The promise of enhancer-associated long noncoding RNAs in cardiac regeneration

Trends in Cardiovascular Medicine

Volumn 25, Issue 7, 2015, Pages 592-602

  Ounzain, Samir ^a   Pedrazzini, Thierry ^a  

^a University of Lausanne Medical Center   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

UNTRANSLATED RNA; LONG UNTRANSLATED RNA;

CARDIOVASCULAR DISEASE; ENHANCER REGION; GENE CONTROL; GENETIC TRANSCRIPTION; GENOME; HEART DEVELOPMENT; HEART FAILURE; HEART STRESS; HUMAN; NONHUMAN; PRIORITY JOURNAL; REVIEW; STEM CELL TRANSPLANTATION; TISSUE REGENERATION; ANIMAL; CARDIAC MUSCLE; CARDIAC MUSCLE CELL; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL REPROGRAMMING TECHNIQUE; CONVALESCENCE; GENE EXPRESSION REGULATION; GENE THERAPY; GENETICS; METABOLISM; NUCLEAR REPROGRAMMING; PATHOLOGY; PATHOPHYSIOLOGY; PROCEDURES; REGENERATION; TRANSPLANTATION;

ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLULAR REPROGRAMMING; CELLULAR REPROGRAMMING TECHNIQUES; GENE EXPRESSION REGULATION; GENETIC THERAPY; HEART FAILURE; HUMANS; MYOCARDIUM; MYOCYTES, CARDIAC; RECOVERY OF FUNCTION; REGENERATION; RNA, LONG NONCODING; TRANSCRIPTION, GENETIC;

EID: 84941996167     PISSN: 10501738     EISSN: 18732615     Source Type: Journal    
DOI: 10.1016/j.tcm.2015.01.014     Document Type: Review

References (64)

