H3K79 methylation: A new conserved mark that accompanies H4 hyperacetylation prior to histone-to-protamine transition in Drosophila and rat

Biology Open

Volumn 3, Issue 6, 2014, Pages 444-452

  Dottermusch Heidel, Christine ^a   Gärtner, Stefanie M K ^a   Tegeder, Isabel ^a   Rathke, Christina ^a   Barckmann, Bridlin ^a,c   Bartkuhn, Marek ^b   Bhushan, Sudhanshu ^b   Steger, Klaus ^b   Meinhardt, Andreas ^b   Renkawitz Pohl, Renate ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b JUSTUS LIEBIG UNIVERSITY   (Germany)

^c INSTITUTE OF HUMAN GENETICS   (France)

Author keywords

Gpp; Gpp D; Grappa; H4 acetylation; Histone toprotamine transition; Spermiogenesis

Indexed keywords

EID: 84979026048     PISSN: None     EISSN: 20466390     Source Type: Journal    
DOI: 10.1242/bio.20147302     Document Type: Article

References (55)

1. Awe, S. and Renkawitz-Pohl, R. (2010). Histone H4 acetylation is essential to proceed from a histone- to a protamine-based chromatin structure in spermatid nuclei of Drosophila melanogaster. Syst. Biol. Reprod. Med. 56, 44-61.
2. Baarends, W. M., Hoogerbrugge, J. W., Roest, H. P., Ooms, M., Vreeburg, J., Hoeijmakers, J. H. and Grootegoed, J. A. (1999). Histone ubiquitination and chromatin remodeling in mouse spermatogenesis. Dev. Biol. 207, 322-333.
3. Barckmann, B., Chen, X., Kaiser, S., Jayaramaiah-Raja, S., Rathke, C., Dottermusch-Heidel, C., Fuller, M. T. and Renkawitz-Pohl, R. (2013). Three levels of regulation lead to protamine and Mst77F expression in Drosophila. Dev. Biol. 377, 33-45.
4. Barreau, C., Benson, E., Gudmannsdottir, E., Newton, F. and White-Cooper, H. (2008). Post-meiotic transcription in Drosophila testes. Development 135, 1897-1902.
5. Bergmann, M. and Kliesch, S. (1994). The distribution pattern of cytokeratin and vimentin immunoreactivity in testicular biopsies of infertile men. Anat. Embryol. (Berl.) 190, 515-520.
6. Braun, R. E. (2001). Packaging paternal chromosomes with protamine. Nat. Genet. 28, 10-12.
7. Carrell, D. T., Emery, B. R. and Hammoud, S. (2007). Altered protamine expression and diminished spermatogenesis: what is the link? Hum. Reprod. Update 13, 313-327.
8. Chandrasekharan, M. B., Huang, F. and Sun, Z. W. (2010). Histone H2B ubiquitination and beyond: Regulation of nucleosome stability, chromatin dynamics and the trans-histone H3 methylation. Epigenetics 5, 460-468.
9. Chen, D. and McKearin, D. M. (2003). A discrete transcriptional silencer in the bam gene determines asymmetric division of the Drosophila germline stem cell. Development 130, 1159-1170.
10. Chen, X., Hiller, M., Sancak, Y. and Fuller, M. T. (2005). Tissue-specific TAFs counteract Polycomb to turn on terminal differentiation. Science 310, 869-872.
11. Cho, C., Willis, W. D., Goulding, E. H., Jung-Ha, H., Choi, Y. C., Hecht, N. B. and Eddy, E. M. (2001). Haploinsufficiency of protamine-1 or -2 causes infertility in mice. Nat. Genet. 28, 82-86.
12. Daigle, S. R., Olhava, E. J., Therkelsen, C. A., Majer, C. R., Sneeringer, C. J., Song, J., Johnston, L. D., Scott, M. P., Smith, J. J., Xiao, Y. et al. (2011). Selective killing of mixed lineage leukemia cells by a potent small-molecule DOT1L inhibitor. Cancer Cell 20, 53-65.
13. Doyen, C. M., Moshkin, Y. M., Chalkley, G. E., Bezstarosti, K., Demmers, J. A., Rathke, C., Renkawitz-Pohl, R. and Verrijzer, C. P. (2013). Subunits of the histone chaperone CAF1 also mediate assembly of protamine-based chromatin. Cell Rep. 4, 59-65.
14. El-Sharnouby, S., Redhouse, J. and White, R. A. (2013). Genome-wide and cellspecific epigenetic analysis challenges the role of polycomb in Drosophila spermatogenesis. PLoS Genet. 9, e1003842.
15. Feng, Q., Wang, H., Ng, H. H., Erdjument-Bromage, H., Tempst, P., Struhl, K. and Zhang, Y. (2002). Methylation of H3-lysine 79 is mediated by a new family of HMTases without a SET domain. Curr. Biol. 12, 1052-1058.
