Histone H4 lysine 20 mono- and tri-methylation define distinct biological processes in SV40 minichromosomes

Cell Cycle

Volumn 9, Issue 7, 2010, Pages 1320-1332

  Balakrishnan, Lata ^a,b   Gefroh, Amanda ^a   Milavetz, Barry ^a  

^a UNIVERSITY OF NORTH DAKOTA   (United States)

^b UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

Encapsidation; Histone H4 lysine 20; Methylation; Replication; SV40

Indexed keywords

HISTONE H4; LYSINE;

ANIMAL CELL; ARTICLE; CHROMATIN; CONTROLLED STUDY; METHYLATION; MINICHROMOSOME; NONHUMAN; SIMIAN VIRUS 40; VIRION; VIRUS GENOME; VIRUS INFECTION;

EID: 77953597006     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.9.7.11123     Document Type: Article

References (67)

1. Luger KMA, Richmond RK, Sargent DF, Richmond TJ. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 1997; 389:251-60.
2. Fernandez-Capetillo O, Mahadevaiah SK, Celeste A, Romanienko PJ, Camerini-Otero RD, Bonner WM, et al. H2AX is required for chromatin remodeling and inactivation of sex chromosomes in male mouse meiosis. Dev Cell 2003; 4:497-508. (Pubitemid 36437557)
3. TK. Chromatin modifications and their function. Cell 2007 128:693-705.
4. Krogan NJ, Kim M, Tong A, Golshani A, Cagney G, Canadien V, et al. Methylation of histone H3 by Set2 in Saccharomyces cerevisiae is linked to transcriptional elongation by RNA polymerase II. Mol Cell Biol 2003; 23:4207-18.
5. Santos-Rosa H, Schneider R, Bannister AJ, Sherriff J, Bernstein BE, Emre NC, et al. Active genes are tri-methylated at K4 of histone H3. Nature 2002; 419:407-11.
6. Jenuwein T, Allis CD. Translating the histone code. Science 2001; 293:1074-80.
7. Strahl BD, Allis CD. The language of covalent histone modifications. Nature 2000; 403:41-5.
8. Allfrey VGFR, Mirsky AE. Acetylation and methylation of histones and their possible role in the regulation of RNA synthesis. PNAS 1964; 51:786-94.
9. Balakrishnan L, Milavetz B. Histone hyperacetylation in the coding region of chromatin undergoing transcription in SV40 minichromosomes is a dynamic process regulated directly by the presence of RNA polymerase II. J Mol Biol 2007; 365:18-30.
10. Davie JRH, Hendzel MJ. Multiple functions of dynamic histone acetylation. J Cell Biochem 2004; 55:98-105.
11. Shepherd GR, Hardin JM, Noland BJ. Methylation of lysine residues of histone fractions in synchronized mammalian cells. Arch Biochem Biophys 1971; 143:1-5.
12. Clarke S. Protein Methylation. Curr Opin Cell Biol 1993; 5:977-83.
13. Sarg B, Koutzamani E, Helliger W, Rundquist I, Lindner HH. Postsynthetic trimethylation of histone H4 at lysine 20 in mammalian tissues is associated with aging. J Biol Chem 2002; 277:39195-201. (Pubitemid 35190888)
14. Strahl BD, Ohba R, Cook RG, Allis CD. Methylation of histone H3 at lysine 4 is highly conserved and correlates with transcriptionally active nuclei in Tetrahymena. Proc Natl Acad Sci USA 1999; 96:14967-72. (Pubitemid 30019748)
15. Taverna SD, Li H, Ruthenburg AJ, Allis CD, Patel DJ. How chromatin-binding modules interpret histone modifications: lessons from professional pocket pickers. Nat Struct Biol 2007; 14:1025-40. (Pubitemid 350060344)
16. Balakrishnan L, Milavetz B. Histone Hyperacetylation during SV40 Transcription is Regulated By p300 and RNA Polymerase II Translocation. J Mol Biol 2007; 371:1022-37. (Pubitemid 47101823)
