
7. Brock, W.A., Trostle, P.K., and Meistrich, M.L. (1980). Meiotic synthesis of testis histones in the rat. Proc. Natl. Acad. Sci. USA 77, 371-375.
8. Chau, V., Tobias, J.W., Bachmair, A., Marriott, D., Ecker, D.J., Gonda, D.K., and Varshavsky, A. (1989). A multiubiquitin chain is confined to specific lysine in a targeted short-lived protein. Science 243, 1576-1583.
9. Chevaillier, P., Mauro, N., Feneux, D., Jouannet, P., and David, G. (1987). Anomalous protein complement of sperm nuclei in some infertile men. Lancet 2, 806-807.
10. Ciechanover, A. (1994). The ubiquitin-proteasome proteolytic pathway. Cell 79, 13-21.
11. Ciechanover, A., DiGiuseppe, J.A., Bercovich, B., Orlan, A., Richter, J.D., Schwartz, A.L., and Brodeur, G.M. (1991). Degradation of nuclear oncoproteins by the ubiquitin proteolysis system in vitro. Proc. Natl. Acad. Sci. USA 88, 139-143.
12. De Yebra, L., Ballescà, J.L., Vanrell, J.A., Bassas, L., and Oliva, R. (1993). Complete selective absence of protamine P2 in humans. J. Biol. Chem. 268, 10553-10557.
13. Dohmen, R.J., Madura, K., Bartel, B., and Varshavsky, A. (1991). The N-end rule is mediated by the UBC2 (RAD6) ubiquitin-conjugating enzyme. Proc. Natl. Acad. Sci. USA 88, 7351-7355.
14. Dullaart, J., Kent, J., and Ryle, M. (1975). Serum gonadotrophin concentrations in infantile female mice. J. Reprod. Fertil. 43, 189-192.
15. Foresta, C., Zorzi, M., Rossata, M., and Varotto, A. (1992). Sperm nuclear instability and staining with aniline blue: abnormal persistance of histones in spermatozoa in infertile men. Int. J. Androl. 15, 330-337.
16. Game, J.C., and Mortimer, R.K. (1974). A genetic study of X-ray sensitive mutants in yeast. Mutation Res. 24, 281-292.
17. Gavrieli, Y., Sherman, Y., and Ben-Sasson, S.A. (1992). Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119, 493-501.
18. Glotzer, M., Murray, A.W, and Kirschner, M.W. (1991). Cyclin is degraded by the ubiquitin pathway. Nature 249, 132-138.
19. Goldknopf, I.L., and Busch, H. (1980). N-bromosuccinimide fragmentation of protein A24 (uH2A): a indication that ubiquitin is the precursor of conjugation in vivo. Biochem. Biophys. Res. Commun. 96, 1724-1731.
20. Gorczyca, W., Gong, J., and Darzynkiewicz, Z. (1993). Detection of DNA strand breaks in individual apoptotic cells by the in situterminal deoxynucleotidyl transferase and nick translation assays. Cancer Res. 53, 1945-1951.
21. Hendriksen, P.J.M., Hoogerbrugge, J.W., Themmen, A.P.N., Koken, M.H.M., Hoeijmakers, J.H.J., Oostra, B.A., Van der Lende, T., and Grootegoed, J.A. (1995). Postmeiotic transcription of X and Y chromosomal genes during spermatogenesis in the mouse. Dev. Biol. 170, 730-733.
22. Hochstrasser, M. (1995). Ubiquitin, proteasomes, and the regulation of intracellular protein degradation. Curr. Opin. Cell Biol. 7, 215-223.
23. Jentsch, S. (1992). Ubiquitin-dependent protein degradation: a cellular perspective. Trends Cell Biol. 2, 98-103.
24. Jentsch, S., McGrath, J.P., and Varshavsky, A. (1987). The yeast DNA repair gene RAD6 encodes a ubiquitin-conjugating enzyme. Nature 329, 131-134.
