Epigenetics, cardiovascular disease, and cellular reprogramming

Journal of Molecular and Cellular Cardiology

Volumn 128, Issue , 2019, Pages 129-133

  Al Hasani, Keith ^a   Mathiyalagan, Prabhu ^b   El Osta, Assam ^a,c  

^a MONASH UNIVERSITY   (Australia)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^c CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

[No Author keywords available]

Indexed keywords

METHYL CPG BINDING PROTEIN 2; MICRORNA; POLYCOMB REPRESSIVE COMPLEX 2; TRANSCRIPTION FACTOR EZH2; UNTRANSLATED RNA;

ATHEROSCLEROSIS; CARDIOVASCULAR DISEASE; DNA METHYLATION; EPIGENETICS; HEART DEVELOPMENT; HEART FAILURE; HEART FIBROBLAST; HEART INFARCTION; HEART MUSCLE FIBROSIS; HEART MUSCLE ISCHEMIA; HEART VENTRICLE HYPERTROPHY; HISTONE CODE; HISTONE MODIFICATION; HUMAN; NONHUMAN; NUCLEAR REPROGRAMMING; PRIORITY JOURNAL; REVIEW; TISSUE REGENERATION; TRANSCRIPTION REGULATION; CARDIAC MUSCLE; CHROMATIN; GENETICS; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION;

CARDIOVASCULAR DISEASES; CELLULAR REPROGRAMMING; CHROMATIN; DNA METHYLATION; EPIGENOMICS; HISTONE CODE; HUMANS; MYOCARDIUM; RNA, UNTRANSLATED; SIGNAL TRANSDUCTION;

EID: 85061012039     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2019.01.019     Document Type: Review

References (77)

