H2B Tyr37 phosphorylation suppresses expression of replication-dependent core histone genes

Nature Structural and Molecular Biology

Volumn 19, Issue 9, 2012, Pages 930-937

  Mahajan, Kiran ^a   Fang, Bin ^a   Koomen, John M ^a   Mahajan, Nupam P ^a,b  

^a H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF SOUTH FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE; HISTONE CLUSTER 1; HISTONE H2B; PHOSPHOTRANSFERASE; RNA POLYMERASE II; TYROSINE; UNCLASSIFIED DRUG; WEE1 KINASE;

ANIMAL CELL; ARTICLE; CELL CYCLE S PHASE; CONTROLLED STUDY; ENZYME INHIBITION; EPIGENETICS; GENE CLUSTER; GENE EXPRESSION; GENE REPLICATION; GENETIC TRANSCRIPTION; MAMMAL CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; YEAST CELL;

ANIMALS; CELL CYCLE PROTEINS; CELL LINE; GENE EXPRESSION REGULATION, FUNGAL; HISTONE CHAPERONES; HISTONES; HUMANS; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN-TYROSINE KINASES; RNA POLYMERASE II; S PHASE; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTIONAL ACTIVATION; TYROSINE;

MAMMALIA;

EID: 84866112974     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2356     Document Type: Article

References (58)

