Acetylation of core histones in response to HDAC inhibitors is diminished in mitotic HeLa cells

Experimental Cell Research

Volumn 316, Issue 13, 2010, Pages 2123-2135

  Patzlaff, Jason S ^a,d   Terrenoire, Edith ^b,e   Turner, Bryan M ^b   Earnshaw, William C ^c   Paulson, James R ^a  

^a UNIVERSITY OF WISCONSIN OSHKOSH   (United States)

^b UNIVERSITY DEPARTMENT OF MEDICINE   (United Kingdom)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d R and D Systems Inc   (United States)

^e BIRMINGHAM CHILDREN S HOSPITAL NHS FOUNDATION TRUST   (United Kingdom)

Author keywords

Butyrate; HDAC inhibitors; Histone acetylation; Metaphase chromosomes; Mitosis; Protein phosphatases

Indexed keywords

BUTYRIC ACID; HISTONE; HISTONE ACETYLTRANSFERASE; HISTONE DEACETYLASE INHIBITOR; HISTONE H3; HISTONE H4; PHOSPHOPROTEIN PHOSPHATASE INHIBITOR;

ACETYLATION; ARTICLE; CELL CYCLE ARREST; CELL LYSATE; CHROMATIN; CONTROLLED STUDY; ENZYME ACTIVITY; HELA CELL; HUMAN; HUMAN CELL; INTERPHASE; METAPHASE; MITOSIS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

EID: 77953811859     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2010.05.003     Document Type: Article

References (100)

