Histone ubiquitination and chromatin remodeling in mouse spermatogenesis

Developmental Biology

Volumn 207, Issue 2, 1999, Pages 322-333

  Baarends, Willy M ^a,b   Hoogerbrugge, Jos W ^a,b   Roest, Henk P ^a,b   Ooms, Marja ^a,b   Vreeburg, Jan ^a,b   Hoeijmakers, Jan H J ^a,b   Grootegoed, J Anton ^a,b  

^a ERASMUS UNIVERSITY ROTTERDAM   (Netherlands)

^b ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

Chromatin; Histone ubiquitination; Protamine; RAD6; Sex body; Spermatogenesis; Testis; Ubiquitin

Indexed keywords

HISTONE; UBIQUITIN;

ANIMAL EXPERIMENT; ARTICLE; CHROMATIN STRUCTURE; DNA REPAIR; IMMUNOBLOTTING; MALE; MALE INFERTILITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY; SPERMATOGENESIS; SPOROGENESIS; TRANSCRIPTION REGULATION;

ANIMALIA; MAMMALIA; SACCHAROMYCES CEREVISIAE;

EID: 0033559541     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1006/dbio.1998.9155     Document Type: Article

References (52)

1. Agell N., Chiva M., Mezquita C. Changes in nuclear content of protein conjugate histone H2A-ubiquitin during rooster spermatogenesis. FEBS Lett. 155:1983;209-212.
2. Agell N., Mezquita C. Cellular content of ubiquitin and formation of ubiquitin conjugates during chicken spermatogenesis. Biochem. J. 250:1988;883-889.
3. Alami-Ouahabi B., Veilluex S., Meistrich M. L., Boissonneault G. The testis-specific high-mobility-group protein, a phosphorylation-dependent DNA-packaging factor of elongating and condensing spermatids. Mol. Cell. Biol. 16:1996;3720-3729.
4. Baarends W. M., Roest H. P., Hoogerbrugge J. W., Hendriksen P. J. M., Hoeijmakers J. H. J., Grootegoed J. A. Chromatin structure and gene expression during spermatogenesis. Testicular Function: From Gene Expression to Genetic Manipulation. 1998;Springer-Verlag, Berlin. p. 83-103.
5. Boissonneault G., Lau Y.-F. A testis-specific gene encoding a nuclear high-mobility-group box protein located in elongating spermatids. Mol. Cell. Biol. 13:1993;4323-4330.
6. Brown G. M., Furlong R. A., Sargent C. A., Erickson R. P., Longepied G., Mitchell M., Jones M. H., Hargreave T. B., Cooke H. J., Affara N. A. Characterisation of the coding sequence and fine mapping of the human DFFRY gene and comparative expression analysis and mapping to the Sxrb interval of the mouse Y chromosome of the Dffry gene. Hum. Mol. Genet. 7:1998;97-107.
7. Chen H. Y., Sun J. M., Zhang Y., Davie J. R., Meistrich M. L. Ubiquitination of histone H3 in elongating spermatids of rat testes. J. Biol. Chem. 273:1998;13165-13169.
8. Davie J. R. Two-dimensional gel systems for rapid histone analysis for use in minislab polyacrylamide gel electrophoresis. Anal. Biochem. 120:1982;276-281.
9. Davie J. R., Lin R., Allis C. D. Timing of the appearance of ubiquitinated histones in developing new macronuclei of Tetrahymena thermophila. Biochem. Cell. Biol. 69:1991;66-71.
10. Davie J. R., Murphy L. C. Level of ubiquitinated histone H2B in chromatin is coupled to ongoing transcription. Biochemistry. 29:1990;4752-4757.
11. Davie J. R., Murphy L. C. Inhibition of transcription selectively reduces the level of ubiquitinated histone H2B in chromatin. Biochem. Biophys. Res. Commun. 203:1994;344-350.
12. Drabent B., Bode C., Bramlage B., Doenecke D. Expression of the mouse testicular histone H1t during spermatogenesis. Histochem. Cell. Biol. 106:1996;247-251.
13. Grootegoed J. A., Jansen R., van der Molen H. J. Effect of glucose on ATP dephosphorylation in rat spermatids. J. Reprod. Fertil. 77:1986;99-107.