25. Kay, G.F., Ashworth, A., Penny, G.D., Dunlop, M., Swift, S., Brockdorff, N., and Rastan, S. (1991). A candidate spermatogenesis gene on the mouse Y chromosome is homologous to ubiquitin-activating enzyme E1. Nature 354, 486-489.
26. Kistler, W.S. (1989). Structure of testis-specific histones, spermatid transition proteins, and their genes in mammals. In Histones and Other Basic Nuclear Proteins., L.S. Hnilica, G.S. Stein, and J.L. Stein, eds. (Boca Raton, Florida: CRC Press), pp. 331-346.
27. Koken, M., Reynolds, P., Bootsma, D., Hoeijmakers, J., Prakash, S., and Prakash, L. (1991 a). Dhr6, a Drosophila homolog of the yeast DNA-repair gene RAD6. Proc. Natl. Acad. Sci. USA 88, 3832-3836.
28. Koken, M.H.M., Reynolds, P., Jaspers-Dekker, I., Prakash, L., Prakash, S., Bootsma, D., and Hoeijmakers, J.H.J. (1991b). Structural and functional conservation of two human homologs of the yeast DNA repair gene RAD6. Proc. Natl. Acad. Sci. USA 88, 8865-8869.
29. Koken, M.H.M., Hoogerbrugge, J.W., Jaspers-Dekker, I., de Wit, J., Willemsen, R., Roest, H.P., Grootegoed, J.A., and Hoeijmakers, J.H.J. (1996). Expression of the ubiquitin-conjugating DNA repair enzymes HHR6A and B suggests a role in spermatogenesis and chromatin modification. Dev. Biol. 173, 119-132.
30. Kornitzer, D., Raboy, B., Kulka, R.G., and Fink, G.R. (1994). Regulated degradation of the transcription factor Gcn4. EMBO J. 13, 6021-6030.
31. Lawrence, C. (1994). The RAD6 repair pathway in Saccharomyces cerevisiae: what does it do, and how does it do it? BioAssays 16, 253-258.
32. Madura, K., Dohmen, R.J., and Varshavsky, A. (1993). N-recognin/ Ubc2 interactions in the N-end rule pathway. J. Biol. Chem. 268, 12046-12054.
33. Meistrich, M.L. (1989). Histone and basic nuclear protein transitions in mammalian spermatogenesis. In Histones and Other Basic Nuclear Proteins, L.S. Hnilica, G.S. Stein, and J.L. Stein, eds. (Boca Raton, Florida: CRC Press), pp. 165-182.
34. Meistrich, M.L., Bucci, L.R., Trostle-Weige, P.K., and Brock, W.A. (1985). Histone variants in rat spermatogonia and primary spermatocytes. Dev. Biol. 112, 230-240.
35. Meistrich, M.L., Trostle-Weige, P.K., Lin, R., Bhatnagar, Y.M., and Allis, C.D. (1992). Highly acetylated H4 is associated with histone displacement in rat spermatids. Mol. Reprod. Dev. 31, 170-181.
36. Mitchell, M.J., Woods, D.R., Tucker, P.K., Opp, J.S., and Bishop, C.E. (1991). Homology of a candidate spermatogenesis gene from the mouse Y chromosome to the ubiquitin-activating enzyme E1. Nature 354, 483-486.
37. Montelone, B.A., Prakash, S., and Prakash, L. (1981). Recombination and mutagenesis in rad6 mutants of Saccharomyces cerevisiae: evidence for multiple functions of the RAD6 gene. Mol. Gen. Genet. 184, 410-415.
38. Nickel, B.E., Roth, S.Y., Cook, R.G., Allis, C.D., and Davie, J.R. (1987). Changes in the histone H2A variant H2A. Z and polyubiquitinated histone species in developing trout testis. Biochemistry 26, 4417-4421.
39. Oliva, R., and Dixon, G.H. (1991). Vertebrate protamine genes and the histone-to-protamine replacement reaction. Progr. Nucleic Acid Res. Mol. Biol. 40, 25-94.
