The long noncoding RNA Wisper controls cardiac fibrosis and remodeling

Science Translational Medicine

Volumn 9, Issue 395, 2017, Pages

  Micheletti, Rudi ^a,g   Plaisance, Isabelle ^a   Abraham, Brian J ^b   Sarre, Alexandre ^c   Ting, Ching Chia ^a   Alexanian, Michael ^a   Maric, Daniel ^a   Maison, Damien ^a   Nemir, Mohamed ^a   Young, Richard A ^b,d   Schroen, Blanche ^e   González, Arantxa ^f   Ounzain, Samir ^a   Pedrazzini, Thierry ^a  

^a University of Lausanne Medical Center   (Switzerland)

^b WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^c UNIVERSITY OF LAUSANNE   (Switzerland)

^d MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^e MAASTRICHT UNIVERSITY   (Netherlands)

^f UNIVERSITY OF NAVARRA   (Spain)

^g INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; LONG UNTRANSLATED RNA; LYSYL HYDROXYLASE 2; PROCOLLAGEN LYSINE 2 OXOGLUTARATE 5 DIOXYGENASE; UNCLASSIFIED DRUG; WISP2 SUPER ENHANCER ASSOCIATED RNA;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTIC STENOSIS; ARTICLE; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; EMBRYO; EXTRACELLULAR MATRIX; GENE EXPRESSION; GENE SILENCING; HEART FIBROBLAST; HEART INFARCTION; HEART MUSCLE FIBROSIS; HEART VENTRICLE REMODELING; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NEWBORN; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; CARDIOMYOPATHY; FIBROBLAST; FIBROSIS; GENETICS; METABOLISM; PATHOLOGY; PHYSIOLOGY;

CARDIOMYOPATHIES; FIBROBLASTS; FIBROSIS; HUMANS; RNA, LONG NONCODING; VENTRICULAR REMODELING;

EID: 85021091121     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.aai9118     Document Type: Article

References (65)