17. Balakrishnan L, Milavetz B. HDAC inhibitors stimulate viral transcription by multiple mechanisms. Virol J 2008; 5:43. (Pubitemid 351519243)
18. Allis CD, Jenuwein T, Reinberg D, Caparros ML. Epigenetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY 2007.
19. Schaffhausen BS, Benjamin TL. Deficiency in histone acetylation in nontransforming host range mutants of polyoma virus. PNAS 1976; 73:1092-6.
20. Balakrishnan L, Milavetz B. Programmed remodeling of hyperacetylated histone H4 and H3 organization on the SV40 genome during lytic infection. Virology 2005; 334:111-23. (Pubitemid 40320739)
21. Milavetz B. Hyperacetylation and differential deacetylation of histones H4 and H3 define two distinct classes of acetylated SV40 chromosomes early in infection. Virology 2004; 319:324-36. (Pubitemid 38251272)
22. Kohlmaier A, Savarese F, Lachner M, Martens J, Jenuwein T, Wutz A. A chromosomal memory triggered by Xist regulates histone methylation in X inactivation. PLoS Biol 2004; 2:171. (Pubitemid 39234412)
23. Vakoc CR, Sachdeva MM, Wang H, Blobel GA. Profile of Histone Lysine Methylation across Transcribed Mammalian Chromatin. Mol Cell Biol 2006; 26:9185-95. (Pubitemid 44904415)
24. Vakoc CR, Mandat SA, Olenchock BJ, Blobe GA. Histone H3 Lysine 9 Methylation and HP1γ Are Associated with Transcription Elongation through Mammalian Chromatin. Mol Cell 2005; 19:381-91.
25. Balakrishnan L, Milavetz B. Reorganization of RNA polymerase II on the SV40 genome occurs coordinately with the early to late transcriptional switch. Virology 2006; 345:31-43. (Pubitemid 43107571)
26. Jasencakova ZMA, Walter J, Turner BM, Schubert I. Histone H4 acetylation of euchromatin and heterochromatin is cell cycle dependent and correlated with replication rather than with transcription. Plant Cell 2000; 12:2087-100. (Pubitemid 32053397)
27. Hirt B. Selective extraction of polyoma DNA from infected mouse cell cultures. J Mol Biol 1967; 26:365-9.
28. Biron VL, McManus KJ, Hu N, Hendzel MJ, Underhill DA. Distinct dynamics and distribution of histone methyl-lysine derivatives in mouse development. Dev Biol 2004; 276:337-51. (Pubitemid 39592398)
29. Desrosiers R, Tanguay RM. Methylation of Drosophila histones at proline, lysine, and arginine residues during heat shock. J Biol Chem 1988; 263:4686-92.
30. Garcia BA, Hake SB, Diaz RL, Kauer M, Morris SA, Recht J, et al. Organismal differences in post-translational modifications in histones H3 and H4. J Biol Chem 2007; 282:7641-55. (Pubitemid 47093632)
31. Julien E, Herr W. A switch in mitotic histone H4 lysine 20 methylation status is linked to M phase defects upon loss of HCF-1. Mol Cell 2004; 14:713-25. (Pubitemid 38780846)
32. Karachentsev D, Sarma K, Reinberg D, Steward R. PR-Set7-dependent methylation of histone H4 Lys 20 functions in repression of gene expression and is essential for mitosis. Genes Dev 2005; 19:431-5. (Pubitemid 40256274)
33. Lu X, Simon MD, Chodaparambil JV, Hansen JC, Shokat KM, Luger K. The effect of H3K79 diimethylation and H4K20 trimethylation on nucleosome and chromatin structure. Nat Struct Mol Biol 2008; 15:1122-4.