1. Luger K., Mäder A.W., Richmond R.K., Sargent D.F., Richmond T.J. Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature 1997, 389:251-260.
2. Kornberg R.D., Lorch Y. Twenty-five years of the nucleosome, fundamental particle of the eukaryotic chromosome. Cell 1999, 98:285-294.
3. Thoma F., Koller T., Klug A. Involvement of histone H1 in the organization of the nucleosome and of the salt-dependent superstructures of chromatin. J. Cell Biol. 1979, 83:403-427.
4. Robinson P.J., An W., Routh A., Martino F., Chapman L., Roeder R.G., Rhodes D. 30 nm chromatin fibre decompaction requires both H4-K16 acetylation and linker histone eviction. J. Mol. Biol. 2008, 381:816-825.
5. Struhl K. Histone acetylation and transcriptional regulatory mechanisms. Genes Dev. 1998, 12:599-606.
6. Brown C.E., Lechner T., Howe L., Workman J.L. The many HATs of transcription coactivators. Trends Biochem. Sci. 2000, 25:15-19.
7. Sterner D.E., Berger S.L. Acetylation of histones and transcription-related factors. Microbiol. Mol. Biol. Rev. 2000, 64:435-459.
8. Roth S.Y., Denu J.M., Allis C.D. Histone acetyltransferases. Annu. Rev. Biochem. 2001, 70:81-120.
9. Eberharter A., Becker P.B. Histone acetylation: a switch between repressive and permissive chromatin. EMBO Rep. 2002, 3:224-229.
10. Li B., Carey M., Workman J.L. The role of chromatin during transcription. Cell 2007, 128:707-719.
11. Kouzarides T. Chromatin modifications and their function. Cell 2007, 128:693-705.
12. Jackson V., Shires A., Chalkley R., Granner D.K. Studies on highly metabolically active acetylation and phosphorylation of histones. J. Biol. Chem. 1975, 250:4856-4863.
13. Riggs M.G., Whittaker R.G., Neumann J.R., Ingram V.M. n-Butyrate causes histone modification in HeLa and Friend erythroleukaemia cells. Nature 1977, 268:462-464.
14. Vidali G., Boffa L.C., Bradbury E.M., Allfrey V.G. Butyrate suppression of histone deacetylation leads to accumulation of multiacetylated forms of histones H3 and H4 and increased DNase I sensitivity of the associated DNA sequences. Proc. Natl. Acad. Sci. U.S.A. 1978, 75:2239-2243.
15. Sealy L., Chalkley R. The effect of sodium butyrate on histone modification. Cell 1978, 14:115-121.
16. Cousens L.S., Gallwitz D., Alberts B.M. Different accessibilities in chromatin to histone acetylase. J. Biol. Chem. 1979, 254:1716-1723.
17. Yoshida M., Kijima M., Akita M., Beppu T. Potent and specific inhibition of mammalian histone deacetylase both in vivo and in vitro by trichostatin A. J. Biol. Chem. 1990, 265:17174-17179.
18. Darkin-Rattray S.J., Gurnett A.M., Myers R.W., Dulski P.M., Crumley T.M., Allocco J.J., Cannova C., Meinke P.T., Colletti S.L., Bednarek M.A., Singh S.B., Goetz M.A., Dombrowski A.W., Polishook J.D., Schmatz D.M. Apicidin: a novel antiprotozoal agent that inhibits parasite histone deacetylase. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:13143-13147.
19. Kim Y.B., Lee K.H., Sugita K., Yoshida M., Horinouchi S. Oxamflatin is a novel antitumor compound that inhibits mammalian histone deacetylase. Oncogene 1999, 18:2461-2470.
20. Pfiel C.J., Zhang F., Huang E.Y., Guenther M.G., Lazar M.A., Klein P.S. Histone deacetylase is a direct target of valproic acid, a potent anticonvulsant, mood stabilizer and teratogen. J. Biol. Chem. 2001, 276:36734-36741.
21. Schultz B.E., Misialek S., Wu J., Tang J., Conn M.T., Tahilramani R., Wong L. Kinetics and comparative reactivity of human class I and class IIb histone deacetylases. Biochemistry 2004, 43:11083-11091.
22. Sekhavat A., Sun J.-M., Davie J.R. Competitive inhibition of histone deacetylases activity by trichostatin A and butyrate. Biochem. Cell Biol. 2007, 85:751-758.
23. Meinke P.T., Colletti S.L., Doss G., Myers R.W., Gurnett A.M., Dulski P.M., Darkin-Rattray S.J., Allocco J.J., Galuska S., Schmatz D.M., Wyvratt M.J., Fisher M.H. Synthesis of apicidin-derived quinolone derivatives: parasite-selective histone deacetylase inhibitors and antiproliferative agents. J. Med. Chem 2000, 43:4919-4922.
24. D'Anna J.A., Tobey R.A., Barham S.S., Gurley L.R. A reduction in the degree of H4 acetylation during mitosis in Chinese hamster cells. Biochem. Biophys. Res. Commun. 1977, 77:187-194.
25. D'Anna J.A., Tobey R.A., Gurley L.R. Concentration-dependent effects of sodium butyrate in Chinese hamster cells: cell-cycle progression, inner-histone acetylation, histone H1 dephosphorylation, and induction of an H1-like protein. Biochemistry 1980, 19:2656-2671.
