Long non-coding RNAs as master regulators in cardiovascular diseases

International Journal of Molecular Sciences

Volumn 16, Issue 10, 2015, Pages 23651-23667

  Archer, Krystal ^a   Broskova, Zuzana ^a   Bayoumi, Ahmed S ^a   Teoh, Jian Peng ^a   Davila, Alec ^a   Tang, Yaoliang ^a   Su, Huabo ^a   Kim, Il Man ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

Chromatin; Epigenetic regulation; Gene regulation; Heart disease; Non coding RNAs

Indexed keywords

CARDIAC APOPTOSIS RELATED LONG UNTRANSLATED RNA; GENOMIC DNA; LONG UNTRANSLATED RNA; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; BIOLOGICAL MARKER;

AMYLOID PLAQUE; APOPTOSIS; ATHEROSCLEROSIS; CARDIOVASCULAR DISEASE; CORONARY ARTERY DISEASE; DOWN REGULATION; GENE EXPRESSION; HEART DEVELOPMENT; HEART FAILURE; HEART INFARCTION; HEART VENTRICLE HYPERTROPHY; HUMAN; MORTALITY; PATHOGENESIS; REPERFUSION INJURY; REVIEW; SIGNAL TRANSDUCTION; UPREGULATION; CARDIOVASCULAR DISEASES; DISEASE COURSE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; PROGNOSIS;

BIOMARKERS; CARDIOVASCULAR DISEASES; DISEASE PROGRESSION; GENE EXPRESSION REGULATION; HUMANS; PROGNOSIS; RNA, LONG NONCODING;

EID: 84943645643     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms161023651     Document Type: Review

References (73)