16. Fenic, I., Hossain, H. M., Sonnack, V., Tchatalbachev, S., Thierer, F., Trapp, J., Failing, K., Edler, K. S., Bergmann, M., Jung, M. et al. (2008). In vivo application of histone deacetylase inhibitor trichostatin-a impairs murine male meiosis. J. Androl. 29, 172-185.
17. Grootegoed, J. A., Baarends, W. M., Roest, H. P. and Hoeijmakers, J. H. (1998). Knockout mouse model and gametogenic failure. Mol. Cell. Endocrinol. 145, 161-166.
18. Hazzouri, M., Pivot-Pajot, C., Faure, A. K., Usson, Y., Pelletier, R., Sèle, B., Khochbin, S. and Rousseaux, S. (2000). Regulated hyperacetylation of core histones during mouse spermatogenesis: involvement of histone deacetylases. Eur. J. Cell Biol. 79, 950-960.
19. Hecht, N. B., Bower, P. A., Waters, S. H., Yelick, P. C. and Distel, R. J. (1986). Evidence for haploid expression of mouse testicular genes. Exp. Cell Res. 164, 183-190.
20. Hime, G. R., Brill, J. A. and Fuller, M. T. (1996). Assembly of ring canals in the male germ line from structural components of the contractile ring. J. Cell Sci. 109, 2779-2788.
21. Howe, L., Brown, C. E., Lechner, T. and Workman, J. L. (1999). Histone acetyltransferase complexes and their link to transcription. Crit. Rev. Eukaryot. Gene Expr. 9, 231-243.
22. Hrdlicka, L., Gibson, M., Kiger, A., Micchelli, C., Schober, M., Schöck, F. and Perrimon, N. (2002). Analysis of twenty-four Gal4 lines in Drosophila melanogaster. Genesis 34, 51-57.
23. Jayaramaiah Raja, S. and Renkawitz-Pohl, R. (2005). Replacement by Drosophila melanogaster protamines and Mst77F of histones during chromatin condensation in late spermatids and role of sesame in the removal of these proteins from the male pronucleus. Mol. Cell. Biol. 25, 6165-6177.
24. Kimmins, S. and Sassone-Corsi, P. (2005). Chromatin remodelling and epigenetic features of germ cells. Nature 434, 583-589.
25. Kleene, K. C. (2003). Patterns, mechanisms, and functions of translation regulation in mammalian spermatogenic cells. Cytogenet. Genome Res. 103, 217-224.
26. Kleene, K. C., Distel, R. J. and Hecht, N. B. (1983). cDNA clones encoding cytoplasmic poly(A)+ RNAs which first appear at detectable levels in haploid phases of spermatogenesis in the mouse. Dev. Biol. 98, 455-464.
27. Klemenz, R., Weber, U. and Gehring, W. J. (1987). The white gene as a marker in a new P-element vector for gene transfer in Drosophila. Nucleic Acids Res. 15, 3947-3959.
28. Kliesch, S., Behre, H. M., Hertle, L. and Bergmann, M. (1998). Alteration of Sertoli cell differentiation in the presence of carcinoma in situ in human testes. J. Urol. 160, 1894-1898.
29. Lacoste, N., Utley, R. T., Hunter, J. M., Poirier, G. G. and Côte, J. (2002). Disruptor of telomeric silencing-1 is a chromatin-specific histone H3 methyltransferase. J. Biol. Chem. 277, 30421-30424.
30. Leduc, F., Maquennehan, V., Nkoma, G. B. and Boissonneault, G. (2008). DNA damage response during chromatin remodeling in elongating spermatids of mice. Biol. Reprod. 78, 324-332.
31. Leser, K., Awe, S., Barckmann, B., Renkawitz-Pohl, R. and Rathke, C. (2012).The bromodomain-containing protein tBRD-1 is specifically expressed in spermatocytes and is essential for male fertility. Biol. Open 1, 597-606.
32. 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.
33. Michiels, F., Buttgereit, D. and Renkawitz-Pohl, R. (1993). An 18-bp element in the 59 untranslated region of the Drosophila beta 2 tubulin mRNA regulates the mRNA level during postmeiotic stages of spermatogenesis. Eur. J. Cell Biol. 62, 66-74.
34. Min,J.,Feng,Q.,Li,Z.,Zhang,Y.andXu,R.M.(2003). Structure of the catalytic domain of human DOT1L, a non-SET domain nucleosomal histone methyltransferase. Cell 112, 711-723.
35. Mohan, M., Herz, H. M., Takahashi, Y. H., Lin, C., Lai, K. C., Zhang, Y., Washburn, M. P., Florens, L. and Shilatifard, A. (2010). Linking H3K79 trimethylation to Wnt signaling through a novel Dot1-containing complex (DotCom). Genes Dev. 24, 574-589.