26. 0 content during cell cycle progression in the presence of butyrate. Exp. Cell Res. 1983, 147:407-417.
27. Moore M., Jackson V., Sealy L., Chalkley R. Comparative studies on highly metabolically active histone acetylation. Biochim. Biophys. Acta 1979, 561:248-260.
28. Turner B.M. Acetylation and deacetylation of histone H4 continue through metaphase with depletion of more acetylated isoforms and altered site usage. Exp. Cell Res. 1989, 182:206-214.
29. Turner B.M., Fellows G. Specific antibodies reveal ordered and cell-cycle-related use of histone H4 acetylation sites in mammalian cells. Eur. J. Biochem. 1989, 179:131-139.
30. Jeppesen P., Mitchell A., Turner B., Perry P. Antibodies to defined histone epitopes reveal variations in chromatin conformation and underacetylation of centric heterochromatin in human metaphase chromosomes. Chromosoma 1992, 101:322-332.
31. Kruhlak M.J., Hendzel M.J., Fischle W., Bertos N.R., Hameed S., Yan X.-J., Verdin Test E. Regulation of global acetylation in mitosis through loss of histone acetyltransferases and deacetylases from chromatin. J. Biol. Chem. 2001, 276:38307-38319.
32. McManus K.J., Hendzel M.J. The relationship between histone H3 phosphorylation and acetylation throughout the mammalian cell cycle. Biochem. Cell Biol. 2006, 84:640-657.
33. Bonenfant D., Towbin H., Coulot M., Schindler P., Mueller D.R., van Oostrom 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.
34. Chahal S.S., Matthews H.R., Bradbury E.M. Acetylation of histone H4 and its role in chromatin structure and function. Nature 1980, 287:76-79.
35. Waterborg J.H., Matthews H.R. Patterns of histone acetylation in the cell cycle of Physarum polycephalum. Biochemistry 1983, 22:1489-1496.
36. Nadler K.D. Histone acetylation during meiosis in Lilium microsporocytes. Exp. Cell Res. 1976, 101:283-292.
37. Kim J.-M., Liu H., Tazaki M., Nagata M., Aoki F. Changes in histone acetylation during mouse oocyte meiosis. J. Cell Biol. 2003, 162:37-46.
38. Taylor J.H. Nucleic acid synthesis in relation to the cell division cycle. Ann. NY Acad. Sci. 1960, 90:409-421.
39. Prescott D.M., Bender M.A. Synthesis of RNA and protein during mitosis in mammalian tissue culture cells. Exp. Cell Res. 1962, 26:260-268.
40. Baserga R. A study of nucleic acid synthesis in ascites tumor cells by two-emulsion autoradiography. J. Cell Biol. 1962, 12:633-637.
41. Terasima T., Tomach L.J. Growth and nucleic acid synthesis in synchronously dividing populations of HeLa cells. Exp. Cell Res. 1963, 30:344-362.
42. White D.A., Belyaev N.D., Turner B.M. Preparation of site-specific antibodies to acetylated histones. Methods 1999, 19:417-424.
43. Kimura H., Hayashi-Takanaka Y., Goto Y., Takizawa N., Nozaki N. The organization of histone H3 modifications as revealed by a panel of specific monoclonal antibodies. Cell Struct. Funct. 2008, 33:61-73.
44. Medappa K.C., McLean C., Rueckert R.R. On the structure of rhinovirus 1A. Virology 1971, 44:259-270.
45. Paulson J.R., Ciesielski W.A., Schram B.R., Mesner P.W. Okadaic acid induces dephosphorylation of histone H1 in metaphase-arrested HeLa cells. J. Cell. Sci. 1994, 107:267-273.
46. Xeros N. Deoxyriboside control and synchronization of mitosis. Nature 1962, 194:682-683.
47. Paulson J.R. Isolation of chromosome clusters from metaphase-arrested HeLa cells. Chromosoma 1982, 85:571-581.
48. Paulson J.R., Patzlaff J.S., Vallis A.J. Evidence that the endogenous histone H1 phosphatase in HeLa mitotic chromosomes is protein phosphatase 1, not protein phosphatase 2A. J. Cell Sci. 1996, 109:1437-1447.
49. Paulson J.R. Sulfhydryl reagents prevent dephosphorylation and proteolysis of histones in isolated HeLa metaphase chromosomes. Eur. J. Biochem. 1980, 111:89-197.
50. Marsden M.P., Laemmli U.K. Metaphase chromosome structure: evidence for a radial loop model. Cell 1979, 17:849-858.
51. Keohane A.M., O'Neill L.P., Belyaev N.D., Lavender J.S., Turner B.M. X-inactivation and histone H4 acetylation in embryonic stem cells. Devel. Biol. 1996, 180:618-630.
52. Honkanen R.E. Cantharidin, another natural toxin that inhibits the activity of serine/threonine protein phosphatases types 1 and 2A. FEBS Lett. 1993, 330:283-286.
53. Laemmli U.K., Favre M. Maturation of the head of bacteriophage T4. I. DNA packaging events. J. Mol. Biol. 1973, 80:575-599.
54. Panyim S., Chalkley R. High resolution acrylamide gel electrophoresis of histones. Arch. Biochem. Biophys. 1969, 130:337-346.