1. Jones, P.A., Baylin, S.B., The epigenomics of cancer. Cell 128 (2007), 683–692.
2. Wamstad, J.A., Alexander, J.M., Truty, R.M., Shrikumar, A., Li, F., Eilertson, K.E., et al. Dynamic and coordinated epigenetic regulation of developmental transitions in the cardiac lineage. Cell 151 (2012), 206–220.
3. Strahl, B.D., Allis, C.D., The language of covalent histone modifications. Nature 403 (2000), 41–45.
4. Paige, S.L., Thomas, S., Stoick-Cooper, C.L., Wang, H., Maves, L., Sandstrom, R., et al. A temporal chromatin signature in human embryonic stem cells identifies regulators of cardiac development. Cell 151 (2012), 221–232.
5. Mathiyalagan, P., Okabe, J., Chang, L., Su, Y., Du, X.J., El-Osta, A., The primary microRNA-208b interacts with Polycomb-group protein, Ezh2, to regulate gene expression in the heart. Nucleic Acids Res. 42 (2014), 790–803.
6. Rinn, J.L., Chang, H.Y., Genome regulation by long noncoding RNAs. Annu. Rev. Biochem. 81 (2012), 145–166.
7. Movassagh, M., Choy, M.K., Knowles, D.A., Cordeddu, L., Haider, S., Down, T., et al. Distinct epigenomic features in end-stage failing human hearts. Circulation 124 (2011), 2411–2422.
8. Delgado-Olguín, P., Huang, Y., Li, X., Christodoulou, D., Seidman, C.E., Seidman, J.G., et al. Epigenetic repression of cardiac progenitor gene expression by Ezh2 is required for postnatal cardiac homeostasis. Nat. Genet. 44 (2012), 343–347.
9. Anderson, D.J., Kaplan, D.I., Bell, K.M., Koutsis, K., Haynes, J.M., Mills, R.J., et al. NKX2-5 regulates human cardiomyogenesis via a HEY2 dependent transcriptional network. Nat. Commun., 9, 2018, 1373.
10. Porrello, E.R., Mahmoud, A.I., Simpson, E., Hill, J.A., Richardson, J.A., Olson, E.N., et al. Transient regenerative potential of the neonatal mouse heart. Science 331 (2011), 1078–1080.
11. Quaife-Ryan, G.A., Sim, C.B., Ziemann, M., Kaspi, A., Rafehi, H., Ramialison, M., et al. Multicellular transcriptional analysis of mammalian heart regeneration. Circulation 136 (2017), 1123–1139.
12. Sim, C.B., Ziemann, M., Kaspi, A., Harikrishnan, K.N., Ooi, J., Khurana, I., et al. Dynamic changes in the cardiac methylome during postnatal development. FASEB J. 29 (2015), 1329–1343.
13. Mayer, S.C., Gilsbach, R., Preissl, S., Monroy Ordonez, E.B., Schnick, T., Beetz, N., et al. Adrenergic repression of the epigenetic reader MeCP2 facilitates cardiac adaptation in chronic heart failure. Circ. Res. 117 (2015), 622–633.
14. Khan, A.W., Ziemann, M., Corcoran, S.J., K N H, Okabe, J., Rafehi, H., Maxwell, S.S., et al. NET silencing by let-7i in postural tachycardia syndrome. JCI Insight., 2, 2017 (e90183).
15. Zimmet, P., Shi, Z., El-Osta, A., Ji, L., Epidemic T2DM, early development and epigenetics: implications of the Chinese Famine. Nat Rev Endocrinol. 14:12 (2018 Oct 11), 738–746.
16. Oh, H.J., Kato, M., Deshpande, S., Zhang, E., Das, S., Lanting, L., Wang, M., Natarajan, R., Inhibition of the processing of miR-25 by HIPK2-Phosphorylated-MeCP2 induces NOX4 in early diabetic nephropathy. Sci. Rep., 6, 2016, 38789.
17. El-Osta, A., Contemporary trends emerging in epigenomics and metabolism. Antioxid. Redox Signal. 29 (2018), 1019–1022.
18. Rosenthal, N., Costa, M.A., Unravelling the endovascular microenvironment by optical coherence tomography. Eur. Heart J. 30 (2010), 139–142.
19. Burridge, P.W., Sharma, A., Wu, J.C., Genetic and epigenetic regulation of human cardiac reprogramming and differentiation in regenerative medicine. Annu. Rev. Genet. 49 (2015), 461–484.
20. Mathiyalagan, P., Chang, L., Du, X.J., El-Osta, A., Cardiac ventricular chambers are epigenetically distinguishable. Cell Cycle 9 (2010), 612–617.
21. Gilsbach, R., Schwaderer, M., Preissl, S., Grüning, B.A., Kranzhöfer, D., Schneider, P., Distinct epigenetic programs regulate cardiac myocyte development and disease in the human heart in vivo. Nat. Commun., 9, 2018, 39.