1. Marzluff, W.F., Gongidi, P., Woods, K.R., Jin, J. & Maltais, L.J. The human and mouse replication-dependent histone genes. Genomics 80, 487-498 (2002).
2. Heintz, N., Sive, H.L. & Roeder, R.G. Regulation of human histone gene expression: kinetics of accumulation and changes in the rate of synthesis and in the half-lives of individual histone mRNAs during the HeLa cell cycle. Mol. Cell. Biol. 3, 539-550 (1983).
3. Osley, M.A. The regulation of histone synthesis in the cell cycle. Annu. Rev. Biochem. 60, 827-861 (1991).
4. Borun, T.W., Gabrielli, F., Ajiro, K., Zweidler, A. & Baglioni, C. Further evidence of transcriptional and translational control of histone messenger RNA during the HeLa S3 cycle. Cell 4, 59-67 (1975).
5. Hereford, L., Bromley, S. & Osley, M.A. Periodic transcription of yeast histone genes. Cell 30, 305-310 (1982).
6. Hereford, L.M., Osley, M.A., Ludwig, T.R. II & McLaughlin, C.S. Cell-cycle regulation of yeast histone mRNA. Cell 24, 367-375 (1981).
7. Osley, M.A. & Hereford, L. Identifcation of a sequence responsible for periodic synthesis of yeast histone 2A mRNA. Proc. Natl. Acad. Sci. USA 79, 7689-7693 (1982).
8. Osley, M.A. & Lycan, D. Trans-acting regulatory mutations that alter transcription of Saccharomyces cerevisiae histone genes. Mol. Cell. Biol. 7, 4204-4210 (1987).
9. Marzluff, W.F., Wagner, E.J. & Duronio, R.J. Metabolism and regulation of canonical histone mRNAs: life without a poly(A) tail. Nat. Rev. Genet. 9, 843-854 (2008).
10. Takayama, Y. et al. Hsk1-and SCF(Pof3)-dependent proteolysis of S. pombe Ams2 ensures histone homeostasis and centromere function. Dev. Cell 18, 385-396 (2010).
11. Matsumoto, S., Yanagida, M. & Nurse, P. Histone transcription in cell cycle mutants of fssion yeast. EMBO J. 6, 1093-1097 (1987).
12. Singh, R.K. & Gunjan, A. Histone tyrosine phosphorylation comes of age. Epigenetics 6, 153-160 (2011).
13. Berger, S.L. Cell signaling and transcriptional regulation via histone phosphorylation. Cold Spring Harb. Symp. Quant. Biol. 75, 23-26 (2010).
14. Russell, P. & Nurse, P. Negative regulation of mitosis by wee1+, a gene encoding a protein kinase homolog. Cell 49, 559-567 (1987).
15. Featherstone, C. & Russell, P. Fission yeast p107wee1 mitotic inhibitor is a tyrosine/serine kinase. Nature 349, 808-811 (1991).
16. McGowan, C.H. & Russell, P. Cell cycle regulation of human WEE1. EMBO J. 14, 2166-2175 (1995).
17. Lundgren, K. et al. mik1 and wee1 cooperate in the inhibitory tyrosine phosphorylation of cdc2. Cell 64, 1111-1122 (1991).
18. Hirai, H. et al. Small-molecule inhibition of Wee1 kinase by MK-1775 selectively sensitizes p53-defcient tumor cells to DNA-damaging agents. Mol. Cancer Ther. 8, 2992-3000 (2009).
19. Mahajan, K. et al. Ack1 mediated AKT/PKB tyrosine 176 phosphorylation regulates its activation. PLoS ONE 5, e9646 (2010).
20. Kim, T.H. et al. A high-resolution map of active promoters in the human genome. Nature 436, 876-880 (2005).
21. Albig, W. & Doenecke, D. The human histone gene cluster at the D6S105 locus. Hum. Genet. 101, 284-294 (1997).
22. Albig, W., Kioschis, P., Poustka, A., Meergans, K. & Doenecke, D. Human histone gene organization: nonregular arrangement within a large cluster. Genomics 40, 314-322 (1997).
23. Wang, Z.F. et al. Characterization of the mouse histone gene cluster on chromosome 13: 45 histone genes in three patches spread over 1 Mb. Genome Res. 6, 688-701 (1996).
24. Mahajan, K. et al. Effect of Ack1 tyrosine kinase inhibitor on ligand-independent androgen receptor activity. Prostate 70, 1274-1285 (2010).
25. Mahajan, K. et al. Ack1-mediated androgen receptor phosphorylation modulates radiation resistance in castration-resistant prostate cancer. J. Biol. Chem. 287, 22112-22122 (2012).
26. Kouzarides, T. Chromatin modifcations and their function. Cell 128, 693-705 (2007).
27. Berger, S.L. The complex language of chromatin regulation during transcription. Nature 447, 407-412 (2007).
28. Laribee, R.N., Fuchs, S.M. & Strahl, B.D. H2B ubiquitylation in transcriptional control: a FACT-fnding mission. Genes Dev. 21, 737-743 (2007).
29. Bungard, D. et al. Signaling kinase AMPK activates stress-promoted transcription via histone H2B phosphorylation. Science 329, 1201-1205 (2010).
30. Robzyk, K., Recht, J. & Osley, M.A. Rad6-dependent ubiquitination of histone H2B in yeast. Science 287, 501-504 (2000).
31. Gardner, K.E., Zhou, L., Parra, M.A., Chen, X. & Strahl, B.D. Identifcation of lysine 37 of histone H2B as a novel site of methylation. PLoS ONE 6, e16244 (2011).
32. Tsukuda, T., Fleming, A.B., Nickoloff, J.A. & Osley, M.A. Chromatin remodelling at a DNA double-strand break site in Saccharomyces cerevisiae. Nature 438, 379-383 (2005).
33. Nakanishi, S. et al. A comprehensive library of histone mutants identifes nucleosomal residues required for H3K4 methylation. Nat. Struct. Mol. Biol. 15, 881-888 (2008).