1. S. D. Prabhu, N. G. Frangogiannis, The biological basis for cardiac repair after myocardial infarction: From inflammation to fibrosis. Circ. Res. 119, 91-112 (2016).
2. N. G. Frangogiannis, Pathophysiology of myocardial infarction. Compr. Physiol. 5, 1841-1875 (2015).
3. Writing Group Members, D. Mozaffarian, E. J. Benjamin, A. S. Go, D. K. Arnett, M. J. Blaha, M. Cushman, S. R. Das, S. de Ferranti, J.-P. Després, H. J. Fullerton, V. J. Howard, M. D. Huffman, C. R. Isasi, M. C Jiménez, S. E. Judd, B. M. Kissela, J. H. Lichtman, L. D. Lisabeth, S. Liu, R. H. Mackey, D. J. Magid, D. K. McGuire, E. R. Mohler III, C. S. Moy, P. Muntner, M. E. Mussolino, K. Nasir, R. W. Neumar, G. Nichol, L. Palaniappan, D. K. Pandey, M. J. Reeves, C.J. Rodriguez, W. Rosamond, P. D. Sorlie, J. Stein, A. Towfighi, T. N. Turan, S. S. Virani, D. Woo, R. W. Yeh, M. B. Turner; American Heart Association Statistics Committee; Stroke Statistics Subcommittee, Heart disease and stroke statistics - 2016 update: A report from the American Heart Association. Circulation 133, e38-e360 (2016).
4. F. G. Spinale, M. R. Zile, Integrating the myocardial matrix into heart failure recognition and management. Circ. Res. 113, 725-738 (2013).
5. E. B. Schelbert, G. C. Fonarow, R. O. Bonow, J. Butler, M. Gheorghiade, Therapeutic targets in heart failure: Refocusing on the myocardial interstitium. J. Am. Coll. Cardiol. 63, 2188-2198 (2014).
6. K. T. Weber, Y. Sun, S. K. Bhattacharya, R. A. Ahokas, I. C. Gerling, Myofibroblast-mediated mechanisms of pathological remodelling of the heart. Nat. Rev. Cardiol. 10, 15-26 (2013).
7. J. K. Lighthouse, E. M. Small, Transcriptional control of cardiac fibroblast plasticity. J. Mol. Cell. Cardiol. 91, 52-60 (2016).
8. K. B. Schuetze, T. A. McKinsey, C. S. Long, Targeting cardiac fibroblasts to treat fibrosis of the heart: Focus on HDACs. J. Mol. Cell. Cardiol. 70, 100-107 (2014).
9. S. Ounzain, T. Pedrazzini, The promise of enhancer-associated long noncoding RNAs in cardiac regeneration. Trends Cardiovasc. Med. 25, 592-602 (2015).
10. S. Ounzain, T. Pedrazzini, Super-enhancer Incs to cardiovascular development and disease. Biochim. Biophys. Acta 1863, 1953-1960 (2016).
11. J. A. Wamstad, X. Wang, O. O. Demuren, L. A. Boyer, Distal enhancers: New insights into heart development and disease. Trends Cell Biol. 24, 294-302 (2014).
12. D. Hnisz, B. J. Abraham, T. I. Lee, A. Lau, V. Saint-Andre, A. A. Sigova, H. A. Hoke, R. A. Young, Super-enhancers in the control of cell identity and disease. Cell 155, 934-947 (2013).
13. W. A. Whyte, D. A. Orlando, D. Hnisz, B. J. Abraham, C. Y. Lin, M. H. Kagey, P. B. Rahl, T. I. Lee, R. A. Young, Master transcription factors and mediator establish super-enhancers at key cell identity genes. Cell 153, 307-319 (2013).
14. A. R. Niederriter, A. Varshney, S. C. J. Parker, D. M. Martin, Super enhancers in cancers, complex disease, and developmental disorders. Genes 6, 1183-1200 (2015).
15. K. V. Morris, J. S. Mattick, The rise of regulatory RNA. Nat. Rev. Genet. 15, 423-437 (2014).
16. R. Kumarswamy, T. Thum, Non-coding RNAs in cardiac remodeling and heart failure. Circ. Res. 113, 676-689 (2013).
17. E. E. Creemers, E. van Rooij, Function and therapeutic potential of noncoding rnas in cardiac fibrosis. Circ. Res. 118, 108-118 (2016).
18. R. A. Boon, S. Dimmeler, MicroRNAs in myocardial infarction. Nat. Rev. Cardiol. 12, 135-142 (2015).