1. Go A.S., Mozaffarian D., Roger V.L., et al. Executive summary: heart disease and stroke statistics-2013 update: a report from the American Heart Association. Circulation 2013, 127:143-152.
2. Fox I.J., Daley G.Q., Goldman S.A., Huard J., Kamp T.J., Trucco M. Stem cell therapy. Use of differentiated pluripotent stem cells as replacement therapy for treating disease. Science 2014, 345:1247391.
3. Garbern J.C., Lee R.T. Cardiac stem cell therapy and the promise of heart regeneration. Cell Stem Cell 2013, 12:689-698.
4. Bergmann O., Bhardwaj R.D., Bernard S., et al. Evidence for cardiomyocyte renewal in humans. Science 2009, 324:98-102.
5. Koitabashi N., Kass D.A. Reverse remodeling in heart failure-mechanisms and therapeutic opportunities. Nat Rev Cardiol 2012, 9:147-157.
6. Oh Y., Wei H., Ma D., Sun X., Liew R. Clinical applications of patient-specific induced pluripotent stem cells in cardiovascular medicine. Heart 2012, 98:443-449.
7. van Berlo J.H., Molkentin J.D. An emerging consensus on cardiac regeneration. Nat Med 2014, 20:1386-1393.
8. Christoffels V.M., Pu W.T. Developing insights into cardiac regeneration. Development 2013, 140:3933-3937.
9. Eulalio A., Mano M., Dal Ferro M., et al. Functional screening identifies miRNAs inducing cardiac regeneration. Nature 2012, 492:376-381.
10. Jopling C., Sleep E., Raya M., Marti M., Raya A., Izpisua Belmonte J.C. Zebrafish heart regeneration occurs by cardiomyocyte dedifferentiation and proliferation. Nature 2010, 464:606-609.
11. Kikuchi K., Holdway J.E., Werdich A.A., et al. Primary contribution to zebrafish heart regeneration by gata4(+) cardiomyocytes. Nature 2010, 464:601-605.
12. Porrello E.R., Mahmoud A.I., Simpson E., et al. Transient regenerative potential of the neonatal mouse heart. Science 2011, 331:1078-1080.
13. Ieda M., Fu J.D., Delgado-Olguin P., et al. Direct reprogramming of fibroblasts into functional cardiomyocytes by defined factors. Cell 2010, 142:375-386.
14. Qian L., Huang Y., Spencer C.I., et al. In vivo reprogramming of murine cardiac fibroblasts into induced cardiomyocytes. Nature 2012, 485:593-598.
15. Song K., Nam Y.J., Luo X., et al. Heart repair by reprogramming non-myocytes with cardiac transcription factors. Nature 2012, 485:599-604.
16. Bruneau B.G. Signaling and transcriptional networks in heart development and regeneration. Cold Spring Harb Perspect Biol 2013, 5:a008292.
17. He A., Kong S.W., Ma Q., Pu W.T. Co-occupancy by multiple cardiac transcription factors identifies transcriptional enhancers active in heart. Proc Natl Acad Sci U S A 2011, 108:5632-5637.
18. Wamstad J.A., Wang X., Demuren O.O., Boyer L.A. Distal enhancers: new insights into heart development and disease. Trends Cell Biol 2014, 24:294-302.
19. Bonora G., Plath K., Denholtz M. A mechanistic link between gene regulation and genome architecture in mammalian development. Curr Opin Genet Dev 2014, 27:92-101.
20. Consortium E.P., Dunham I., Kundaje A., et al. An integrated encyclopedia of DNA elements in the human genome. Nature 2012, 489:57-74.
21. Yue F., Cheng Y., Breschi A., et al. A comparative encyclopedia of DNA elements in the mouse genome. Nature 2014, 515:355-364.
22. Lam M.T., Li W., Rosenfeld M.G., Glass C.K. Enhancer RNAs and regulated transcriptional programs. Trends Biochem Sci 2014, 39:170-182.
23. Orom U.A., Shiekhattar R. Long noncoding RNAs usher in a new era in the biology of enhancers. Cell 2013, 154:1190-1193.
24. Batista P.J., Chang H.Y. Long noncoding RNAs: cellular address codes in development and disease. Cell 2013, 152:1298-1307.
25. Mercer T.R., Mattick J.S. Structure and function of long noncoding RNAs in epigenetic regulation. Nat Struct Mol Biol 2013, 20:300-307.
26. Ounzain S., Crippa S., Pedrazzini T. Small and long non-coding RNAs in cardiac homeostasis and regeneration. Biochim Biophys Acta 2013, 1833:923-933.
27. Gama-Carvalho M., Andrade J., Bras-Rosario L. Regulation of cardiac cell fate by microRNAs: implications for Heart regeneration. Cells 2014, 3:996-1026.
28. Olson E.N. MicroRNAs as therapeutic targets and biomarkers of cardiovascular disease. Sci Transl Med 2014, 6:239ps233.
29. Jayawardena T.M., Egemnazarov B., Finch E.A., et al. MicroRNA-mediated in vitro and in vivo direct reprogramming of cardiac fibroblasts to cardiomyocytes. Circ Res 2012, 110:1465-1473.
30. Jayawardena T.M., Finch E.A., Zhang L., et al. MicroRNA induced cardiac reprogramming in vivo: evidence for mature cardiac myocytes and improved cardiac function. Circ Res 2015, 116:418-424.
31. Tay Y., Rinn J., Pandolfi P.P. The multilayered complexity of ceRNA crosstalk and competition. Nature 2014, 505:344-352.
32. Ounzain S., Micheletti R., Beckmann T., et al. Genome-wide profiling of the cardiac transcriptome after myocardial infarction identifies novel heart-specific long non-coding RNAs. Eur Heart J 2015, 36:353-368.
33. Hu W., Alvarez-Dominguez J.R., Lodish H.F. Regulation of mammalian cell differentiation by long non-coding RNAs. EMBO Rep 2012, 13:971-983.
