Hypoxia-induced epigenetic modifications are associated with cardiac tissue fibrosis and the development of a myofibroblast-like phenotype

Human Molecular Genetics

Volumn 23, Issue 8, 2014, Pages 2176-2188

  Watson, Chris J ^a,b   Collier, Patrick ^a   Tea, Isaac ^a   Neary, Roisin ^a   Watson, Jenny A ^a   Robinson, Claire ^a   Phelan, Dermot ^a   Ledwidge, Mark T ^b   Mcdonald, Kenneth M ^b   Mccann, Amanda ^a   Sharaf, Osama ^a   Baugh, John A ^a  

^a UNIVERSITY COLLEGE DUBLIN   (Ireland)

^b ST MICHAEL'S HOSPITAL   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; ALPHA SMOOTH MUSCLE ACTIN; ALPHA TUBULIN; COLLAGEN TYPE 1; DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 3A; DNA METHYLTRANSFERASE 3B; FIBRILLAR COLLAGEN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; SMALL INTERFERING RNA; TRANSFORMING GROWTH FACTOR BETA;

AGED; ARTICLE; CELL MATURATION; CONTROLLED STUDY; CYTOKINE RESPONSE; DNA METHYLATION; ENZYME REPRESSION; EPIGENETICS; FEMALE; FIBROBLAST; GENETIC ASSOCIATION; HEART MUSCLE CELL; HEART MUSCLE FIBROSIS; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPOXIA; MAJOR CLINICAL STUDY; MALE; MYOFIBROBLAST; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

AGED; ANOXIA; BLOTTING, WESTERN; CELLS, CULTURED; COLLAGEN; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; EPIGENOMICS; FEMALE; FIBROSIS; FLOW CYTOMETRY; HEART; HUMANS; IMMUNOENZYME TECHNIQUES; MALE; MYOFIBROBLASTS; PHENOTYPE; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, SMALL INTERFERING; TRANSFORMING GROWTH FACTOR BETA;

EID: 84897879302     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt614     Document Type: Article

References (29)