14. Haas A. L., Bright Reback P., Chau V. Ubiquitin conjugation by the yeast RAD6 and CDC34 gene products. J. Biol. Chem. 266:1991;5104-5112.
15. Henchoz S., De Rubertis F., Pauli D., Spierer P. The dose of a putative ubiquitin-specific protease affects position-effect variegation inDrosophila melanogaster. Mol. Cell. Biol. 16:1996;5717-5725.
16. 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., Grootegoed J. A. Postmeiotic transcription of X and Y chromosomal genes during spermatogenesis in the mouse. Dev. Biol. 170:1995;730-733.
17. Huang H., Kahana A., Gottschling D. E., Prakash L., Liebman S. W. The ubiquitin-conjugating enzyme Rad6 (Ubc2) is required for silencing inSaccharomyces cerevisiae. Mol. Cell. Biol. 17:1997;6693-6699.
18. Izquierdo M. Ubiquitin genes and ubiquitin protein location in polytene chromosomes ofDrosophila. Chromosoma. 103:1994;193-197.
19. Jentsch S., McGrath J. P., Varshavsky A. The yeast DNA repair gene RAD6 encodes a ubiquitin-conjugating enzyme. Nature. 329:1987;131-134.
20. Jones M. H., Furlong R. A., Burkin H., Chalmers I. J., Brown G. M., Khwaja O., Affara N. A. TheDrosophila. Hum. Mol. Genet. 5:1996;1695-1701.
21. Kajimoto Y., Hashimoto T., Shirai Y., Nishino N., Kuno T., Tanaka C. cDNA cloning and tissue distribution of a rat ubiquitin carboxyl-terminal hydrolase PGP9.5. J. Biochem. 112:1992;28-32.
22. Koken M. H., Reynolds P., Jaspers-Dekker L., Prakash L., Prakash S., Bootsma D., Hoeijmakers J. H. J. Structural and functional conservation of two human homologs of the yeast DNA repair gene RAD6. Proc. Natl. Acad. Sci. USA. 88:1991;8865-8869.
23. Koken M. H. M., Hoogerbrugge J. W., Jaspers-Dekker I., de Wit J., Willemsen R., Roest H. P., Grootegoed J. A., Hoeijmakers J. H. J. Expression of the ubiquitin-conjugating DNA repair enzymes HHR6A and B suggests a role in spermatogenesis and chromatin modification. Dev. Biol. 173:1996;119-132.
24. Kovalenko O. V., Plug A. W., Haaf T., Gonda D. K., Ashley T., Ward D. C., Radding C. M., Golub E. I. Mammalian ubiquitin-conjugating enzyme Ubc9 interacts with Rad51 recombination protein and localizes in synaptonemal complexes. Proc. Natl. Acad. Sci. USA. 93:1996;2958-2963.
25. Lanneau M., Loir M. An electrophoretic investigation of mammalian spermatid-specific nuclear proteins. J. Reprod. Fertil. 65:1982;163-170.
26. Lawrence C. TheRAD6Saccharomyces cerevisiae: Bioessays. 16:1994;253-258.
27. Li W., Nagaraja S., Delcuve G. P., Hendzel M. J., Davie J. R. Effects of histone acetylation, ubiquitination and variants on nucleosome stability. Biochem. J. 296:1993;737-744.
28. Matsui S. I., Seon B. K., Sandberg A. A. Disappearance of a structural chromatin protein A24 in mitosis: Implications for molecular basis of chromatin condensation. Proc. Natl. Acad. Sci. USA. 76:1979;6386-6390.
29. Matsui S., Sandberg A. A., Negoro S., Seon B. K., Goldstein G. Isopeptidase: A novel eukaryotic enzyme that cleaves isopeptide bonds. Proc. Natl. Acad. Sci. USA. 79:1982;1535-1539.
30. Meistrich M. L., Bruce W. R., Clermont Y. Cellular composition of fractions of mouse testis cells following velocity sedimentation separation. Exp. Cell Res. 79:1973;213-227.
31. Meistrich M. L., Trostle-Weige P. K., Lin R., Bhatnagar Y. M., Allis C. D. Highly acetylated H4 is associated with histone displacement in rat spermatids. Mol. Reprod. Dev. 31:1992;170-181.
32. Mezquita J., Pau M., Mezquita C. Heat-shock inducible polyubiquitin gene UbI undergoes alternative initiation and alternative splicing in mature chicken testes. Mol. Reprod. Dev. 46:1997;471-475.