22. Takahashi, K., Yamanaka, S., Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126 (2006), 663–676.
23. Djuric, U., Ellis, J., Epigenetics of induced pluripotency, the seven-headed dragon. Stem Cell Res Ther, 1, 2010, 3.
24. Al-Hasani, K., Pfeifer, A., Courtney, M., Ben-Othman, N., Gjernes, E., Vieira, A., et al. Adult duct-lining cells can reprogram into β-like cells able to counter repeated cycles of toxin-induced diabetes. Dev. Cell 26 (2013), 86–100.
25. Ben-Othman, N., Vieira, A., Courtney, M., Record, F., Gjernes, E., Avolio, F., et al. Long-term GABA administration induces alpha cell-mediated beta-like cell neogenesis. Cell 168 (2017), 73–85.
26. Cho, Y., Kim, B., Bae, H., Kim, W., Baek, J., Woo, K., et al. Direct gingival fibroblasts/osteoblast transdifferentiation via epigenetics. J. Dent. Res. 96 (2017), 555–561.
27. Cho, Y.D., Bae, H.S., Lee, D.S., Yoon, W.J., Woo, K.M., Baek, J.H., et al. Epigenetic priming confers direct cell trans-differentiation from adipocyte to osteoblast in a transgene-free state. J. Cell. Physiol. 231 (2016), 1484–1494.
28. Thal, M.A., Krishnamurthy, P., Mackie, A.R., Hoxha, E., Lambers, E., Verma, S., et al. Enhanced angiogenic and cardiomyocyte differentiation capacity of epigenetically reprogrammed mouse and human endothelial progenitor cells augments their efficacy for ischemic myocardial repair. Circ. Res. 111 (2012), 180–190.
29. Ieda, M., Fu, J.D., Delgado-Olguin, P., Vedantham, V., Hayashi, Y., Bruneau, B.G., et al. Direct reprogramming of fibroblasts into functional cardiomyocytes by defined factors. Cell 142 (2010), 375–386.
30. Garg, V., Kathiriya, I.S., Barnes, R., Schluterman, M.K., King, I.N., Butler, C.A., et al. GATA4 mutations cause human congenital heart defects and reveal an interaction with TBX5. Nature 424 (2003), 443–447.
31. Lin, Q., Schwarz, J., Bucana, C., Olson, E.N., Control of mouse cardiac morphogenesis and myogenesis by transcription factor MEF2C. Science 276 (1997), 1404–1407.
32. Jayawardena, T.M., Egemnazarov, B., Finch, E.A., Zhang, L., Payne, J.A., Pandya, K., et al. MicroRNA-mediated in vitro and in vivo direct reprogramming of cardiac fibroblasts to cardiomyocytes. Circ. Res. 110 (2012), 1465–1473.
33. Muraoka, N., Yamakawa, H., Miyamoto, K., Sadahiro, T., Umei, T., Isomi, M., et al. MiR-133 promotes cardiac reprogramming by directly repressing Snai1 and silencing fibroblast signatures. EMBO J. 33 (2014), 1565–1581.
34. Fu, J.D., Stone, N.R., Liu, L., Spencer, C.I., Qian, L., Hayashi, Y., et al. Direct reprogramming of human fibroblasts toward a cardiomyocyte-like state. Stem Cell Rep 1 (2013), 235–247.
35. Liu, Z., Chen, O., Zheng, M., Wang, L., Zhou, Y., Yin, C., et al. Re-patterning of H3K27me3, H3K4me3 and DNA methylation during fibroblast conversion into induced cardiomyocytes. Stem Cell Res. 16 (2016), 507–518.
36. Eulalio, A., Mano, M., Dal Ferro, M., Zentilin, L., Sinagra, G., Zacchigna, S., et al. Functional screening identifies miRNAs inducing cardiac regeneration. Nature 492 (2012), 376–381.
37. Porrello, E.R., Mahmoud, A.I., Simpson, E., Johnson, B.A., Grinsfelder, D., Canseco, D., et al. Regulation of neonatal and adult mammalian heart regeneration by the miR-15 family. Proc. Natl. Acad. Sci. U. S. A. 110 (2013), 187–192.
38. Yang, F., Chen, Q., He, S., Yang, M., Maguire, E.M., An, W., et al. miR-22 is a novel mediator of vascular smooth muscle cell phenotypic modulation and neointima formation. Circulation 137 (2018), 1824–1841.
39. Lim, S.Y., Sivakumaran, P., Crombie, D.E., Dusting, G.J., Pébay, A., Dilley, R.J., Trichostatin A enhances differentiation of human induced pluripotent stem cells to cardiogenic cells for cardiac tissue engineering. Stem Cells Transl. Med. 2 (2013), 715–725.