1. Ezkurdia, I.; Juan, D.; Rodriguez, J.M.; Frankish, A.; Diekhans, M.; Harrow, J.; Vazquez, J.; Valencia, A.; Tress, M.L. The shrinking human protein coding complement: Are there now fewer than 20,000 genes? Available online: http://arxiv.org/abs/1312.7111 (accessed on 1 July 2015).
2. Rinn, J.L.; Chang, H.Y. Genome regulation by long noncoding RNAs. Annu. Rev. Biochem. 2012, 81, 145-166.
3. Ma, Y.; Ma, W.; Huang, L.; Feng, D.; Cai, B. Long non-coding RNAs, a new important regulator of cardiovascular physiology and pathology. Int. J. Cardiol. 2015, 188, 105-110.
4. Sonoki, H.; Sato, T.; Endo, S.; Matsunaga, T.; Yamaguchi, M.; Yamazaki, Y.; Sugatani, J.; Ikari, A. Quercetin decreases claudin-2 expression mediated by up-regulation of microRNA miR-16 in Lung adenocarcinoma A549 cells. Nutrients 2015, 7, 4578-4592.
5. Agrawal, N.; Dasaradhi, P.V.N.; Mohmmed, A.; Malhotra, P.; Bhatnagar, R.K.; Mukherjee, S.K. RNA interference: Biology, mechanism, and applications. Microbiol. Mol. Biol. Rev. 2003, 67, 657-685.
6. Mercer, T.R.; Dinger, M.E.; Mattick, J.S. Long non-coding RNAs: Insights into functions. Nat. Rev. Genet. 2009, 10, 155-159.
7. Young, R.S.; Ponting, C.P. Identification and function of long non-coding RNAs. Essays Biochem. 2013, 54, 113-126.
8. Kaikkonen, M.U.; Lam, M.T.Y.; Glass, C.K. Non-coding RNAs as regulators of gene expression and epigenetics. Cardiovasc. Res. 2011, 90, 430-440.
9. Klattenhoff, C.A.; Scheuermann, J.C.; Surface, L.E.; Bradley, R.K.; Fields, P.A.; Steinhauser, M.L.; Ding, H.; Butty, V.L.; Torrey, L.; Haas, S. Braveheart, a long noncoding RNA required for cardiovascular lineage commitment. Cell 2013, 152, 570-583.
10. Wang, K.; Liu, F.; Zhou, L.Y.; Long, B.; Yuan, S.M.; Wang, Y.; Liu, C.Y.; Sun, T.; Zhang, X.J.; Li, P.F. The long noncoding RNA CHRF regulates cardiac hypertrophy by targeting miR-489. Circ. Res. 2014, 114, 1377-1388.
11. Moran, V.A.; Perera, R.J.; Khalil, A.M. Emerging functional and mechanistic paradigms of mammalian long non-coding RNAs. Nucleic Acids Res. 2012, 40, 6391-6400.
12. Ma, L.; Bajic, V.B.; Zhang, Z. On the classification of long non-coding RNAs. RNA Biol. 2013, 10, 924-933.
13. Birney, E.; Stamatoyannopoulos, J.A.; Dutta, A.; Guigó, R.; Gingeras, T.; Margulies, E.H.; Weng, Z.; Snyder, M.; Dermitzakis, E.T.; Thurman, R.E.; et al. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 2007, 447, 799-816.
14. Prensner, J.R.; Iyer, M.K.; Balbin, O.A.; Dhanasekaran, S.M.; Cao, Q.; Brenner, J.C.; Laxman, B.; Asangani, I.A.; Grasso, C.S.; Kominsky, H.D.; et al. Transcriptome sequencing across a prostate cancer cohort identifies PCAT-1, an unannotated lincRNA implicated in disease progression. Nat. Biotechnol. 2011, 29, 742-749.
15. Cheng, J.; Kapranov, P.; Drenkow, J.; Dike, S.; Brubaker, S.; Patel, S.; Long, J.; Stern, D.; Tammana, H.; Helt, G. Transcriptional maps of 10 human chromosomes at 5-nucleotide resolution. Science 2005, 308, 1149-1154.
16. Guttman, M.; Garber, M.; Levin, J.Z.; Donaghey, J.; Robinson, J.; Adiconis, X.; Fan, L.; Koziol, M.J.; Gnirke, A.; Nusbaum, C. Ab initio reconstruction of cell type-specific transcriptomes in mouse reveals the conserved multi-exonic structure of lincRNAs. Nat. Biotechnol. 2010, 28, 503-510.
17. Zhang, X.; Rice, K.; Wang, Y.; Chen, W.; Zhong, Y.; Nakayama, Y.; Zhou, Y.; Klibanski, A. Maternally expressed gene 3 (MEG3) noncoding ribonucleic acid: Isoform structure, expression, and functions. Endocrinology 2010, 151, 939-947.
18. Mercer, T.R.; Dinger, M.E.; Sunkin, S.M.; Mehler, M.F.; Mattick, J.S. Specific expression of long noncoding RNAs in the mouse brain. Proc. Natl. Acad. Sci. USA 2008, 105, 716-721.
19. Carninci, P.; Kasukawa, T.; Katayama, S.; Gough, J.; Frith, M.C.; Maeda, N.; Oyama, R.; Ravasi, T.; Lenhard, B.; Wells, C. The transcriptional landscape of the mammalian genome. Science 2005, 309, 1559-1563.
20. Leygue, E. Steroid receptor RNA activator (SRA1): Unusual bifaceted gene products with suspected relevance to breast cancer. Nucl. Recept. Signal. 2007, 5, e006.
21. Campalans, A.; Kondorosi, A.; Crespi, M. Enod40, a short open reading frame-containing mRNA, induces cytoplasmic localization of a nuclear RNA binding protein in Medicago truncatula. Plant Cell 2004, 16, 1047-1059.
22. Tian, D.; Sun, S.; Lee, J.T. The long noncoding RNA, Jpx, is a molecular switch for X chromosome inactivation. Cell 2010, 143, 390-403.
23. Penny, G.D.; Kay, G.F.; Sheardown, S.A.; Rastan, S.; Brockdorff, N. Requirement for Xist in X chromosome inactivation. Nature 1996, 379, 131-137.
24. Hung, T.; Wang, Y.; Lin, M.F.; Koegel, A.K.; Kotake, Y.; Grant, G.D.; Horlings, H.M.; Shah, N.; Umbricht, C.; Wang, P. Extensive and coordinated transcription of noncoding RNAs within cell-cycle promoters. Nat. Genet. 2011, 43, 621-629.
