CAMP induces hypertrophy and alters DNA methylation in HL-1 cardiomyocytes

American Journal of Physiology - Cell Physiology

Volumn 309, Issue 6, 2015, Pages C425-C436

  Fang, Xiefan ^a   Robinson, Jourdon ^a   Wang Hu, John ^a   Jiang, Lingli ^a   Freeman, Daniel A ^a   Rivkees, Scott A ^a   Wendler, Christopher C ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

5 cyclic monophosphate; Adenosine 3 ; Cardiomyocyte hypertrophy; Deoxyribonucleic acid methylation

Indexed keywords

ATRIAL NATRIURETIC FACTOR; AZACITIDINE; BRAIN NATRIURETIC PEPTIDE; BUCLADESINE; CAFFEINE; CYCLIC AMP; DIOXYGENASE; DNA; DNA METHYLTRANSFERASE; GENOMIC DNA; MICRORNA; MICRORNA 208A; MICRORNA 208B; MYOCYTE ENHANCER FACTOR 2; MYOCYTE ENHANCER FACTOR 2C; MYOCYTE ENHANCER FACTOR 2D; MYOSIN HEAVY CHAIN; MYOSIN HEAVY CHAIN 6; MYOSIN HEAVY CHAIN 7; MYOSIN HEAVY CHAIN 7B; SMALL UNTRANSLATED RNA; TET METHYLCYTOSINE DIOXYGENASE; THEOPHYLLINE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GATA 4; TRANSCRIPTION FACTOR NFATC1; TROPONIN I; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL LINE; CELL SIZE; CONTROLLED STUDY; DNA METHYLATION; ENZYME ACTIVITY; ENZYME INHIBITION; GENE EXPRESSION; GENE FUNCTION; HEART ATRIUM; HEART MUSCLE CELL; HYPERTROPHIC CARDIOMYOPATHY; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; RECEPTOR UPREGULATION; ANIMAL; CARDIAC MUSCLE CELL; CARDIOMEGALY; CARDIOMYOPATHY; GENETICS; HEART; METABOLISM; MOUSE; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; UPREGULATION;

ANIMALS; CARDIOMEGALY; CARDIOMYOPATHIES; CELL LINE; CYCLIC AMP; DNA METHYLATION; GENE EXPRESSION; HEART; MICE; MICRORNAS; MYOCYTES, CARDIAC; UP-REGULATION;

EID: 84941603020     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00058.2015     Document Type: Article

References (57)