34. Booher, R.N., Deshaies, R.J. & Kirschner, M.W. Properties of Saccharomyces cerevisiae wee1 and its differential regulation of p34CDC28 in response to G1 and G2 cyclins. EMBO J. 12, 3417-3426 (1993).
35. Mollapour, M. et al. Swe1Wee1-dependent tyrosine phosphorylation of Hsp90 regulates distinct facets of chaperone function. Mol. Cell 37, 333-343 (2010).
36. Wei, Y., Jin, J. & Harper, J.W. The cyclin E/Cdk2 substrate and Cajal body component p220(NPAT) activates histone transcription through a novel LisH-like domain. Mol. Cell. Biol. 23, 3669-3680 (2003).
37. Zhao, J. et al. NPAT links cyclin E-Cdk2 to the regulation of replication-dependent histone gene transcription. Genes Dev. 14, 2283-2297 (2000).
38. Osley, M.A., Gould, J., Kim, S., Kane, M.Y. & Hereford, L. Identifcation of sequences in a yeast histone promoter involved in periodic transcription. Cell 45, 537-544 (1986).
39. Xu, H., Kim, U.J., Schuster, T. & Grunstein, M. Identifcation of a new set of cell cycle-regulatory genes that regulate S-phase transcription of histone genes in Saccharomyces cerevisiae. Mol. Cell. Biol. 12, 5249-5259 (1992).
40. Prochasson, P., Florens, L., Swanson, S.K., Washburn, M.P. & Workman, J.L. The HIR corepressor complex binds to nucleosomes generating a distinct protein/DNA complex resistant to remodeling by SWI/SNF. Genes Dev. 19, 2534-2539 (2005).
41. Green, E.M. et al. Replication-independent histone deposition by the HIR complex and Asf1. Curr. Biol. 15, 2044-2049 (2005).
42. Dimova, D., Nackerdien, Z., Furgeson, S., Eguchi, S. & Osley, M.A. A role for transcriptional repressors in targeting the yeast Swi/Snf complex. Mol. Cell 4, 75-83 (1999).
43. Sherwood, P.W., Tsang, S.V. & Osley, M.A. Characterization of HIR1 and HIR2, two genes required for regulation of histone gene transcription in Saccharomyces cerevisiae. Mol. Cell. Biol. 13, 28-38 (1993).
44. Spector, M.S., Raff, A., DeSilva, H., Lee, K. & Osley, M.A. Hir1p and Hir2p function as transcriptional corepressors to regulate histone gene transcription in the Saccharomyces cerevisiae cell cycle. Mol. Cell. Biol. 17, 545-552 (1997).
45. Fillingham, J. et al. Two-color cell array screen reveals interdependent roles for histone chaperones and a chromatin boundary regulator in histone gene repression. Mol. Cell 35, 340-351 (2009).
46. Kaufman, P.D., Cohen, J.L. & Osley, M.A. Hir proteins are required for position-dependent gene silencing in Saccharomyces cerevisiae in the absence of chromatin assembly factor I. Mol. Cell. Biol. 18, 4793-4806 (1998).
47. Yamane, K. et al. Asf1/HIRA facilitate global histone deacetylation and associate with HP1 to promote nucleosome occupancy at heterochromatic loci. Mol. Cell 41, 56-66 (2011).
48. Nelson, D.M. et al. Coupling of DNA synthesis and histone synthesis in S phase independent of cyclin/cdk2 activity. Mol. Cell. Biol. 22, 7459-7472 (2002).
49. Xiao, A. et al. WSTF regulates the H2A.X DNA damage response via a novel tyrosine kinase activity. Nature 457, 57-62 (2009).
50. Cook, P.J. et al. Tyrosine dephosphorylation of H2AX modulates apoptosis and survival decisions. Nature 458, 591-596 (2009).
51. Dawson, M.A. et al. JAK2 phosphorylates histone H3Y41 and excludes HP1alpha from chromatin. Nature 461, 819-822 (2009).
52. Singh, R.K., Kabbaj, M.H., Paik, J. & Gunjan, A. Histone levels are regulated by phosphorylation and ubiquitylation-dependent proteolysis. Nat. Cell Biol. 11, 925-933 (2009).
53. Dollard, C., Ricupero-Hovasse, S.L., Natsoulis, G., Boeke, J.D. & Winston, F. SPT10 and SPT21 are required for transcription of particular histone genes in Saccharomyces cerevisiae. Mol. Cell. Biol. 14, 5223-5228 (1994).
54. Hess, D., Liu, B., Roan, N.R., Sternglanz, R. & Winston, F. Spt10-dependent transcriptional activation in Saccharomyces cerevisiae requires both the Spt10 acetyltransferase domain and Spt21. Mol. Cell. Biol. 24, 135-143 (2004).
55. Yates, J.R. III, Eng, J.K., McCormack, A.L. & Schieltz, D. Method to correlate tandem mass spectra of modifed peptides to amino acid sequences in the protein database. Anal. Chem. 67, 1426-1436 (1995).
56. Perkins, D.N., Pappin, D.J., Creasy, D.M. & Cottrell, J.S. Probability-based protein identifcation by searching sequence databases using mass spectrometry data. Electrophoresis 20, 3551-3567 (1999).
57. Mahajan, N.P. et al. Activated Cdc42-associated kinase Ack1 promotes prostate cancer progression via androgen receptor tyrosine phosphorylation. Proc. Natl. Acad. Sci. USA 104, 8438-8443 (2007).
58. Mahajan, N.P., Whang, Y.E., Mohler, J.L. & Earp, H.S. Activated tyrosine kinase Ack1 promotes prostate tumorigenesis: role of Ack1 in polyubiquitination of tumor suppressor Wwox. Cancer Res. 65, 10514-10523 (2005).