34. Pannetier M, Julien E, Schotta G, Tardat M, Sardet C, Jenuwein T, et al. PR-SET7 and SUV4-20H regulate H4 lysine-20 methylation at imprinting control regions in the mouse. EMBO Rep 2008; 9:998-1005.
35. Payne C, Braun RE. Histone lysine trimethylation exhibits a distinct perinuclear distribution in Plzf-expressing spermatogonia. Dev Biol 2006; 293:461-72.
36. Sakaguchi A, Karachentsev D, Seth-Pasricha M, Druzhinina M, Steward R. Functional characterization of the Drosophila Hmt4-20/Suv4-20 histone methyltransferase. Genetics 2008; 179:317-22.
37. Sarg B, Helliger W, Talasz H, Koutzamani E, Lindner HH. Histone H4 hyperacetylation precludes histone H4 lysine 20 trimethylation. J Biol Chem 2004; 279:53458-64. (Pubitemid 40051851)
38. Shechter D, Nicklay JJ, Chitta RK, Shabanowitz J, Hunt DF, Allis CD. Analysis of histones in Xenopus laevis I. A distinct index of enriched variants and modifications exists in each cell type and is remodeled during developmental transitions. J Biol Chem 2009; 284:1064-74.
39. Smith KM, Kothe GO, Matsen CB, Khlafallah TK, Adhvaryu KK, Hemphill M, et al. The fungus Neurospora crassa displays telomeric silencing mediated by multiple sirtuins and by methylation of histone H3 lysine 9. Epigenetics Chromatin 2008; 1:5.
40. nd ed. Cold Spring Harbor Laboratory 1981.
41. Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, Wang Z, et al. High-resolution profiling of histone methylations in the human genome. Cell 2007; 129:823-37. (Pubitemid 46802390)
42. Frye M, Fisher AG, Watt FM. Epidermal stem cells are defined by global histone modifications that are altered by Myc-induced differentiation. PLoS ONE 2007; 2:763. (Pubitemid 351385879)
43. Pesavento JJ, Yang H, Kelleher NL, Mizzen CA. Certain and progressive methylation of histone H4 at lysine 20 during the cell cycle. Mol Cell Biol 2008; 28:468-86.
44. Talasz H, Lindner HH, Sarg B, Helliger W. Histone H4-lysine 20 monomethylation is increased in promoter and coding regions of active genes and correlates with hyperacetylation. J Biol Chem 2005; 280:38814-22. (Pubitemid 43853784)
45. Ueberheide B, Mollah S. Deciphering the histone code using mass spectrometry. Int J Mass Spectrom 2007; 259:46-56.
46. Greeson NT, Sengupta R, Arida AR, Jenuwein T, Sanders SL. Di-methyl H4 lysine 20 targets the checkpoint protein Crb2 to sites of DNA damage. J Biol Chem 2008; 283:33168-74.
47. Yang H, Pesavento JJ, Starnes TW, Cryderman DE, Wallrath LL, Kelleher NL, et al. Preferential dimethylation of histone H4 lysine 20 by Suv4-20. J Biol Chem 2008; 283:12085-92.
48. Fang J, Feng Q, Ketel CS, Wang H, Cao R, Xia L, et al. Purification and functional characterization of SET8, a nucleosomal histone H4-lysine 20-specific methyltransferase. Curr Biol 2002; 12:1086-99. (Pubitemid 34766930)
49. Nishioka K, Rice JC, Sarma K, Erdjument-Bromage H, Werner J, Wang Y, et al. PR-Set7 is a nucleosome-specific methyltransferase that modifies lysine 20 of histone H4 and is associated with silent chromatin. Mol Cell 2002; 9:1201-13.
50. Sims JK, Houston SI, Magazinnik T, Rice JC. A transtail histone code defined by monomethylated H4 Lys-20 and H3 Lys-9 demarcates distinct regions of silent chromatin. J Biol Chem 2006; 281:12760-6.