1. Babuin L, Jaffe AS. Troponin: the biomarker of choice for the detection of cardiac injury. Can Med Assoc J 173: 1191-1202, 2005.
2. Bender AT, Beavo JA. Cyclic nucleotide phosphodiesterases: molecular regulation to clinical use. Pharmacol Rev 58: 488-520, 2006.
3. Boswell-Smith V, Spina D, Page CP. Phosphodiesterase inhibitors. Br J Pharmacol 147, Suppl 1: S252-S257, 2006.
4. Buscariollo DL, Fang X, Greenwood V, Xue H, Rivkees SA, Wendler CC. Embryonic caffeine exposure acts via A1 adenosine receptors to alter adult cardiac function and DNA methylation in mice. PloS one 9: e87547, 2014.
5. Chang CP, Bruneau BG. Epigenetics and cardiovascular development. Ann Rev Physiol 74: 41-68, 2012.
6. Chien KR. Myocyte survival pathways and cardiomyopathy: implications for trastuzumab cardiotoxicity. Semin Oncol 27: 9-100, 2000.
7. Claycomb WC, Lanson NA Jr, Stallworth BS, Egeland DB, Delcarpio JB, Bahinski A, and Izzo NJ Jr. HL-1 cells: a cardiac muscle cell line that contracts and retains phenotypic characteristics of the adult cardiomyocyte. Proc Natl Acad Sci USA 95: 2979-2984, 1998.
8. Clifford CP, Nunez DJ. Human beta-myosin heavy chain mRNA prevalence is inversely related to the degree of methylation of regulatory elements. Cardiovasc Res 38: 736-743, 1998.
9. Corrales J, Fang X, Thornton C, Mei W, Barbazuk WB, Duke M, Scheffler BE, Willett KL. Effects on specific promoter DNA methylation in zebrafish embryos and larvae following benzo[a]pyrene exposure. Comp Biochem Physiol Toxicol Pharmacol 163: 37-46, 2014.
10. Corsten MF, Dennert R, Jochems S, Kuznetsova T, Devaux Y, Hofstra L, Wagner DR, Staessen JA, Heymans S, Schroen B. Circulating MicroRNA-208b and MicroRNA-499 reflect myocardial damage in cardiovascular disease. Circ Cardiovasc Genetics 3: 499-506, 2010.
11. Dai YS, Cserjesi P, Markham BE, Molkentin JD. The transcription factors GATA4 and dHAND physically interact to synergistically activate cardiac gene expression through a p300-dependent mechanism. J Biol Chem 277: 24390-24398, 2002.
12. Daniel PB, Walker WH, Habener JF. Cyclic AMP signaling and gene regulation. Ann Rev Nutr 18: 353-383, 1998.
13. Denis H, Ndlovu MN, Fuks F. Regulation of mammalian DNA methyltransferases: a route to new mechanisms. EMBO Rep 12: 647-656, 2011.
14. Dirkx E, da Costa Martins PA, De Windt LJ. Regulation of fetal gene expression in heart failure. Biochim Biophys Acta 1832: 2414-2424, 2013.
15. Eindhoven JA, van den Bosch AE, Boersma E, Roos-Hesselink JW. The usefulness of brain natriuretic peptide in simple congenital heart disease-a systematic review. Cardiol Young 23: 315-324, 2013.
16. Fang X, Corrales J, Thornton C, Scheffler BE, Willett KL. Global and gene specific DNA methylation changes during zebrafish development. Comp Biochem Physiol B Biochem Mol Biol 166: 99-108, 2013.
17. Fang X, Dong W, Thornton C, Scheffler B, Willett KL. Benzo(a)pyrene induced glycine N-methyltransferase messenger RNA expression in Fundulus heteroclitus embryos. Marine Environ Res Suppl 69: S74-S76, 2010.
18. Fang X, Mei W, Barbazuk WB, Rivkees SA, Wendler CC. Caffeine exposure alters cardiac gene expression in embryonic cardiomyocytes. Am J Physiol Regul Integr Comp Physiol 307: R1471-R1487, 2014.
19. Fang X, Thornton C, Scheffler BE, Willett KL. Benzo[a]pyrene decreases global and gene specific DNA methylation during zebrafish development. Environ Toxicol Pharmacol 36: 40-50, 2013.
20. Faulk C, Dolinoy DC. Timing is everything: the when and how of environmentally induced changes in the epigenome of animals. Epigenetics 6: 791-797, 2011.
21. Flores K, Wolschin F, Corneveaux JJ, Allen AN, Huentelman MJ, Amdam GV. Genome-wide association between DNA methylation and alternative splicing in an invertebrate (Abstract). BMC Genomics 13: 480, 2012.