55. Paulson J.R., Higley L.L. Acid-urea polyacrylamide slab gel electrophoresis of proteins: preventing distortion of gel wells during preelectrophoresis. Anal. Biochem. 1999, 268:157-159.
56. Bonner W.M., Laskey R.A. A film detection method for tritium-labelled proteins and nucleic acids in polyacrylamide gels. Eur. J. Biochem. 1974, 46:83-88.
57. Rao J., Otto W.R. Fluorimetric DNA assay for cell growth estimation. Anal. Biochem. 1992, 207:186-192.
58. Hosokawa Y., Shimomura Y., Harris R.A., Ozawa T. Determination of short-chain acyl-coenzyme A esters by high-performance liquid chromatography. Anal. Biochem. 1986, 153:45-49.
59. Thorne A.W., Kmiciek D., Mitchelson K., Sautiere P., Crane-Robinson C. Patterns of histone acetylation. Eur. J. Biochem. 1990, 193:701-713.
60. D'Anna J.A., Gurley L.R., Deaven L.L. Dephosphorylation of histones H1 and H3 during the isolation of metaphase chromosomes. Nucleic Acids Res. 1978, 5:3195-3207.
61. Ishihara H., Martin B.L., Brautigan D.L., Karaki H., Ozaki H., Kato Y., Fusetani N., Watabe S., Hashimoto K., Uemura D., Hartshorne D.J. Calyculin A and okadaic acid: inhibitors of protein phosphatase activity. Biochem. Biophys. Res. Commun. 1989, 159:871-877.
62. MacKintosh C., Beattie K.A., Klumpp S., Cohen P., Codd G.A. Cyanobacterial microcystin-LR is a potent and specific inhibitor of protein phosphatases 1 and 2A from both mammals and higher plants. FEBS Lett. 1990, 264:187-192.
63. Turner B.M. Histone acetylation and an epigenetic code. Bioessays 2000, 22:836-845.
64. Strahl B.C., Allis C.D. The language of covalent histone modifications. Nature 2000, 403:41-45.
65. Henikoff S. Histone modifications: combinatorial complexity or cumulative simplicity?. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:5308-5309.
66. Shogren-Knaak M., Ishii H., Sun J.-M., Pazin M.J., Davie J.R., Peterson C.L. Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science 2006, 311:844-847.
67. Sciortino S., Gurtner A., Manni I., Fontemaggi G., Dey A., Sacchi A., Ozato K., Piaggio G. The cyclin B1 gene is actively transcribed during mitosis in HeLa cells. EMBO Rep. 2001, 2:1018-1023.
68. Leresche A., Wolf V.J., Gottesfeld J.M. Repression of RNA polymerase II and III transcription during M phase of the cell cycle. Exp. Cell Res. 1996, 29:282-288.
69. Gottesfeld J.M., Forbes D.J. Mitotic repression of the transcriptional machinery. Trends Biochem. Sci. 1997, 22:197-202.
70. Heix J., Vente A., Voit R., Budde A., Michaelidis T.M., Grummt T. Mitotic silencing of human rRNA synthesis: inactivation of the promoter selectivity factor SL1 by cdc2/cyclin B-mediated phosphorylation. EMBO J. 1998, 17:7373-7381.
71. Kuhn A., Vente A., Dorée M., Grummt I. I, Mitotic phosphorylation of the TBP-containing factor SL1 represses ribosomal gene transcription. J. Mol. Biol. 1998, 284:1-5.
72. Dynlacht B.D. Regulation of transcription by proteins that control the cell cycle. Nature 1997, 389:149-152.
73. Long J.J., Leresche A., Kriwacki R.W., Gottesfeld J.M. Repression of TFIIH transcriptional activity and TFIIH-associated cdk7 kinase activity at mitosis. Mol. Cell. Biol. 1998, 18:1467-1576.
74. Shogren-Knaak M., Peterson C.L. Switching on chromatin: mechanistic role of histone H4-K16 acetylation. Cell Cycle 2006, 5:1361-1365.
75. Cimini D., Mattiuzzo M., Torosantucci L., Degrassi F. Histone hyperacetylation in mitosis prevents sister chromatid separation and produces chromosome segregation defects. Mol. Biol. Cell 2003, 14:3821-3833.
76. Vagnarelli P., Hudson D.F., Ribeiro S.A., Trinkle-Mulcahy L., Spence J.M., Lai F., Farr C.J., Lamond A.L., Earnshaw W.C. Condensin and Repo-man PP1 co-operate in the regulation of chromosome architecture during mitosis. Nat. Cell Biol. 2006, 8:1133-1142.
77. Barlev N.A., Poltoratsky V., Owen-Hughes T., Ying C., Liu L., Workman J.L., Berger S.L. Repression of GCN5 histone acetyltransferase activity via bromodomain-mediated binding and phosphorylation by the Ku-DNA-dependent protein kinase complex. Mol. Cell. Biol. 1998, 18:1349-1358.
78. Ait-Si-Ali S., Ramirez S., Barre F.-X., Dkhissi F., Magnaghi-Jaulin L., Girault J.A., Robin P., Knibiehler M., Pritchard L.L., Ducommun B., Trouche D., Harel-Belian A. Histone acetyltransferase activity of CBP is controlled by cyclin-dependent kinases and oncoprotein E1A. Nature 1998, 396:184-186.