51. Delaval K, Govin J, Cerqueira F, Rousseaux S, Khochbin S, Feil R. Differential histone modifications mark mouse imprinting control regions during spermatogenesis. EMBO J 2007; 26:720-9.
52. Knehr M, Poppe M, Enulescu M, Eickelbaum W, Stoehr M, Schroeter D, et al. A critical appraisal of synchronization methods applied to achieve maximal enrichment of HeLa cells in specific cell cycle phases. Exp Cell Res 1995; 217:546-53.
53. Kourmouli N, Jeppesen P, Mahadevhaiah S, Burgoyne P, Wu R, Gilbert DM, et al. Heterochromatin and trimethylated lysine 20 of histone H4 in animals. J Cell Sci 2004; 117:2491-501.
54. Kourmouli N, Sun YM, van der Sar S, Singh PB, Brown JP. Epigenetic regulation of mammalian pericentric heterochromatin in vivo by HP1. Biochem Biophys Res Commun 2005; 337:901-7. (Pubitemid 41446999)
55. Schotta G, Lachner M, Sarma K, Ebert A, Sengupta R, Reuter G, et al. A silencing pathway to induce H3-K9 and H4-K20 trimethylation at constitutive heterochromatin. Genes Dev 2004; 18:1251-62. (Pubitemid 38720593)
56. Chodaparambil JV, Barbera AJ, Lu X, Kaye KM, Hansen JC, Luger K. A charged and contoured surface on the nucleosome regulates chromatin compaction. Nat Struct Mol Biol 2007; 14:1105-7. (Pubitemid 350060342)
57. Dorigo B, Schalch T, Kulangara A, Duda S, Schroeder RR, Richmond TJ. Nucleosome arrays reveal the two-start organization of the chromatin fiber. Science 2004; 306:1571-3. (Pubitemid 39564956)
58. Shogren-Knaak M, Ishii H, Sun JM, Pazin MJ, Davie JR, Peterson CL. Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science 2006; 311:844-7. (Pubitemid 43228847)
59. Zhou J, Fan JY, Rangasamy D, Tremethick DJ. The nucleosome surface regulates chromatin compaction and couples it with transcriptional repression. Nat Struct Mol Biol 2007; 14:1070-6. (Pubitemid 350060339)
60. Zhang Y, Reinberg D. Transcription regulation by histone methylation: interplay between different covalent modifications of the core histone tails. Genes Dev 2001; 15:2343-60. (Pubitemid 32899739)
61. Kan J, Zou L, Zhang J, Wu R, Wang Z, Liang C. Origin recognition complex (ORC) mediates histone 3 lysine 4 methylation through cooperation with Spp1 in Saccharomyces cerevisiae. J Biol Chem 2008; 283:33803-7.
62. Rice JC, Nishioka K, Sarma K, Steward R, Reinberg D, Allis CD. Mitotic-specific methylation of histone H4 Lys 20 follows increased PR-Set7 expression and its localization to mitotic chromosomes. Genes Dev 2002; 16:2225-30. (Pubitemid 35013085)
63. Friez M, Hermansen R, Milavetz B. Chromatin structure of the simian virus 40 late promoter: a deletional analysis. J Virol 1999; 73:1990-7. (Pubitemid 29098101)
64. Hermansen R, Sierra MA, Johnson J, Friez M, Milavetz B. Identification of Simian virus 40 promoter DNA sequences capable of conferring restriction endonuclease hypersensitivity. J Virol 1996; 70:3416-22. (Pubitemid 26157324)
65. Brady JN, Winston VD, Consigli RA. Dissociation of polyoma virus by the chelation of calcium ions found associated with purified virions. J Virol 1977; 3:717-24.
66. IJpenberg A, Tan NS, Gelman L, Kersten S, Seydoux J, Xu J, et al. In vivo activation of PPAR target genes by RXR homodimers. EMBO J 2004; 23:2083-91.
67. Milavetz BI. SP1 and AP-1 elements direct chromatin remodeling in SV40 chromosomes during the first 6 hours of infection. Virology 2002; 294:170-9.