Mass spectrometry analysis of dynamic post-translational modifications of TH2B during spermatogenesis

Molecular Human Reproduction

Volumn 15, Issue 6, 2009, Pages 373-378

  Lu, Shuang ^a,b   Xie, Yong M ^d   Li, Xin ^b   Luo, Ji ^e   Shi, Xin Q ^c   Hong, Xin ^d   Pan, Ying H ^e   Ma, Xu ^a,b  

^a GRADUATE SCHOOL OF PEKING UNION MEDICAL COLLEGE   (China)

^b WHO Human Reproduction Research Collaborative Center   (China)

^c National Institute Research for Family Planning   (China)

^d BRUKER DALTONIK GMBH   (Germany)

^e INSTITUTE OF PLANT PROTECTION   (China)

Author keywords

Chromatin; Post translational modifications; Spermatogenesis; Testis specific histones; TH2B

Indexed keywords

HISTONE; HISTONE TH2B; UNCLASSIFIED DRUG;

ACETYLATION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EPIGENETICS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HISTONE CODE; LIQUID CHROMATOGRAPHY; MALE; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN METHYLATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; RAT; SPERMATID; SPERMATOCYTE; SPERMATOGENESIS; SPERMATOGONIUM; TANDEM MASS SPECTROMETRY;

ACETYLATION; ANIMALS; CHROMATOGRAPHY, LIQUID; HISTONES; MALE; MASS SPECTROMETRY; METHYLATION; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; RATS; RATS, SPRAGUE-DAWLEY; SPERMATIDS; SPERMATOCYTES; SPERMATOGENESIS; TANDEM MASS SPECTROMETRY;

EID: 65549153107     PISSN: 13609947     EISSN: 14602407     Source Type: Journal    
DOI: 10.1093/molehr/gap028     Document Type: Article

References (34)