22. Frey N, Katus HA, Olson EN, Hill JA. Hypertrophy of the heart: a new therapeutic target? Circulation 109: 1580-1589, 2004.
23. Gidlof O, Smith JG, Miyazu K, Gilje P, Spencer A, Blomquist S, Erlinge D. Circulating cardio-enriched microRNAs are associated with long-term prognosis following myocardial infarction (Abstract). BMC Cardiovasc Dis 13: 12, 2013.
24. Haas J, Frese KS, Park YJ, Keller A, Vogel B, Lindroth AM, Weichenhan D, Franke J, Fischer S, Bauer A, Marquart S, Sedaghat-Hamedani F, Kayvanpour E, Kohler D, Wolf NM, Hassel S, Nietsch R, Wieland T, Ehlermann P, Schultz JH, Dosch A, Mereles D, Hardt S, Backs J, Hoheisel JD, Plass C, Katus HA, Meder B. Alterations in cardiac DNA methylation in human dilated cardiomyopathy. EMBO Mol Med 5: 413-429, 2013.
25. He YW, Wang HS, Zeng J, Fang X, Chen HY, Du J, Yang XY. Sodium butyrate inhibits interferon-gamma induced indoleamine 2,3-dioxygenase expression via STAT1 in nasopharyngeal carcinoma cells. Life Sci 93: 509-515, 2013.
26. Hershberger RE, Hedges DJ, Morales A. Dilated cardiomyopathy: the complexity of a diverse genetic architecture. Nat Rev Cardiol 10: 531-547, 2013.
27. Inoue A, Zhang Y. Replication-dependent loss of 5-hydroxymethylcytosine in mouse preimplantation embryos (Abstract). Science 334: 194, 2011.
28. Kass SU, Pruss D, Wolffe AP. How does DNA methylation repress transcription? Trends Genet 13: 444-449, 1997.
29. Koczor CA, Lee EK, Torres RA, Boyd A, Vega JD, Uppal K, Yuan F, Fields EJ, Samarel AM, Lewis W. Detection of differentially methylated gene promoters in failing and nonfailing human left ventricle myocardium using computation analysis. Physiol Genomics 45: 597-605, 2013.
30. Kohli RM, Zhang Y. TET enzymes, TDG and the dynamics of DNA demethylation. Nature 502: 472-479, 2013.
31. Landstrom AP, Kellen CA, Dixit SS, van Oort RJ, Garbino A, Weisleder N, Ma J, Wehrens XH, Ackerman MJ. Junctophilin-2 expression silencing causes cardiocyte hypertrophy and abnormal intracellular calcium-handling. Circ Heart Fail 4: 214-223, 2011.
32. Lee Y, Nadal-Ginard B, Mahdavi V, Izumo S. Myocyte-specific enhancer factor 2 and thyroid hormone receptor associate and synergistically activate the alpha-cardiac myosin heavy-chain gene. Mol Cell Biol 17: 2745-2755, 1997.
33. Lohse MJ, Engelhardt S, Eschenhagen T. What is the role of betaadrenergic signaling in heart failure? Circ Res 93: 896-906, 2003.
34. Lompre AM, Nadal-Ginard B, Mahdavi V. Expression of the cardiac ventricular alpha-and beta-myosin heavy chain genes is developmentally and hormonally regulated. J Biol Chem 259: 6437-6446, 1984.
35. Meissner JD, Umeda PK, Chang KC, Gros G, Scheibe RJ. Activation of the beta myosin heavy chain promoter by MEF-2D, MyoD, p300, and the calcineurin/NFATc1 pathway. J Cell Physiol 211: 138-148, 2007.
36. Movassagh M, Choy MK, Goddard M, Bennett MR, Down TA, Foo RS. Differential DNA methylation correlates with differential expression of angiogenic factors in human heart failure. PLoS One 5: e8564, 2010.
37. Movassagh M, Choy MK, Knowles DA, Cordeddu L, Haider S, Down T, Siggens L, Vujic A, Simeoni I, Penkett C, Goddard M, Lio P, Bennett MR, Foo RS. Distinct epigenomic features in end-stage failing human hearts. Circulation 124: 2411-2422, 2011.
38. Movsesian MA, Bristow MR. Alterations in cAMP-mediated signaling and their role in the pathophysiology of dilated cardiomyopathy. Curr Topics Dev Biol 68: 25-48, 2005.
39. Newby LK, Jesse RL, Babb JD, Christenson RH, De Fer TM, Diamond GA, Fesmire FM, Geraci SA, Gersh BJ, Larsen GC, Kaul S, McKay CR, Philippides GJ, Weintraub WS. ACCF 2012 expert consensus document on practical clinical considerations in the interpretation of troponin elevations: a report of the American College of Cardiology Foundation task force on Clinical Expert Consensus Documents. J Am Coll Cardiol 60: 2427-2463, 2012.