40. Chang, L., Kiriazis, H., Gao, X.M., Du, X.J., El-Osta, A., Cardiac genes show contextual SWI/SNF interactions with distinguishable gene activities. Epigenetics. 6 (2011), 760–768.
41. 1 , Tuano NK, Rafehi H, Gao XM, Ziemann M, Du XJ et al. HDAC inhibition attenuates cardiac hypertrophy by acetylation and deacetylation of target genes. Epigenetics 2015;10:418–30.
42. Rafehi, H., Balcerczyk, A., Lunke, S., Kaspi, A., Ziemann, M., Kn, H., et al. Vascular histone deacetylation by pharmacological HDAC inhibition. Genome Res. 24 (2014), 1271–1284.
43. He, L., Hannon, G.J., MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet. 5 (2004), 522–531.
44. Chen, J.F., Murchison, E.P., Tang, R., Callis, T.E., Tatsuguchi, M., Deng, Z., et al. Targeted deletion of Dicer in the heart leads to dilated cardiomyopathy and heart failure. Proc. Natl. Acad. Sci. U. S. A. 105 (2008), 2111–2116.
45. Zhao, Y., Samal, E., Srivastava, D., Serum response factor regulates a muscle-specific microRNA that targets Hand2 during cardiogenesis. Nature 436 (2005), 214–220.
46. Saxena, A., Tabin, C.J., miRNA-processing enzyme Dicer is necessary for cardiac outflow tract alignment and chamber septation. Proc. Natl. Acad. Sci. U. S. A. 107 (2010), 87–91.
47. Huang, Z.P., Chen, J.F., Regan, J.N., Maguire, C.T., Tang, R.H., Dong, X.R., et al. Loss of microRNAs in neural crest leads to cardiovascular syndromes resembling human congenital heart defects. Arterioscler. Thromb. Vasc. Biol. 30 (2010), 2575–2586.
48. Sheehy, N.T., Cordes, K.R., White, M.P., Ivey, K.N., Srivastava, D., The neural crest-enriched microRNA miR-452 regulates epithelial-mesenchymal signaling in the first pharyngeal arch. Development 137 (2010), 4307–4316.
49. Zehir, A., Hua, L.L., Maska, E.L., Morikawa, Y., Cserjesi, P., Dicer is required for survival of differentiating neural crest cells. Dev. Biol. 340 (2010), 459–467.
50. Mahdavi, V., Chambers, A.P., Nadal-Ginard, B., Cardiac alpha- and beta-myosin heavy chain genes are organized in tandem. Proc. Natl. Acad. Sci. U. S. A. 81 (1984), 2626–2630.
51. van Rooij, E., Quiat, D., Johnson, B.A., Sutherland, L.B., Qi, X., Richardson, J.A., et al. A family of microRNAs encoded by myosin genes governs myosin expression and muscle performance. Dev. Cell 17 (2009), 662–673.
52. Montgomery, R.L., Hullinger, T.G., Semus, H.M., Dickinson, B.A., Seto, A.G., Lynch, J.M., et al. Therapeutic inhibition of miR-208a improves cardiac function and survival during heart failure. Circulation 124 (2011), 1537–1547.
53. Grueter, C.E., van Rooij, E., Johnson, B.A., DeLeon, S.M., Sutherland, L.B., Qi, X., et al. A cardiac microRNA governs systemic energy homeostasis by regulation of MED13. Cell 149 (2012), 671–683.
54. Corsten, M.F., Dennert, R., Jochems, S., Kuznetsova, T., Devaux, Y., Hofstra, L., et al. Circulating MicroRNA-208b and MicroRNA-499 reflect myocardial damage in cardiovascular disease. Circ. Cardiovasc. Genet. 3 (2010), 499–506.
55. Xiao, J., Shen, B., Li, J., Lv, D., Zhao, Y., Wang, F., Xu, J., Serum microRNA-499 and microRNA-208a as biomarkers of acute myocardial infarction. Int. J. Clin. Exp. Med. 7 (2014), 136–141.
56. Gupta, S.K., Foinquinos, A., Thum, S., Remke, J., Zimmer, K., Bauters, C., et al. Preclinical development of a microRNA-based therapy for elderly patients with myocardial infarction. J. Am. Coll. Cardiol. 68 (2016), 1557–1571.
57. Sassi, Y., Avramopoulos, P., Ramanujam, D., Gruter, L., Werfel, S., Giosele, S., et al. Cardiac myocyte miR-29 promotes pathological remodeling of the heart by activating Wnt signaling. Nat. Commun., 8, 2017, 1614.
58. Chandrasekaran, S., Peterson, R.E., Mani, S.K., Addy, B., Buchholz, A.L., Xu, L., et al. Histone deacetylases facilitate sodium/calcium exchanger up-regulation in adult cardiomyocytes. FASEB J. 23 (2009), 3851–3864.