36. Montellier, E., Boussouar, F., Rousseaux, S., Zhang, K., Buchou, T., Fenaille, F., Shiota, H., Debernardi, A., Héry, P., Curtet, S. et al. (2013). Chromatin-tonucleoprotamine transition is controlled by the histone H2B variant TH2B. Genes Dev. 27, 1680-1692.
37. Morris, C. A., Benson, E. and White-Cooper, H. (2009). Determination of gene expression patterns using in situ hybridization to Drosophila testes. Nat. Protoc. 4, 1807-1819.
38. Ng, H. H., Feng, Q., Wang, H., Erdjument-Bromage, H., Tempst, P., Zhang, Y. and Struhl, K. (2002). Lysine methylation within the globular domain of histone H3 by Dot1 is important for telomeric silencing and Sir protein association. Genes Dev. 16, 1518-1527.
39. Nguyen, A. T. and Zhang, Y. (2011). The diverse functions of Dot1 and H3K79 methylation. Genes Dev. 25, 1345-1358.
40. Oliva, R. (2006). Protamines and male infertility. Hum. Reprod. Update 12, 417-435.
41. Prakash, L. (1989). The structure and function of RAD6 and RAD18 DNA repair genes of Saccharomyces cerevisiae. Genome 31, 597-600.
42. Rathke, C., Baarends, W. M., Jayaramaiah-Raja, S., Bartkuhn, M., Renkawitz, R. and Renkawitz-Pohl, R. (2007). Transition from a nucleosome-based to a protamine-based chromatin configuration during spermiogenesis in Drosophila. J. Cell Sci. 120, 1689-1700.
43. Rathke, C., Barckmann, B., Burkhard, S., Jayaramaiah-Raja, S., Roote, J. and Renkawitz-Pohl, R. (2010). Distinct functions of Mst77F and protamines in nuclear shaping and chromatin condensation during Drosophila spermiogenesis. Eur. J. Cell Biol. 89, 326-338.
44. Rathke, C., Baarends, W. M., Awe, S. and Renkawitz-Pohl, R. (2014). Chromatin dynamics during spermiogenesis. Biochim. Biophys. Acta 1839, 155-168.
45. Renkawitz-Pohl, R., Hollmann, M., Hempel, L. and Schäfer, M. A. (2005).Spermatogenesis. In Comprehensive Molecular Insect Science: Reproduction and Development, Vol. 1 (ed. L. I. Gilbert, K. Iatrou and S. S. Gill), pp. 157-177. Amsterdam: Elsevier.
46. Russell, L. D., Ettlin, R. A., Hikim, A. P. S. and Clegg, E. D. (1990). Histological and Histopathological Evaluation of the Testis. St Louis, MO: Cache River Press.
47. Sassone-Corsi, P. (2002). Unique chromatin remodeling and transcriptional regulation in spermatogenesis. Science 296, 2176-2178.
48. Shanower, G. A., Muller, M., Blanton, J. L., Honti, V., Gyurkovics, H. and Schedl, P. (2005). Characterization of the grappa gene, the Drosophila histone H3 lysine 79 methyltransferase. Genetics 169, 173-184.
49. Sonnack, V., Failing, K., Bergmann, M. and Steger, K. (2002). Expression of hyperacetylated histone H4 during normal and impaired human spermatogenesis. Andrologia 34, 384-390.
50. Steger, K., Fink, L., Failing, K., Bohle, R. M., Kliesch, S., Weidner, W. and Bergmann, M. (2003). Decreased protamine-1 transcript levels in testes from infertile men. Mol. Hum. Reprod. 9, 331-336.
51. Steger, D. J., Lefterova, M. I., Ying, L., Stonestrom, A. J., Schupp, M., Zhuo, D., Vakoc, A. L., Kim, J. E., Chen, J., Lazar, M. A. et al. (2008). DOT1L/KMT4 recruitment and H3K79 methylation are ubiquitously coupled with gene transcription in mammalian cells. Mol. Cell. Biol. 28, 2825-2839.
52. Vakoc, C. R., Sachdeva, M. M., Wang, H. and Blobel, G. A. (2006). Profile of histone lysine methylation across transcribed mammalian chromatin. Mol. Cell. Biol. 26, 9185-9195.
53. Vibranovski, M. D., Lopes, H. F., Karr, T. L. and Long, M. (2009). Stage-specific expression profiling of Drosophila spermatogenesis suggests that meiotic sex chromosome inactivation drives genomic relocation of testis-expressed genes. PLoS Genet. 5, e1000731.
54. Vibranovski, M. D., Chalopin, D. S., Lopes, H. F., Long, M. and Karr, T. L. (2010). Direct evidence for postmeiotic transcription during Drosophila melanogaster spermatogenesis. Genetics 186, 431-433.
55. Wood, A., Schneider, J. and Shilatifard, A. (2005). Cross-talking histones: implications for the regulation of gene expression and DNA repair. Biochem. Cell Biol. 83, 460-467.