40. Oliveira-Carvalho V, Carvalho VO, Bocchi EA. The emerging role of miR-208a in the heart. DNA Cell Biol 32: 8-12, 2013.
41. Osadchii OE. Cardiac hypertrophy induced by sustained beta-adrenoreceptor activation: pathophysiological aspects. Heart Fail Rev 12: 66-86, 2007.
42. Petersen CA, Krumholz KA, Burleigh BA. Toll-like receptor 2 regulates interleukin-1beta-dependent cardiomyocyte hypertrophy triggered by Trypanosoma cruzi. Infect Immun 73: 6974-6980, 2005.
43. Seternes OM, Sorensen R, Johansen B, Moens U. Activation of protein kinase A by dibutyryl cAMP treatment of NIH 3T3 cells inhibits proliferation but fails to induce Ser-133 phosphorylation and transcriptional activation of CREB. Cell Signal 11: 211-219, 1999.
44. Sharma P, Garg G, Kumar A, Mohammad F, Kumar SR, Tanwar VS, Sati S, Sharma A, Karthikeyan G, Brahmachari V, Sengupta S. Genome wide DNA methylation profiling for epigenetic alteration in coronary artery disease patients. Gene 541: 31-40, 2014.
45. Sharma P, Kumar J, Garg G, Kumar A, Patowary A, Karthikeyan G, Ramakrishnan L, Brahmachari V, Sengupta S. Detection of altered global DNA methylation in coronary artery disease patients. DNA Cell Biol 27: 357-365, 2008.
46. Shaywitz AJ, Greenberg ME. CREB: a stimulus-induced transcription factor activated by a diverse array of extracellular signals. Ann Rev Biochem 68: 821-861, 1999.
47. Shirodkar AV, Marsden PA. Epigenetics in cardiovascular disease. Curr Opin Cardiol 26: 209-215, 2011.
48. Shukla S, Kavak E, Gregory M, Imashimizu M, Shutinoski B, Kashlev M, Oberdoerffer P, Sandberg R, Oberdoerffer S. CTCF-promoted RNA polymerase II pausing links DNA methylation to splicing. Nature 479: 74-79, 2011.
49. Sim CB, Ziemann M, Kaspi A, Harikrishnan KN, Ooi J, Khurana I, Chang L, Hudson JE, El-Osta A, Porrello ER. Dynamic changes in the cardiac methylome during postnatal development. FASEB J 29: 1329-1343, 2015.
50. Szyf M. Epigenetics, DNA methylation, and chromatin modifying drugs. Ann Rev Pharmacol Toxicol 49: 243-263, 2009.
51. van Rooij E, Quiat D, Johnson BA, Sutherland LB, Qi X, Richardson JA, Kelm RJ Jr, Olson EN. A family of microRNAs encoded by myosin genes governs myosin expression and muscle performance. Dev Cell 17: 662-673, 2009.
52. Xu H, Baldini A. Genetic pathways to mammalian heart development: recent progress from manipulation of the mouse genome. Semin Cell Dev Biol 18: 77-83, 2007.
53. Yang X, Han H, De Carvalho DD, Lay FD, Jones PA, Liang G. Gene body methylation can alter gene expression and is a therapeutic target in cancer. Cancer Cell 26: 577-590, 2014.
54. Ying AK, Hassanain HH, Roos CM, Smiraglia DJ, Issa JJ, Michler RE, Caligiuri M, Plass C, Goldschmidt-Clermont PJ. Methylation of the estrogen receptor-alpha gene promoter is selectively increased in proliferating human aortic smooth muscle cells. Cardiovasc Res 46: 172-179, 2000.
55. Zhang X, Odom DT, Koo SH, Conkright MD, Canettieri G, Best J, Chen H, Jenner R, Herbolsheimer E, Jacobsen E, Kadam S, Ecker JR, Emerson B, Hogenesch JB, Unterman T, Young RA, Montminy M. Genome-wide analysis of cAMP-response element binding protein occupancy, phosphorylation, and target gene activation in human tissues. Proc Natl Acad Sci USA 102: 4459-4464, 2005.
56. Zhao L, Kang I, Fang X, Wang W, Lee MA, Hollins RR, Marshall MR, Chung S. Gamma-tocotrienol attenuates high-fat diet-induced obesity and insulin resistance by inhibiting adipose inflammation and M1 macrophage recruitment. Int J Obes (Lond) 39: 438-446, 2015.
57. Zhou Y, Lu Y, Tian W. Epigenetic features are significantly associated with alternative splicing (Abstract). BMC Genomics 13: 123, 2012.