19. S. Ounzain, R. Micheletti, C. Arnan, I. Plaisance, D. Cecchi, B. Schroen, F. Reverter, M. Alexanian, C. Gonzales, S. Y. Ng, G. Bussotti, I. Pezzuto, C. Notredame, S. Heymans, R. Guigó, R. Johnson, T. Pedrazzini, CARMEN, a human super enhancer-associated long noncoding RNA controlling cardiac specification, differentiation and homeostasis. J. Mol. Cell. Cardiol. 89, 98-112 (2015).
20. P. Han, W. Li, C.-H. Lin, J. Yang, C. Shang, S. T. Nurnberg, K. K. Jin, W. Xu, C.-Y. Lin, C-J. Lin, Y. Xiong, H. C. Chien, B. Zhou, E. Ashley, D. Bernstein, P.-S. Chen, H.-S. Chen, T. Quertermous, C.-P. Chang, A long noncoding RNA protects the heart from pathological hypertrophy. Nature 514, 102-106 (2014).
21. J. Viereck, R. Kumarswamy, A. Foinquinos, K. Xiao, P. Avramopoulos, M. Kunz, M. Dittrich, T. Maetzig, K. Zimmer, J. Remke, A. Just, J. Fendrich, K. Scherf, E. Bolesani, A. Schambach, F. Weidemann, R. Zweigerdt, L. J. de Windt, S. Engelhardt, T. Dandekar, S. Batkai, T. Thum, Long noncoding RNA Chast promotes cardiac remodeling. Sci. Transl. Med. 8, 326ra322 (2016).
22. K. Wang, F. Liu, L.-Y. Zhou, B. Long, S.-M. Yuan, Y. Wang, C.-Y. Liu, T. Sun, X.-J. Zhang, P.-F. Li, The long noncoding RNA CHRF regulates cardiac hypertrophy by targeting miR-489. Circ. Res. 114, 1377-1388 (2014).
23. M.-T. Piccoli, C. Bär, T. Thum, Non-coding RNAs as modulators of the cardiac fibroblast phenotype. J. Mol. Cell. Cardiol. 92, 75-81 (2016).
24. T. R. Mercer, J. S. Mattick, Structure and function of long noncoding RNAs in epigenetic regulation. Nat. Struct. Mol. Biol. 20, 300-307 (2013).
25. W. Li, D. Notani, M. G. Rosenfeld, Enhancers as non-coding RNA transcription units: Recent insights and future perspectives. Nat. Rev. Genet. 17, 207-223 (2016).
26. A. A. Sigova, A. C. Mullen, B. Molinie, S. Gupta, D. A. Orlando, M. G. Guenther, A. E. Almada, C. Lin, P. A. Sharp, C. C. Giallourakis, R. A. Young, Divergent transcription of long noncoding RNA/mRNA gene pairs in embryonic stem cells. Proc. Natl. Acad. Sci. U.S.A. 110,2876-2881 (2013).
27. A. A. Sigova, B. J. Abraham, X. Ji, B. Molinie, N. M. Hannett, Y. E. Guo, M. Jangi, C. C. Giallourakis, P. A. Sharp, R. A. Young, Transcription factor trapping by RNA in gene regulatory elements. Science 350, 978-981 (2015).
28. M. Melé, J. L. Rinn, "Cat's Cradling" the 3D genome by the act of LncRNA transcription. Mol. Cell 62, 657-664 (2016).
29. S. Ounzain, R. Micheletti, T. Beckmann, B. Schroen, M. Alexanian, I. Pezzuto, S. Crippa, M. Nemir, A. Sarre, R. Johnson, J. Dauvillier, F. Burdet, M. Ibberson, R. Guigó, I. Xenarios, S. Heymans, T. Pedrazzini, Genome-wide profiling of the cardiac transcriptome after myocardial infarction identifies novel heart-specific long non-coding RNAs. Eur. Heart J. 36, 353-368 (2015).
30. S. Ounzain, I. Pezzuto, R. Micheletti, F. Burdet, R. Sheta, M. Nemir, C. Gonzales, A. Sarre, M. Alexanian, M. J. Blow, D. May, R. Johnson, J. Dauvillier, L. A. Pennacchio, T. Pedrazzini, Functional importance of cardiac enhancer-associated noncoding RNAs in heart development and disease. J. Mol. Cell. Cardiol. 76, 55-70 (2014).
31. D. Jeong, M.-A. Lee, Y. Li, D. K. Yang, C Kho, J. G. Oh, G. Hong, A. Lee, M. H. Song, T. J. LaRocca, J. Chen, L. Liang, S. Mitsuyama, V. D'Escamard, J. C. Kovacic, T. H. Kwak, R. J. Hajjar, W. J. Park, Matricellular protein CCN5 reverses established cardiac fibrosis. J. Am. Coll. Cardiol. 67, 1556-1568 (2016).
