At1 receptor induced alterations in histone H2A reveal novel insights into GPCR control of chromatin remodeling

PLoS ONE

Volumn 5, Issue 9, 2010, Pages 1-13

  Jagannathan, Rajaganapathi ^a   Kaveti, Suma ^a   Desnoyer, Russell W ^a   Willard, Belinda ^a   Kinter, Michael ^a   Karnik, Sadashiva S ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN 1 RECEPTOR; G PROTEIN COUPLED RECEPTOR; HISTONE H2A; HISTONE H2AC; HISTONE H2AG; HISTONE H2AL; HISTONE H2AM; HISTONE H2AO; HISTONE H2AQ; LOSARTAN; PROTEIN AQ96QV6; UNCLASSIFIED DRUG; HISTONE;

ARTICLE; CELL STRAIN HEK293; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; DRUG TARGETING; FAST PROTEIN LIQUID CHROMATOGRAPHY; GENE ACTIVATION; GENE CONTROL; GENE IDENTIFICATION; HUMAN; HUMAN CELL; IMMUNOCHEMISTRY; MASS SPECTROMETRY; MOLECULAR DYNAMICS; PROTEIN DEPHOSPHORYLATION; PROTEIN ISOLATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; SEPARATION TECHNIQUE; STRUCTURE ANALYSIS; CHROMATIN; GENETICS; HETEROCHROMATIN; METABOLISM; METHYLATION; PHOSPHORYLATION;

CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; HEK293 CELLS; HETEROCHROMATIN; HISTONES; HUMANS; METHYLATION; PHOSPHORYLATION; RECEPTOR, ANGIOTENSIN, TYPE 1;

EID: 77958607874     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0012552     Document Type: Article

References (59)