40. Peterson, M.W., and Gruenhaupt, D. (1992). Protamine interaction with the epithelial cell surface. J. Appl. Physiol. 72, 236-241.
41. Reynolds, P., Koken, M.H.M., Hoeijmakers, J.H.J., Prakash, S., and Prakash, L. (1990). The rhp6+ gene of Schizosaccharomyces pombe: a structural and functional homolog of the RAD6 gene from the distantly related yeast Saccharomyces cerevisiae. EMBO J. 9, 1423-1430.
42. Rhim, J.A., Connor, W., Dixon, G.H., Harendza, C.J., Evenson, D.P., Palmiter, R.D., and Brinster, R.L. (1995). Expression of an avian protamine in transgenic mice disrupts chromatin structure in spermatozoa. Biol. Reprod. 52, 20-32.
43. Riele te, H., Robonus Maandag, E., Clarke, A., Hooper, M., and Berns, A. (1990). Consecutive inactivation of both alleles of the pim-1 proto-oncogene by homologous recombination in embryonic stem cells. Nature 348, 649-651.
44. Roller, M.L., Lossie, A.C., Koken, M.H.M., Smit, E.M.E., Hagemeijer, A., and Camper, S.A. (1995). Localization of sequences related to the human RAD6 DNA repair gene on mouse chromosomes 11 and 13. Mamm. Genome 6, 305-306.
45. Russell, L.D., Ettlin, R.A., Sinha Hikim, A.P., and Clegg, E.D. (1990). Histological and Histopathological Evaluation of the Testis. (Clearwater, Florida: Cache River Press).
46. Scheffner, M., Nuber, U., and Huibregtse, J.M. (1995). Protein ubiquitination involving an E1-E2-E3 enzyme ubiquitin thioester cascade. Nature 373, 81-83.
47. r=17000) is homologous to the yeast DNA repair gene RAD6. EMBO J. 9, 1431-1435.
48. Seufert, W., Futcher, B., and Jentsch, S. (1995). Role of a ubiquitin-conjugating enzyme in degradation of S-and M-phase cyclins. Nature 373, 78-81.
49. Taalman, R.D.F.M., Jaspers, N.G.J., Scheres, J.M.J.C., de Wit, J., and Hustinx, T.J.W. (1983). Hypersensitivity to ionizing radiation, in vitro, in a new chromosomal breakage disorder, the Nijmegen Breakage Syndrome. Mutation Res. 112, 23-32.
50. Thomas, K.R., and Capecchi, M.R. (1987). Site-directed mutagenesis by gene targeting in mouse embryo-derived stem cells. Cell 51, 503-512.
51. Thorne, A.W., Sautiere, P., Briand, G., and Crane-Robinson, C. (1987). The structure of ubiquitinated histone H2B. EMBO J. 6, 1005-1010.
52. Unni, E., Mayerhofer, A., Zhang, Y., Bhatnagar, Y.M., Russell, L.D., and Meistrich, M.L. (1995). Increased accessibility of the N-terminus of testis-specific histone TH2B to antibodies in elongating spermatids. Mol. Reprod. Dev. 42, 210-219.
53. Wing, S.S., and Jain, P. (1995). Molecular cloning, expression and characterization of a ubiquitin enzyme (E217kD) highly expressed in rat testis. Biochem. J. 305, 125-132.
54. Wong, T.-W., Straus, F.H., and Warner, N.E. (1973). Testicular biopsy in the study of male infertility. Arch. Pathol. 95, 151-159.
55. Zhou, X.Y., Morreau, H., Rottier, R., Davis, D., Bonten, E., Gillemans, N., Wenger, D., Grosveld, F.G., Doherty, P., Suzuki, K., et al. (1995). Mouse model for the lysozomal disorder galactosialidosis and correction of the phenotype with overexpressing erythroid precursor cells. Genes Dev. 9, 2623-2634.