32. S. Pott, J. D. Lieb, What are super-enhancers? Nat. Genet. 47, 8-12 (2015).
33. T. Okubo, B. L. M. Hogan, Hyperactive Wnt signaling changes the developmental potential of embryonic lung endoderm. J Biol. 3, 11 (2004).
34. N. G. Frangogiannis, The inflammatory response in myocardial injury, repair, and remodelling. Nat. Rev. Cardiol. 11, 255-265 (2014).
35. P. Wiesel, L. Mazzolai, J. Nussberger, T. Pedrazzini, Two-kidney, one clip and one-kidney, one clip hypertension in mice. Hypertension 29, 1025-1030 (1997).
36. S. Konermann, M. D. Brigham, A. E. Trevino, J. Joung, O. O. Abudayyeh, C Barcena, P. D. Hsu, N. Habib, J. S. Gootenberg, H. Nishimasu, O. Nureki, F. Zhang, Genome-scale transcriptional activation by an engineered CRISPR-Cas9 complex. Nature 517, 583-588 (2015).
37. F. Yang, F. Yi, X. Han, Q. Du, Z. Liang, MALAT-1 interacts with hnRNP C in cell cycle regulation. FEBS Lett. 587, 3175-3181 (2013).
38. E. Hacisuleyman, L. A. Goff, C. Trapnell, A. Williams, J. Henao-Mejia, L. Sun, P. McClanahan, D. G. Hendrickson, M. Sauvageau, D. R. Kelley, M. Morse, J. Engreitz, E. S. Lander, M. Guttman, H. F. Lodish, R. Flavell, A. Raj, J. L. Rinn, Topological organization of multichromosomal regions by the long intergenic noncoding RNA Firre. Nat. Struct. Mol. Biol. 21, 198-206 (2014).
39. C. Le Guiner, F. Lejeune, D. Galiana, L. Kister, R. Breathnach, J. Stévenin, F. Del Gatto-Konczak, TIA-1 and TIAR activate splicing of alternative exons with weak 5' splice sites followed by a U-rich stretch on their own pre-mRNAs. J. Biol. Chem. 276, 40638-40646 (2001).
40. S. Waris, M. C J. Wilce, J. A. Wilce, RNA recognition and stress granule formation by TIA proteins. Int. J. Mol. Sci. 15, 23377-23388 (2014).
41. L.-Y. Tan, P. Whitfield, M. Llorian, E. Monzon-Casanova, M. D. Diaz-Munoz, M. Turner, C. W. J. Smith, Generation of functionally distinct isoforms of PTBP3 by alternative splicing and translation initiation. Nucleic Acids Res. 43, 5586-5600 (2015).
42. Y. Blech-Hermoni, S. J. Stillwagon, A. N. Ladd, Diversity and conservation of CELF1 and CELF2 RNA and protein expression patterns during embryonic development. Dev. Dyn. 242, 767-777 (2013).
43. G. Haas, S. Cetin, M. Messmer, B. Chane-Woon-Ming, O. Terenzi, J. Chicher, L. Kuhn, P. Hammann, S. Pfeffer, Identification of factors involved in target RNA-directed microRNA degradation. Nucleic Acids Res. 44, 2873-2887 (2016).
44. H. N. Yeowell, L. C. Walker, D. M. Mauger, P. Seth, M. A. Garcia-Blanco, TIA nuclear proteins regulate the alternate splicing of lysyl hydroxylase 2. J. Invest. Dermatol. 129, 1402-1411 (2009).
45. T. Zhang, N. Delestienne, G. Huez, V. Kruys, C. Gueydan, Identification of the sequence determinants mediating the nucleo-cytoplasmic shuttling of TIAR and TIA-1 RNA-binding proteins. J. Cell Sci. 118,5453-5463 (2005).
46. 1 up-regulation. Clin. Sci. 126, 497-506 (2014).
47. G. Rizki, L. A. Boyer, Lncing epigenetic control of transcription to cardiovascular development and disease. Circ. Res. 117, 192-206 (2015).
48. Z. Wang, X.-J. Zhang, Y.-X. Ji, P. Zhang, K.-Q. Deng, J. Gong, S. Ren, X. Wang, I. Chen, H. Wang, C. Gao, T. Yokota, Y. S. Ang, S. Li, A. Cass, T. M. Vondriska, G. Li, A. Deb, D. Srivastava, H.-T. Yang, X. Xiao, H. Li, Y. Wang, The long noncoding RNA Chaer defines an epigenetic checkpoint in cardiac hypertrophy. Nat. Med. 22, 1131-1139 (2016).