1. Kong, P., Christia, P. and Frangogiannis, N.G. (2013) The pathogenesis of cardiac fibrosis. Cell. Mol. Life Sci., http://dx.doi.org/10.1007/s00018-013-1349-6.
2. Swynghedauw, B. (1999) Molecular mechanisms of myocardial remodeling. Physiol. Rev., 79, 215-262.
3. van den Borne, S.W., Diez, J., Blankesteijn, W.M., Verjans, J., Hofstra, L. and Narula, J. (2010) Myocardial remodeling after infarction: the role of myofibroblasts. Nat. Rev. Cardiol., 7, 30-37.
4. Barallobre-Barreiro, J., Didangelos, A., Schoendube, F.A., Drozdov, I., Yin, X., Fernandez-Caggiano, M., Willeit, P., Puntmann, V.O., Aldama-Lopez, G., Shah, A.M. et al. (2012) Proteomics analysis of cardiac extracellular matrix remodeling in a porcine model of ischemia/reperfusion injury. Circulation, 125, 789-802.
5. Opie, L.H., Commerford, P.J., Gersh, B.J. and Pfeffer, M.A. (2006) Controversies in ventricular remodelling. Lancet, 367, 356-367.
6. Gabrielsen, A., Lawler, P.R., Yongzhong, W., Steinbruchel, D., Blagoja, D., Paulsson-Berne, G., Kastrup, J. and Hansson, G.K. (2007) Gene expression signals involved in ischemic injury, extracellular matrix composition and fibrosis defined by global mRNA profiling of the human left ventricular myocardium. J. Mol. Cell. Cardiol., 42, 870-883.
7. Egger, G., Liang, G., Aparicio, A. and Jones, P.A. (2004) Epigenetics in human disease and prospects for epigenetic therapy. Nature, 429, 457-463.
8. Sharma, S., Kelly, T.K. and Jones, P.A. (2010) Epigenetics in cancer. Carcinogenesis, 31, 27-36.
9. Robinson, C.M., Watson, C.J. and Baugh, J.A. (2012) Epigenetics within the matrix: a neo-regulator of fibrotic disease. Epigenetics, 7, 987-993.
10. Papait, R., Greco, C., Kunderfranco, P., Latronico, M.V. and Condorelli, G. (2013) Epigenetics: a new mechanism of regulation of heart failure? Basic Res. Cardiol., 108, 361.
11. Holotnakova, T., Ziegelhoffer, A., Ohradanova, A., Hulikova, A., Novakova, M., Kopacek, J., Pastorek, J. and Pastorekova, S. (2008) Induction of carbonic anhydrase IX by hypoxia and chemical disruption of oxygen sensing in rat fibroblasts and cardiomyocytes. Pflugers Arch., 456, 323-337.
12. Ivan, M., Kondo, K., Yang, H., Kim, W., Valiando, J., Ohh, M., Salic, A., Asara, J.M., Lane, W.S. and Kaelin, W.G. Jr. (2001) HIF alpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science, 292, 464-468.
13. Jaakkola, P., Mole, D.R., Tian, Y.M., Wilson, M.I., Gielbert, J., Gaskell, S.J., Kriegsheim, A., Hebestreit, H.F., Mukherji, M., Schofield, C.J. et al. (2001) Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science, 292, 468-472.
14. Lorenzen, J.M., Martino, F. and Thum, T. (2012) Epigenetic modifications in cardiovascular disease. Basic Res. Cardiol., 107, 245.
15. Ordovas, J.M. and Smith, C.E. (2010) Epigenetics and cardiovascular disease. Nat. Rev. Cardiol., 7, 510-519.
16. Han, P., Hang, C.T., Yang, J. and Chang, C.P. (2011) Chromatin remodeling in cardiovascular development and physiology. Circ. Res., 108, 378-396.
17. Watson, J.A., Watson, C.J., McCrohan, A.M., Woodfine, K., Tosetto, M., McDaid, J., Gallagher, E., Betts, D., Baugh, J., O'Sullivan, J. et al. (2009) Generation of an epigenetic signature by chronic hypoxia in prostate cells. Hum. Mol. Genet., 18, 3594-3604.
18. Watson, J.A., Watson, C.J., McCann, A. and Baugh, J. (2010) Epigenetics, the epicenter of the hypoxic response. Epigenetics, 5, 293-296.
19. Roll, J.D., Rivenbark, A.G., Jones, W.D. and Coleman, W.B. (2008) DNMT3b overexpression contributes to a hypermethylator phenotype in human breast cancer cell lines. Mol. Cancer, 7, 15.
20. Robertson, K.D., Uzvolgyi, E., Liang, G., Talmadge, C., Sumegi, J., Gonzales, F.A. and Jones, P.A. (1999) The human DNA methyltransferases (DNMTs) 1, 3a and 3b: coordinate mRNA expression in normal tissues and overexpression in tumors. Nucleic Acids Res., 27, 2291-2298.
21. Pan, X., Chen, Z., Huang, R., Yao, Y. and Ma, G. (2013) Transforming growth factor beta1 induces the expression of collagen type I by DNA methylation in cardiac fibroblasts. PloS one, 8, e60335.
22. Wang, Y., Fan, P.S. and Kahaleh, B. (2006) Association between enhanced type I collagen expression and epigenetic repression of the FLI1 gene in scleroderma fibroblasts. Arthritis Rheum., 54, 2271-2279.
23. Patterson, A.J., Chen, M., Xue, Q., Xiao, D. and Zhang, L. (2010) Chronic prenatal hypoxia induces epigenetic programming of PKC{epsilon} gene repression in rat hearts. Circ. Res., 107, 365-373.
24. Meyer, K., Zhang, H. and Zhang, L. (2009) Direct effect of cocaine on epigenetic regulation of PKC1 gene repression in the fetal rat heart. J. Mol. Cell. Cardiol., 47, 504-511.
25. Klein, G., Schaefer, A., Hilfiker-Kleiner, D., Oppermann, D., Shukla, P., Quint, A., Podewski, E., Hilfiker, A., Schroder, F., Leitges, M. et al. (2005) Increased collagen deposition and diastolic dysfunction but preserved myocardial hypertrophy after pressure overload in mice lacking PKCepsilon. Circ. Res., 96, 748-755.
26. Watson, C.J., O'Kane, H., Maxwell, P., Sharaf, O., Petak, I., Hyland, P.L., O'Rouke, D., McKnight, J., Canning, P. and Williamson, K. (2012) Identification of a methylation hotspot in the death receptor Fas/CD95 in bladder cancer. Int. J. Oncol., 40, 645-654.
27. Robinson, C.M., Neary, R., Levendale, A., Watson, C.J. and Baugh, J.A. (2012) Hypoxia-induced DNA hypermethylation in human pulmonary fibroblasts is associated with Thy-1 promoter methylation and the development of a pro-fibrotic phenotype. Respir. Res., 13, 74.
28. Mei, C., Sun, L., Liu, Y., Yang, Y., Cai, X., Liu, M., Yao, W., Wang, C., Li, X., Wang, L. et al. (2010) Transcriptional and post-transcriptional control of DNA methyltransferase 3B is regulated by phosphatidylinositol 3 kinase/Aktpathway inhumanhepatocellular carcinoma cell lines. J. Cell. Biochem., 111, 158-167.
29. Novakovic, B., Wong, N.C., Sibson, M., Ng, H.K., Morley, R., Manuelpillai, U., Down, T., Rakyan, V.K., Beck, S., Hiendleder, S. et al. (2010) DNA methylation-mediated down-regulation of DNA methyltransferase-1 (DNMT1) is coincident with, but not essential for, global hypomethylation in human placenta. J. Biol. Chem., 285, 9583-9593.