79. Ait-Si-Ali S., Carlisi D., Ramirez S., Upegui-Gonzalez L.-C., Duquet A., Robin P., Rudkin B., Harel-Belian A., Trouche D. Phosphorylation by p44 MAP kinase/ERK1 stimulates CBP histone acetyltransferase activity in vitro. Biochem. Biophys. Res. Commun. 1999, 262:157-162.
80. Kumar B.R.P., Swaminathan V., Banerjee S., Kundu T.K. p300-mediated acetylation of human transcriptional coactivator PC4 is inhibited by phosphorylation. J. Biol. Chem. 2001, 276:16804-16809.
81. Yuan L.W., Soh J.W., Weinstein I.B. Inhibition of histone acetyltransferase function of p300 by PKC?. Biochim. Biophys. Acta 2002, 1592:205-211.
82. Kovacs K.A., Steinmann M., Magistretti P.J., Halfon O., Cardinaux J.-R. CCAAT/enhancer-binding protein family members recruit the coactivator CREB-binding protein and trigger its phosphorylation. J. Biol. Chem. 2003, 278:36959-36965.
83. Huang W.-C., Chen C.-C. Akt phosphorylation of p300 at Ser-1834 is essential for its histone acetyltransferase and transcriptional activity. Mol. Cell. Biol. 2005, 25:6592-6602.
84. Chen Y.-J., Wang Y.-N., Chang W.-C. ERK2-mediated C-terminal serine phosphorylation of p300 is vital to the regulation of epidermal growth factor-induced keratin 16 gene expression. J. Biol. Chem. 2007, 282:27215-27228.
85. Lemercier C., Legube G., Caron C., Louwagie M., Garin J., Trouche D., Khochbin S. Tip60 acetyltransferase activity is controlled by phosphorylation. J. Biol. Chem. 2003, 278:4713-4718.
86. Taipale M., Rea S., Richter K., Vilar A., Lichter P., Imhof A., Akhtar A. hMOF histone acetyltransferase is required for histone H4 lysine 16 acetylation in mammalian cells. Mol. Cell Biol. 2005, 25:6798-6810.
87. Rea S., Xouri G., Akhtar A. Males absent on the first (MOF): from flies to humans. Oncogene 2007, 26:5385-5394.
88. Thomas T., Dixon M.P., Kueh A.J., Voss A.K. Mof (MYST1 or KAT8) is essential for progression of embryonic development past the blastocyst stage and required for normal chromatin architecture. Mol. Cell. Biol. 2008, 28:5093-5105.
89. Chen D., Dundr M., Wang C., Leung A., Lamond A., Misteli T., Huang S. Condensed mitotic chromatin is accessible to transcription factors and chromatin structural proteins. J. Cell Biol. 2005, 168:41-54.
90. Turner B.M., O'Neill L.P., Allan I.M. Histone H4 acetylation in human cells. Frequency of acetylation at different sites defined by immunolabeling with site-specific antibodies. FEBS Lett. 1989, 253:141-145.
91. Chicoine L.G., Schulman I.G., Richman R., Cook R.G., Allis C.D. Nonrandom utilization of acetylation sites in histones isolated from Tetrahymena. Evidence for functionally distinct H4 acetylation sites. J. Biol. Chem. 1986, 261:1071-1076.
92. Couppez M., Martin-Ponthieu A., Sautiere P. Histone H4 from cuttlefish testis is sequentially acetylated. Comparison with acetylation of calf thymus histone H4. J. Biol. Chem. 1987, 262:2854-2860.
93. Johnson C.A., White D.A., Lavender J.S., O'Neill L.P., Turner B.M. Human class I histone deacetylase complexes show enhanced catalytic activity in the presence of ATP and co-immunoprecipitate with the ATP-dependent chaperone protein Hsp70. J. Biol. Chem. 2002, 277:9590-9597.
94. Sengupta N., Seto E. Regulation of histone deacetylase activities. J. Cell. Biochem. 2004, 93:57-67.
95. Berndsen C.E., Denu J.M. Catalysis and substrate selection by histone/protein lysine acetyltransferases. Curr. Opin. Struct. Biol. 2008, 18:682-689.
96. Marmorstein R., Trievel R.C. Histone modifying enzymes: structures, mechanisms and specificities. Biochim. Biophys. Acta 2009, 1789:58-68.
97. Smith E.R., Cayrou C., Huang R., Lane W.S., Cote J., Lucchesi J.C. A human protein complex homologous to the Drosophila MSL complex is responsible for the majority of histone H4 acetylation at lysine 16. Mol. Cell. Biol. 2005, 25:9175-9188.
98. Berndsen C.E., Selleck W., McBryant S.J., Hansen J.C., Tan S., Denu J.M. Nucleosome recognition by the Piccolo NuA4 histone acetyltransferase complex. Biochemistry 2007, 46:2091-2099.
99. Berndsen C.E., Tsubota T., Lindner S.E., Lee S., Holton J.M., Kaufman P.D., Keck J.L., Denu J.M. Molecular functions of the histone acetyltransferase chaperone complex Rtt109-Vps75. Nat. Struct. Mol. Biol. 2008, 15:948-956.
100. Fillingham J., Recht J., Silva A.C., Suter B., Emili A., Stagljar I., Krogan N.J., Allis C.D., Keogh M.C., Greenblatt J.F. Chaperone control of the activity and specificity of the histone H3 acetyltransferase Rtt109. Mol. Cell. Biol. 2008, 28:4342-4253.