34. Flynn R.A., Chang H.Y. Long noncoding RNAs in cell-fate programming and reprogramming. Cell Stem Cell 2014, 14:752-761.
35. Loewer S., Cabili M.N., Guttman M., et al. Large intergenic non-coding RNA-RoR modulates reprogramming of human induced pluripotent stem cells. Nat Genet 2010, 42:1113-1117.
36. Buecker C., Wysocka J. Enhancers as information integration hubs in development: lessons from genomics. Trends Genet 2012, 28:276-284.
37. Xie W., Ren B. Developmental biology. Enhancing pluripotency and lineage specification. Science 2013, 341:245-247.
38. Blow M.J., McCulley D.J., Li Z., et al. ChIP-Seq identification of weakly conserved heart enhancers. Nat Genet 2010, 42:806-810.
39. Wamstad J.A., Alexander J.M., Truty R.M., et al. Dynamic and coordinated epigenetic regulation of developmental transitions in the cardiac lineage. Cell 2012, 151:206-220.
40. Maurano M.T., Humbert R., Rynes E., et al. Systematic localization of common disease-associated variation in regulatory DNA. Science 2012, 337:1190-1195.
41. Hnisz D., Abraham B.J., Lee T.I., et al. Super-enhancers in the control of cell identity and disease. Cell 2013, 155:934-947.
42. Parker S.C., Stitzel M.L., Taylor D.L., et al. Chromatin stretch enhancer states drive cell-specific gene regulation and harbor human disease risk variants. Proc Natl Acad Sci U S A 2013, 110:17921-17926.
43. Whyte W.A., Orlando D.A., Hnisz D., et al. Master transcription factors and mediator establish super-enhancers at key cell identity genes. Cell 2013, 153:307-319.
44. He A., Gu F., Hu Y., et al. Dynamic GATA4 enhancers shape the chromatin landscape central to heart development and disease. Nat Commun 2014, 5:4907.
45. Papait R., Cattaneo P., Kunderfranco P., et al. Genome-wide analysis of histone marks identifying an epigenetic signature of promoters and enhancers underlying cardiac hypertrophy. Proc Natl Acad Sci U S A 2013, 110:20164-20169.
46. Bulger M., Groudine M. Functional and mechanistic diversity of distal transcription enhancers. Cell 2011, 144:327-339.
47. Marques A.C., Hughes J., Graham B., Kowalczyk M.S., Higgs D.R., Ponting C.P. Chromatin signatures at transcriptional start sites separate two equally populated yet distinct classes of intergenic long noncoding RNAs. Genome Biol 2013, 14:R131.
48. De Santa F., Barozzi I., Mietton F., et al. A large fraction of extragenic RNA pol II transcription sites overlap enhancers. PLoS Biol 2010, 8:e1000384.
49. Ounzain S., Pezzuto I., Micheletti R., et al. Functional importance of cardiac enhancer-associated noncoding RNAs in heart development and disease. J Mol Cell Cardiol 2014, 76:55-70.
50. Orom U.A., Derrien T., Beringer M., et al. Long noncoding RNAs with enhancer-like function in human cells. Cell 2010, 143:46-58.
51. Wang K.C., Yang Y.W., Liu B., et al. A long noncoding RNA maintains active chromatin to coordinate homeotic gene expression. Nature 2011, 472:120-124.
52. Li W., Notani D., Ma Q., et al. Functional roles of enhancer RNAs for oestrogen-dependent transcriptional activation. Nature 2013, 498:516-520.
53. Schaukowitch K., Joo J.Y., Liu X., Watts J.K., Martinez C., Kim T.K. Enhancer RNA facilitates NELF release from immediate early genes. Mol Cell 2014, 56:29-42.
54. Guttman M., Donaghey J., Carey B.W., et al. lincRNAs act in the circuitry controlling pluripotency and differentiation. Nature 2011, 477:295-300.
55. Klattenhoff C.A., Scheuermann J.C., Surface L.E., et al. Braveheart, a long noncoding RNA required for cardiovascular lineage commitment. Cell 2013, 152:570-583.
56. He A., Ma Q., Cao J., et al. Polycomb repressive complex 2 regulates normal development of the mouse heart. Circ Res 2012, 110:406-415.
57. Grote P., Wittler L., Hendrix D., et al. The tissue-specific lncRNA Fendrr is an essential regulator of heart and body wall development in the mouse. Dev Cell 2013, 24:206-214.
58. Pipes G.C., Creemers E.E., Olson E.N. The myocardin family of transcriptional coactivators: versatile regulators of cell growth, migration, and myogenesis. Genes Dev 2006, 20:1545-1556.
59. Matkovich S.J., Edwards J.R., Grossenheider T.C., de Guzman Strong C., Dorn G.W. Epigenetic coordination of embryonic heart transcription by dynamically regulated long noncoding RNAs. Proc Natl Acad Sci U S A 2014, 111:12264-12269.
60. Werber M., Wittler L., Timmermann B., Grote P., Herrmann B.G. The tissue-specific transcriptomic landscape of the mid-gestational mouse embryo. Development 2014, 141:2325-2330.
61. Yang K.C., Yamada K.A., Patel A.Y., et al. Deep RNA sequencing reveals dynamic regulation of myocardial noncoding RNAs in failing human heart and remodeling with mechanical circulatory support. Circulation 2014, 129:1009-1021.
62. Han P., Li W., Lin C.H., et al. A long noncoding RNA protects the heart from pathological hypertrophy. Nature 2014, 514:102-106.
63. Hang C.T., Yang J., Han P., et al. Chromatin regulation by Brg1 underlies heart muscle development and disease. Nature 2010, 466:62-67.
64. Takahashi H., Carninci P. Widespread genome transcription: new possibilities for RNA therapies. Biochem Biophys Res Commun 2014, 452:294-301.