33. Moazed D., Johnson D. A deubiquitinating enzyme interacts with SIR4 and regulates silencing inS. cerevisiae. Cell. 86:1996;667-677.
34. Monesi V. Differential rate of ribonucleic acid synthesis in the autosomes and sex chromosomes during male meiosis in the mouse. Chromosoma. 17:1965;11-21.
35. Nickel B. E., Roth S. Y., Cook R. G., Allis C. D., Davie J. R. Changes in the histone H2A variant H2A. Z and polyubiquitinated histone species in developing trout testis. Biochemistry. 26:1987;4417-4421.
36. Nickel B. E., Allis C. D., Davie J. R. Ubiquitinated histone H2B is preferentially located in transcriptionally active chromatin. Biochemistry. 28:1989;958-963.
37. Oliva R., Dixon G. H. Vertebrate protamine genes and the histone-to-protamine replacement reaction. Prog. Nucleic Acid Res. Mol. Biol. 40:1991;25-94.
38. Oud J. L., de Jong J. H., de Rooij D. G. A sequential analysis of meiosis in the male mouse using a restricted spermatocyte population obtained by a hydroxyurea/triaziquone treatment. Chromosoma. 71:1979;237-248.
39. Peters A. H., Plug A. W., van Vugt M. J., de Boer P. A drying-down technique for the spreading of mammalian meiocytes from the male and female germline. Chromosome Res. 5:1997;66-68.
40. Roest H. P., Klaveren van J., de Wit J., van Gurp C. G., Koken M. H. M., Vermey M., Roijen van J. H., Vreeburg J. T. M., Baarends W. M., Bootsma D. et al. Inactivation of the HR6B ubiquitin-conjugating DNA repair enzyme in mice causes a defect in spermatogenesis associated with chromatin modification. Cell. 86:1996;799-810.
41. Swerdlow P. S., Schuster T., Finley D. A conserved sequence in histone H2A which is a ubiquitination site in higher eucaryotes is not required for growth inSaccharomyces cerevisiae. Mol. Cell. Biol. 10:1990;4905-4911.
42. Unni E., Mayerhofer A., Zhang Y., Bhatnagar Y. M., Russell L. D., Meistrich M. K. Increased accessibility of the N-terminus of testis-specific histone TH2B to antibodies in elongating spermatids. Mol. Reprod. Dev. 42:1995;210-219.
43. Varshavsky A. The ubiquitin system. Trends Biochem. Sci. 22:1997;383-387.
44. Vassilev A. P., Rasmussen H. H., Christensen E. I., Nielsen S., Celis J. E. The levels of ubiquitinated histone H2A are highly upregulated in transformed human cells: Partial colocalization of uH2A clusters and PCNA/cyclin foci in a fraction of cells in S-phase. J. Cell Sci. 108:1995;1205-1215.
45. Ward W. S., Coffey D. S. DNA packaging and organization in mammalian spermatozoa: Comparison with somatic cells. Biol. Reprod. 44:1991;569-574.
46. West M. H., Bonner W. M. Histone 2A, a heteromorphous family of eight protein species. Biochemistry. 19:1980;3238-3245.
47. Wilkinson K. D. Regulation of ubiquitin-dependent processes by deubiquitinating enzymes. FASEB J. 11:1997;1245-1256.
48. 17kD. Biochem. J. 305:1995;125-132.
49. Wing S. S., Bédard Morales, C. Hingamp, P. and Trasler. A novel rat homolog of theSaccharomyces cerevisiae. Mol. Cell. Biol. 16:1996;4064-4072.
50. Wu R. S., Kohn K. W., Bonner W. M. Metabolism of ubiquitinated histones. J. Biol. Chem. 256:1981;5916-5920.
51. Yamaguchi T., Kim N. S., Sekine S., Seino H., Osaka F., Yamao F., Kato S. Cloning and expression of cDNA encoding a human ubiquitin-conjugating enzyme similar to theDrosophila. J. Biochem. 120:1996;494-497.
52. Yasugi T., Howley P. M. Identification of the structural and functional human homolog of the yeast ubiquitin-conjugating enzyme UBC9. Nucleic Acids Res. 24:1996;2005-2010.