1. Lee C, Hwang SA, Jang SH, Chung HS, Bhat MB, et al. (2007) Manifold active-state conformations in GPCRs: agonist-activated constitutively active mutant AT1 receptor preferentially couples to Gq compared to the wild-type AT1 receptor. FEBS Lett 581: 2517-2522.
2. Perez DM, Karnik SS (2005) Multiple signaling states of G-protein-coupled receptors. Pharmacol Rev 57: 147-161.
3. Karnik SS, Gogonea C, Patil S, Saad Y, Takezako T (2003) Activation of G-protein-coupled receptors: a common molecular mechanism. Trends Endocrinol Metab 14: 431-437.
4. Hanson MA, Stevens RC (2009) Discovery of new GPCR biology: one receptor structure at a time. Structure 17: 8-14.
5. Kang J, Shi Y, Xiang B, Qu B, Su W, et al. (2005) A nuclear function of beta-arrestin1 in GPCR signaling: regulation of histone acetylation and gene transcription. Cell 123: 833-847.
6. Oka SI, Ago T, Kitazono T, Zablocki D, Sadoshima J. (2009) The role of redox modulation of class II histone deacetylases in mediating pathological cardiac hypertrophy. J Mol Med.
7. Davis FJ, Pillai JB, Gupta M, Gupta MP (2005) Concurrent opposite effects of trichostatin A, an inhibitor of histone deacetylases, on expression of alpha-MHC and cardiac tubulins: implication for gain in cardiac muscle contractility. Am J Physiol Heart Circ Physiol 288: H1477-1490.
8. Balbi AP, Francescato HD, Marin EC, Costa RS, Coimbra TM (2009) Roles of mitogen-activated protein kinases and angiotensin II in renal development. Braz J Med Biol Res 42: 38-43.
9. Martini JS, Raake P, Vinge LE, DeGeorge BR, Jr., Chuprun JK, et al. (2008) Uncovering G protein-coupled receptor kinase-5 as a histone deacetylase kinase in the nucleus of cardiomyocytes. Proc Natl Acad Sci USA 105: 12457-12462.
10. Nakatani Y, Tagami H, Shestakova E (2006) How is epigenetic information on chromatin inherited after DNA replication? Ernst Schering Res Found Workshop. pp 89-96.
11. Griendling KK, Lassegue B, Alexander RW (1996) Angiotensin receptors and their therapeutic implications. Annu Rev Pharmacol Toxicol 36: 281-306.
12. Mehta PK, Griendling KK (2007) Angiotensin II cell signaling: physiological and pathological effects in the cardiovascular system. Am J Physiol Cell Physiol 292: C82-97.
13. Dzau VJ, Lopez-Ilasaca M (2005) Searching for transcriptional regulators of Ang II-induced vascular pathology. J Clin Invest 115: 2319-2322.
14. McKinsey TA, Olson EN (1999) Cardiac hypertrophy: sorting out the circuitry. Curr Opin Genet Dev 9: 267-274.
15. Sadoshima J, Izumo S (1997) The cellular and molecular response of cardiac myocytes to mechanical stress. Annu Rev Physiol 59: 551-571.
16. Chien KR (1999) Stress pathways and heart failure. Cell 98: 555-558.
17. MacLellan WR, Schneider MD (1998) Success in failure: modeling cardiac decompensation in transgenic mice. Circulation 97: 1433-1435.
18. Morishita R, Gibbons GH, Ellison KE, Lee W, Zhang L, et al. (1994) Evidence for direct local effect of angiotensin in vascular hypertrophy. In vivo gene transfer of angiotensin converting enzyme. J Clin Invest 94: 978-984.
19. Brasier AR, Jamaluddin M, Han Y, Patterson C, Runge MS (2000) Angiotensin II induces gene transcription through cell-type-dependent effects on the nuclear factor-kappaB (NF-kappaB) transcription factor. Mol Cell Biochem 212: 155-169.
20. Yoshida T, Hoofnagle MH, Owens GK (2004) Myocardin and Prx1 contribute to angiotensin II-induced expression of smooth muscle alpha-actin. Circ Res 94: 1075-1082.
21. Zhan Y, Brown C, Maynard E, Anshelevich A, Ni W, et al. (2005) Ets-1 is a critical regulator of Ang II-mediated vascular inflammation and remodeling. J Clin Invest 115: 2508-2516.
22. Yue H, Li W, Desnoyer R, Karnik SS. Role of nuclear unphosphorylated STAT3 in angiotensin II type 1 receptor-induced cardiac hypertrophy. Cardiovasc Res 85: 90-99.
23. Garcia BA, Barber CM, Hake SB, Ptak C, Turner FB, et al. (2005) Modifications of human histone H3 variants during mitosis. Biochemistry 44: 13202-13213.
24. Bonenfant D, Coulot M, Towbin H, Schindler P, van Oostrum J (2006) Characterization of histone H2A and H2B variants and their post-translational modifications by mass spectrometry. Mol Cell Proteomics 5: 541-552.
25. Chen IY, Lypowy J, Pain J, Sayed D, Grinberg S, et al. (2006) Histone H2A.z is essential for cardiac myocyte hypertrophy but opposed by silent information regulator 2alpha. J Biol Chem 281: 19369-19377.
26. Alvelo-Ceron D, Niu L, Collart DG (2000) Growth regulation of human variant histone genes and acetylation of the encoded proteins. Mol Biol Rep 27: 61-71.
27. Kamakaka RT, Biggins S (2005) Histone variants: deviants? Genes Dev 19: 295-310.
28. Redon C, Pilch D, Rogakou E, Sedelnikova O, Newrock K, et al. (2002) Histone H2A variants H2AX and H2AZ. Curr Opin Genet Dev 12: 162-169.
29. Bao Y, Konesky K, Park YJ, Rosu S, Dyer PN, et al. (2004) Nucleosomes containing the histone variant H2A.Bbd organize only 118 base pairs of DNA. EMBO J 23: 3314-3324.