1. Altheim BA, Schultz MC. Histone modification governs the cell cycle regulation of a replication-independent chromatin assembly pathway in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 1999;96 1345-1350.
2. Bellve AR. Purification, culture, and fractionation of spermatogenic cells. Methods Enzymol 1993;225:84-113.
3. Black BE, Foltz DR, Chakravarthy S, Luger K, Woods VL Jr, Cleveland DW. Structural determinants for generating centromeric chromatin. Nature 2004;430:578-582.
4. Bonenfant D, Coulot M, Towbin H, Schindler P, van Oostrum J. Characterization of histone H2A and H2B variants and their post-translational modifications by mass spectrometry. Mol Cell Proteomics 2006;5:541-552.
5. Bonenfant D, Towbin H, Coulot M, Schindler P, Mueller DR van Oostrum J. Analysis of dynamic changes in post-translational modifications of human histones during cell cycle by mass spectrometry. Mol Cell Proteomics 2007;6:1917-1932.
6. Cheung P, Allis CD, Sassone-Corsi P. Signaling to chromatin through histone modifications. Cell 2000;103:263-271.
7. Dalal Y, Furuyama T, Vermaak D, Henikoff S. Structure, dynamics, and evolution of centromeric nucleosomes. Proc Natl Acad Sci USA 2007; 104:15974-15981.
8. Daujat S, Zeissler U, Waldmann T, Happel N, Schneider R. HP1 binds specifically to Lys26-methylated histone H1.4, whereas simultaneous Ser27 phosphorylation blocks HP1 binding. J Biol Chem 2005; 280 38090-38095.
9. de la Barre AE, Angelov D, Molla A, Dimitrov S. The N-terminus of histone H2B, but not that of histone H3 or its phosphorylation, is essential for chromosome condensation. EMBO J 2001;20 6383-6393.
10. FischleW,Wang Y, Allis CD. Binary switches and modification cassettes in histone biology and beyond. Nature 2003;425:475-479.
11. Govin J, Lestrat C, Caron C, Pivot-Pajot C, Rousseaux S, Khochbin S. Histone acetylation-mediated chromatin compaction during mouse spermatogenesis. Ernst Schering Res Found Workshop 2006;57 155-172.
12. Govin J, Escoffier E, Rousseaux S, Kuhn L, Ferro M, Thevenon J, Catena R, Davidson I, Garin J, Khochbin S et al. Pericentric heterochromatin reprogramming by new histone variants during mouse spermiogenesis. J Cell Biol 2007;176:283-294.
13. Hirota T, Lipp JJ, Toh BH, Peters JM. Histone H3 serine 10 phosphorylation by Aurora B causes HP1 dissociation from heterochromatin. Nature 2005;438:1176-1180.
14. Johnson L, Mollah S, Garcia BA, Muratore TL, Shabanowitz J, Hunt DF, Jacobsen SE. Mass spectrometry analysis of Arabidopsis histone H3 reveals distinct combinations of post-translational modifications. Nucleic Acids Res 2004;32:6511-6518.
15. Kierszenbaum AL, Rivkin E, Fefer-Sadler S, Mertz JR, Tres LL. Purification, partial characterization, and localization of Sak57, an acidic intermediate filament keratin present in rat spermatocytes, spermatids, and sperm. Mol Reprod Dev 1996;44:382-394.
16. Kimmins S, Crosio C, Kotaja N, Hirayama J, Monaco L, Hoog C van Duin M, Gossen JA, Sassone-Corsi P. Differential functions of the Aurora-B and Aurora-C kinases in mammalian spermatogenesis. Mol Endocrinol 2007;21:726-739.
17. Lee DY, Hayes JJ, Pruss D, Wolffe AP. A positive role for histone acetylation in transcription factor access to nucleosomal DNA. Cell 1993;72:73-84.
18. Lewis JD, Abbott DW, Ausio J. A haploid affair: Core histone transitions during spermatogenesis. Biochem Cell Biol 2003;81:131-140.
19. Meistrich ML, Bucci LR, Trostle-Weige PK, Brock WA. Histone variants in rat spermatogonia and primary spermatocytes. Dev Biol 1985; 112 230-240.
20. Parra MA, Kerr D, Fahy D, Pouchnik DJ, Wyrick JJ. Deciphering the roles of the histone H2B N-terminal domain in genome-wide transcription. Mol Cell Biol 2006;26:3842-3852.
21. Pivot-Pajot C, Caron C, Govin J, Vion A, Rousseaux S, Khochbin S. Acetylation-dependent chromatin reorganization by BRDT, a testis-specific bromodomain-containing protein. Mol Cell Biol 2003; 23:5354-5365.
22. Placek BJ, Gloss LM. The N-terminal tails of the H2A-H2B histones affect dimer structure and stability. Biochemistry 2002;41 14960-14968.
23. Recht J, Osley MA. Mutations in both the structured domain and N-terminus of histone H2B bypass the requirement for Swi-Snf in yeast. EMBO J 1999;18:229-240.
24. Rousseaux S, Caron C, Govin J, Lestrat C, Faure AK, Khochbin S. Establishment of male-specific epigenetic information. Gene 2005; 345:139-153.
25. Sasai K, Katayama H, Stenoien DL, Fujii S, Honda R, Kimura M, Okano Y, Tatsuka M, Suzuki F, Nigg EA et al. Aurora-C kinase is a novel chromosomal passenger protein that can complement Aurora-B kinase function in mitotic cells. Cell Moti Cytoskeleton 2004;59 249-263.
26. Schueler MG, Dunn JM, Bird CP, Ross MT, Viggiano L, Rocchi M, Willard HF, Green ED. Progressive proximal expansion of the primate X chromosome centromere. Proc Natl Acad Sci USA 2005; 102:10563-10568.
27. Shang E, Nickerson HD, Wen D, Wang X, Wolgemuth DJ. The first bromodomain of Brdt, a testis-specific member of the BET sub-family of double-bromodomain-containing proteins, is essential for male germ cell differentiation. Development 2007;134:3507-3515.
28. Smith FF, Tres LL, Kierszenbaum AL. Expression of testis-specific histone genes during the development of rat spermatogenic cells in vitro. Dev Dyn 1992;193:49-57.
29. Tang CJ, Lin CY, Tang TK. Dynamic localization and functional implications of Aurora-C kinase during male mouse meiosis. Dev Biol 2006; 290:398-410.
30. Trostle-Weige PK, Meistrich ML, Brock WA, Nishioka K. Isolation and characterization of TH 3 a germ cell-specific variant of histone 3 in rat testis. J Biol Chem 1984;259:8769-8776.
31. Turner BM. Cellular memory and the histone code. Cell 2002; 111 285-291.
32. West MH, Bonner WM. Histone 2B can be modified by the attachment of ubiquitin. Nucleic Acids Res 1980;8:4671-4680.
33. Zalensky AO, Siino JS, Gineitis AA, Zalenskaya IA, Tomilin NV, Yau P, Bradbury EM. Human testis/sperm-specific histone H2B (hTSH2B). Molecular cloning and characterization. J Biol Chem 2002; 277 43474-43480.
34. Zhang K, Tang H, Huang L, Blankenship JW, Jones PR, Xiang F, Yau PM, Burlingame AL. Identification of acetylation and methylation sites of histone H3 from chicken erythrocytes by high-accuracy matrix-assisted laser desorption ionization-time-of-flight, matrix-assisted laser desorption ionization-postsource decay, and nanoelectrospray ionization tandem mass spectrometry. Anal Biochem 2002;306:259-269.