59. Cao, D.J., Wang, Z.V., Battiprolu, P.K., Jiang, N., Morales, C.R., Kong, Y., et al. Histone deacetylase (HDAC) inhibitors attenuate cardiac hypertrophy by suppressing autophagy. Proc. Natl. Acad. Sci. U. S. A. 108 (2011), 4123–4128.
60. Kee, H.J., Kook, H., Kruppel-like factor 4 mediates histone deacetylase inhibitor-induced prevention of cardiac hypertrophy. J. Mol. Cell. Cardiol. 47 (2009), 770–780.
61. Glenn, D.J., Wang, F., Chen, S., Nishimoto, M., Gardner, D.G., Endothelin-stimulated human B-type natriuretic peptide gene expression is mediated by Yin Yang 1 in association with histone deacetylase 2. Hypertension 53 (2009), 549–555.
62. Trivedi, C.M., Luo, Y., Yin, Z., Zhang, M., Zhu, W., Wang, T., et al. Hdac2 regulates the cardiac hypertrophic response by modulating Gsk3 beta activity. Nat. Med. 13 (2007), 324–331.
63. Kee, H.J., Eom, G.H., Joung, H., Shin, S., Kim, J.R., Cho, Y.K., et al. Activation of histone deacetylase 2 by inducible heat shock protein 70 in cardiac hypertrophy. Circ. Res. 103 (2008), 1259–1269.
64. Kee, H.J., Sohn, I.S., Nam, K.I., Park, J.E., Qian, Y.R., Yin, Z., et al. Inhibition of histone deacetylation blocks cardiac hypertrophy induced by angiotensin II infusion and aortic banding. Circulation 113 (2006), 51–59.
65. Zhu, H., Shan, L., Schiller, P.W., Mai, A., Peng, T., Histone deacetylase-3 activation promotes tumor necrosis factor-alpha (TNF-alpha) expression in cardiomyocytes during lipopolysaccharide stimulation. J. Biol. Chem. 285 (2010), 9429–9436.
66. Hohl, M., Wagner, M., Reil, J.C., Muller, S.A., Tauchnitz, M., Zimmer, A.M., et al. HDAC4 controls histone methylation in response to elevated cardiac load. J. Clin. Invest. 123 (2013), 1359–1370.
67. Granger, A., Abdullah, I., Huebner, F., Stout, A., Wang, T., Huebner, T., et al. Histone deacetylase inhibition reduces myocardial ischemia-reperfusion injury in mice. FASEB J. 22 (2008), 3549–3560.
68. Sucharov, C.C., Dockstader, K., McKinsey, T.A., YY1 protects cardiac myocytes from pathologic hypertrophy by interacting with HDAC5. Mol. Biol. Cell 19 (2008), 4141–4153.
69. Tao, R., de Zoeten, E.F., Ozkaynak, E., Chen, C., Wang, L., Porrett, P.M., et al. Deacetylase inhibition promotes the generation and function of regulatory T cells. Nat. Med. 13 (2007), 1299–1307.
70. Zhang, C.L., McKinsey, T.A., Chang, S., Antos, C.L., Hill, J.A., Olson, E.N., Class II histone deacetylases act as signal-responsive repressors of cardiac hypertrophy. Cell 110 (2002), 479–488.
71. Lai, H.L., Grachoff, M., McGinley, A.L., Khan, F.F., Warren, C.M., Chowdhury, S.A., et al. Maintenance of adult cardiac function requires the chromatin factor Asxl2. J. Mol. Cell. Cardiol. 53 (2012), 734–741.
72. Zhang, Q.J., Chen, H.Z., Wang, L., Liu, D.P., Hill, J.A., Liu, Z.P., The histone trimethyllysine demethylase JMJD2A promotes cardiac hypertrophy in response to hypertrophic stimuli in mice. J. Clin. Invest. 121 (2011), 2447–2456.
73. Ohtani, K., Vlachojannis, G.J., Koyanagi, M., Boeckel, J.N., Urbich, C., Farcas, R., et al. Epigenetic regulation of endothelial lineage committed genes in pro-angiogenic hematopoietic and endothelial progenitor cells. Circ. Res. 109 (2011), 1219–1229.
74. Stein, A.B., Jones, T.A., Herron, T.J., Patel, S.R., Day, S.M., Noujaim, S.F., et al. Loss of H3K4 methylation destabilizes gene expression patterns and physiological functions in adult murine cardiomyocytes. J. Clin. Invest. 121 (2011), 2641–2650.
75. Borlak, J., Thum, T., Hallmarks of ion channel gene expression in end-stage heart failure. FASEB J. 17 (2003), 1592–1608.
76. Diehl, F., Brown, M.A., van Amerongen, M.J., Novoyatleva, T., Wietelmann, A., Harriss, J., et al. Cardiac deletion of Smyd2 is dispensable for mouse heart development. PLoS One, 5, 2010, e9748.
77. Nguyen, A.T., Xiao, B., Neppl, R.L., Kallin, E.M., Li, J., Chen, T., et al. DOT1L regulates dystrophin expression and is critical for cardiac function. Genes Dev. 25 (2011), 263–274.