30. Dion MF, Kaplan T, Kim M, Buratowski S, Friedman N, et al. (2007) Dynamics of replication-independent histone turnover in budding yeast. Science 315: 1405-1408.
31. Mito Y, Henikoff JG, Henikoff S (2007) Histone replacement marks the boundaries of cis-regulatory domains. Science 315: 1408-1411.
32. Heintzman ND, Hon GC, Hawkins RD, Kheradpour P, Stark A, et al. (2009) Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 459: 108-112.
33. Su X, Lucas DM, Zhang L, Xu H, Zabrouskov V, et al. (2009) Validation of an LC-MS based approach for profiling histones in chronic lymphocytic leukemia. Proteomics 9: 1197-1206.
34. Mariani MR, Carpaneto EM, Ulivi M, Allfrey VG, Boffa LC (2003) Correlation between butyrate-induced histone hyperacetylation turn-over and c-myc expression. J Steroid Biochem Mol Biol 86: 167-171.
35. Zhang Y, Griffin K, Mondal N, Parvin JD (2004) Phosphorylation of histone H2A inhibits transcription on chromatin templates. J Biol Chem 279: 21866-21872.
36. Barber CM, Turner FB, Wang Y, Hagstrom K, Taverna SD, et al. (2004) The enhancement of histone H4 and H2A serine 1 phosphorylation during mitosis and S-phase is evolutionarily conserved. Chromosoma 112: 360-371.
37. Beck HC, Nielsen EC, Matthiesen R, Jensen LH, Sehested M, et al. (2006) Quantitative proteomic analysis of post-translational modifications of human histones. Mol Cell Proteomics 5: 1314-1325.
38. Bonenfant D, Towbin H, Coulot M, Schindler P, Mueller DR, et al. (2007) Analysis of dynamic changes in post-translational modifications of human histones during cell cycle by mass spectrometry. Mol Cell Proteomics 6: 1917-1932.
39. Goll MG, Bestor TH (2002) Histone modification and replacement in chromatin activation. Genes Dev 16: 1739-1742.
40. Turner BM (2002) Cellular memory and the histone code. Cell 111: 285-291.
41. Zhang L, Eugeni EE, Parthun MR, Freitas MA (2003) Identification of novel histone post-translational modifications by peptide mass fingerprinting. Chro-mosoma 112: 77-86.
42. Espino PS, Drobic B, Dunn KL, Davie JR (2005) Histone modifications as a platform for cancer therapy. J Cell Biochem 94: 1088-1102.
43. Strahl BD, Allis CD (2000) The language of covalent histone modifications. Nature 403: 41-45.
44. Vaquero A, Loyola A, Reinberg D. (2003) The constantly changing face of chromatin. Sci Aging Knowledge Environ 2003: RE4.
45. Ausio J, Abbott DW, Wang X, Moore SC (2001) Histone variants and histone modifications: a structural perspective. Biochem Cell Biol 79: 693-708.
46. Henikoff S (2005) Histone modifications: combinatorial complexity or cumulative simplicity? Proc Natl Acad Sci USA 102: 5308-5309.
47. Fischle W, Wang Y, Jacobs SA, Kim Y, Allis CD, et al. (2003) Molecular basis for the discrimination of repressive methyl-lysine marks in histone H3 by Polycomb and HP1 chromodomains. Genes Dev 17: 1870-1881.
48. Hirota T, Lipp JJ, Toh BH, Peters JM (2005) Histone H3 serine 10 phosphorylation by Aurora B causes HP1 dissociation from heterochromatin. Nature 438: 1176-1180.
49. Loyola A, Bonaldi T, Roche D, Imhof A, Almouzni G (2006) PTMs on H3 variants before chromatin assembly potentiate their final epigenetic state. Mol Cell 24: 309-316.
50. Daujat S, Zeissler U, Waldmann T, Happel N, Schneider R (2005) HP1 binds specifically to Lys26-methylated histone H1.4, whereas simultaneous Ser27 phosphorylation blocks HP1 binding. J Biol Chem 280: 38090-38095.
51. Thiriet C, Hayes JJ (2005) Replication-independent core histone dynamics at transcriptionally active loci in vivo. Genes Dev 19: 677-682.
52. Bock C, Walter J, Paulsen M, Lengauer T (2007) CpG island mapping by epigenome prediction. PLoS Comput Biol 3: e110.
53. Lee JH, Gaetz J, Bugarija B, Fernandes CJ, Snyder GE, et al. (2009) Chromatin analysis of occluded genes. Hum Mol Genet.
54. Strange PG (2008) Signaling mechanisms of GPCR ligands. Curr Opin Drug Discov Devel 11: 196-202.
55. Ye S, Huber T, Vogel R, Sakmar TP (2009) FTIR analysis of GPCR activation using azido probes. Nat Chem Biol 5: 397-399.
56. Miura S, Karnik SS (2002) Constitutive activation of angiotensin II type 1 receptor alters the orientation of transmembrane Helix-2. J Biol Chem 277: 24299-24305.
57. White SM, Constantin PE, Claycomb WC (2004) Cardiac physiology at the cellular level: use of cultured HL-1 cardiomyocytes for studies of cardiac muscle cell structure and function. Am J Physiol Heart Circ Physiol 286: H823-829.
58. Majors AK, Sengupta S, Willard B, Kinter MT, Pyeritz RE, Jacobsen DW (2002) Homocysteine binds to human plasma fibronectin and inhibits its interaction with fibrin. Arterioscler Thromb Vasc Biol 22: 1354-1359.
59. Eskeland R, Czermin B, Boeke J, Bonaldi T, Regula JT, et al. (2004) The N-terminus of Drosophila SU(VAR)3-9 mediates dimerization and regulates its methyltransferase activity. Biochemistry 43: 3740-3749.