49. C. Sánchez-Jimenez, J. M. Izquierdo, T-cell intracellular antigens in health and disease. Cell Cycle 14, 2033-2043 (2015).
50. J. Wu, D. P. Reinhardt, C. Batmunkh, W. Lindenmaier, R. K-K. Far, H. Notbohm, N. Hunzelmann, J. Brinckmann, Functional diversity of lysyl hydroxylase 2 in collagen synthesis of human dermal fibroblasts. Exp. Cell Res. 312, 3485-3494 (2006).
51. Z. Wang, M. Kayikci, M. Briese, K. Zarnack, N. M. Luscombe, G. Rot, B. Zupan, T. Curk, J. Ule, iCLIP predicts the dual splicing effects of TIA-RNA interactions. PLOS Biol. 8, e1000530 (2010).
52. L. Liu, H. Yue, Q. Liu, J. Yuan, J. Li, G. Wei, X. Chen, Y. Lu, M. Guo, J. Luo, R. Chen, LncRNA MT1JP functions as a tumor suppressor by interacting with TIAR to modulate the p53 pathway. Oncotarget 7, 15787-15800 (2016).
53. C. Sánchez-Jiménez, J. M. Izquierdo, T-cell intracellular antigen (TIA)-proteins deficiency in murine embryonic fibroblasts alters cell cycle progression and induces autophagy. PLOS ONE 8, e75127 (2013).
54. J. Davis, N. Salomonis, N. Ghearing, S.-C. J. Lin, J. Q. Kwong, A. Mohan, M. S. Swanson, J. D. Molkentin, MBNL1-mediated regulation of differentiation RNAs promotes myofibroblast transformation and the fibrotic response. Nat. Commun. 6, 10084 (2015).
55. R. Kumarswamy, C. Bauters, I. Volkmann, F. Maury, J. Fetisch, A. Holzmann, G. Lemesle, P. de Groote, F. Pinet, T. Thum, Circulating long noncoding RNA, LIPCAR, predicts survival in patients with heart failure. Circ. Res. 114, 1569-1575 (2014).
56. B. E. Bernstein, J. A. Stamatoyannopoulos, J. F. Costello, B. Ren, A. Milosavljevic, A. Meissner, M. Kellis, M. A. Marra, A. L. Beaudet, J. R. Ecker, P. J. Farnham, M. Hirst, E. S. Lander, T. S. Mikkelsen, J. A. Thomson, The NIH roadmap epigenomics mapping consortium. Nat. Biotechnol. 28, 1045-1048 (2010).
57. L. H. Michael, M. L. Entman, C. J. Hartley, K. A. Youker, J. Zhu, S. R. Hall, H. K. Hawkins, K. Berens, C. M. Ballantyne, Myocardial ischemia and reperfusion: A murine model. Am. J. Physiol. 269, H2147-H2154 (1995).
58. B. López, R. Querejeta, A. González, M. Larman, J. Díez, Collagen cross-linking but not collagen amount associates with elevated filling pressures in hypertensive patients with stage C heart failure: Potential role of lysyl oxidase. Hypertension 60, 677-683 (2012).
59. A. Dobin, C. A. Davis, F. Schlesinger, J. Drenkow, C. Zaleski, S. Jha, P. Batut, M. Chaisson, T. R. Gingeras, STAR: Ultrafast universal RNA-seq aligner. Bioinformatics 29, 15-21 (2013).
60. S. Anders, P. T. Pyl, W. Huber, HTSeq - A Python framework to work with high-throughput sequencing data. Bioinformatics 31, 166-169 (2015).
61. L. Wang, S. Wang, W. Li, RSeQC: Quality control of RNA-seq experiments. Bioinformatics 28, 2184-2185 (2012).
62. B. Li, C. N. Dewey, RSEM: Accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bionformatics 12, 323 (2011).
63. M. D. Robinson, D. J. McCarthy, G. K. Smyth, edgeR: A Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139-140 (2010).
64. M. E. Ritchie, B. Phipson, D. Wu, Y. Hu, C. W. Law, W. Shi, G. K. Smyth, limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 43, e47 (2015).
65. Y. Benjamini, Y. Hochberg, Controlling the false discovery rate: A practical and powerful approach to multiple testing. J. R. Stat. Soc. Series B Stat. Methodol. 57, 289-300 (1995).