25. Bonasio, R.; Tu, S.; Reinberg, D. Molecular signals of epigenetic states. Science 2010, 330, 612-616.
26. Spitale, R.C.; Tsai, M.C.; Chang, H.Y. RNA templating the epigenome: Long noncoding RNAs as molecular scaffolds. Epigenetics 2011, 6, 539-543.
27. Collins, K. Physiological assembly and activity of human telomerase complexes. Mech. Ageing Dev. 2008, 129, 91-98.
28. Chen, J.L.; Greider, C.W. Template boundary definition in mammalian telomerase. Genes Dev. 2003, 17, 2747-2752.
29. Zappulla, D.C.; Cech, T.R. Yeast telomerase RNA: A flexible scaffold for protein subunits. Proc. Natl. Acad. Sci. USA 2004, 101, 10024-10029.
30. He, S.; Su, H.; Liu, C.; Skogerbø, G.; He, H.; He, D.; Zhu, X.; Liu, T.; Zhao, Y.; Chen, R. MicroRNA-encoding long non-coding RNAs. BMC Genom. 2008, 9, 236.
31. Wang, K.; Long, B.; Zhou, L.Y.; Liu, F.; Zhou, Q.Y.; Liu, C.Y.; Fan, Y.Y.; Li, P.F. CARL lncRNA inhibits anoxia-induced mitochondrial fission and apoptosis in cardiomyocytes by impairing miR-539-dependent PHB2 downregulation. Nat. Commun. 2014, 5, 3596.
32. Shirasawa, S.; Harada, H.; Furugaki, K.; Akamizu, T.; Ishikawa, N.; Ito, K.; Ito, K.; Tamai, H.; Kuma, K.; Kubota, S. SNPs in the promoter of a B cell-specific antisense transcript, SAS-ZFAT, determine susceptibility to autoimmune thyroid disease. Hum. Mol. Genet. 2004, 13, 2221-2231.
33. Dharap, A.; Pokrzywa, C.; Vemuganti, R. Increased binding of stroke-induced long non-coding RNAs to the transcriptional corepressors Sin3A and coREST. ASN Neuro 2013, 5, 283-289.
34. Schonrock, N.; Harvey, R.P.; Mattick, J.S. Long noncoding RNAs in cardiac development and pathophysiology. Circ. Res. 2012, 111, 1349-1362.
35. Fatima, R.; Akhade, V.S.; Pal, D.; Rao, S.M. Long noncoding RNAs in development and cancer: Potential biomarkers and therapeutic targets. Mol. Cell. Ther. 2015, 3, 5.
36. Pauli, A.; Rinn, J.L.; Schier, A.F. Non-coding RNAs as regulators of embryogenesis. Nat. Rev. Genet. 2011, 12, 136-149.
37. Mohamed, J.S.; Gaughwin, P.M.; Lim, B.; Robson, P.; Lipovich, L. Conserved long noncoding RNAs transcriptionally regulated by Oct4 and Nanog modulate pluripotency in mouse embryonic stem cells. RNA 2010, 16, 324-337.
38. Congrains, A.; Kamide, K.; Oguro, R.; Yasuda, O.; Miyata, K.; Yamamoto, E.; Kawai, T.; Kusunoki, H.; Yamamoto, H.; Takeya, Y. Genetic variants at the 9p21 locus contribute to atherosclerosis through modulation of ANRIL and CDKN2A/B. Atherosclerosis 2012, 220, 449-455.
39. Hu, Y.W.; Yang, J.Y.; Ma, X.; Chen, Z.P.; Hu, Y.R.; Zhao, J.Y.; Li, S.F.; Qiu, Y.R.; Lu, J.B.; Wang, Y.C. A lincRNA-DYNLRB2-2/GPR119/GLP-1R/ABCA1-dependent signal transduction pathway is essential for the regulation of cholesterol homeostasis. J. Lipid Res. 2014, 55, 681-697.
40. Hu, Y.W.; Zhao, J.Y.; Li, S.F.; Huang, J.L.; Qiu, Y.R.; Ma, X.; Wu, S.G.; Chen, Z.P.; Hu, Y.R.; Yang, J.Y. RP5-833A20.1/miR-382-5p/NFIA-dependent signal transduction pathway contributes to the regulation of cholesterol homeostasis and inflammatory reaction. Arterioscler. Thromb. Vasc. Biol. 2015, 35, 87-101.
41. Han, P.; Li, W.; Lin, C.H.; Yang, J.; Shang, C.; Nurnberg, S.T.; Jin, K.K.; Xu, W.; Lin, C.Y.; Lin, C.J.; et al. A long noncoding RNA protects the heart from pathological hypertrophy. Nature 2014, 514, 102-106.
42. Kumarswamy, R.; Bauters, C.; Volkmann, I.; Maury, F.; Fetisch, J.; Holzmann, A.; Lemesle, G.; de Groote, P.; Pinet, F.; Thum, T. Circulating long noncoding RNA, LIPCAR, predicts survival in patients with heart failure. Circ. Res. 2014, 114, 1569-1575.
43. Broadbent, H.M.; Peden, J.F.; Lorkowski, S.; Goel, A.; Ongen, H.; Green, F.; Clarke, R.; Collins, R.; Franzosi, M.G.; Tognoni, G. Susceptibility to coronary artery disease and diabetes is encoded by distinct, tightly linked SNPs in the ANRIL locus on chromosome 9p. Hum. Mol. Genet. 2008, 17, 806-814.
44. Liu, H.; Song, G.; Zhou, L.; Hu, X.; Liu, M.; Nie, J.; Lu, S.; Wu, X.; Cao, Y.; Tao, L. Compared analysis of LncRNA expression profiling in pdk1 gene knockout mice at two time points. Cell. Physiol. Biochem. 2013, 32, 1497-1508.
45. Kurian, L.; Aguirre, A.; Sancho-Martinez, I.; Benner, C.; Hishida, T.; Nguyen, T.B.; Reddy, P.; Nivet, E.; Krause, M.N.; Nelles, D.A. Identification of novel long noncoding RNAs underlying vertebrate cardiovascular development. Circulation 2015, 131, 1278-1290.
46. Grote, P.; Wittler, L.; Hendrix, D.; Koch, F.; Währisch, S.; Beisaw, A.; Macura, K.; Bläss, G.; Kellis, M.; Werber, M. The tissue-specific lncRNA Fendrr is an essential regulator of heart and body wall development in the mouse. Dev. Cell 2013, 24, 206-214.
47. Ishii, N.; Ozaki, K.; Sato, H.; Mizuno, H.; Saito, S.; Takahashi, A.; Miyamoto, Y.; Ikegawa, S.; Kamatani, N.; Hori, M. Identification of a novel non-coding RNA, MIAT, that confers risk of myocardial infarction. J. Hum. Genet. 2006, 51, 1087-1099.
48. Wang, K.; Liu, C.Y.; Zhou, L.Y.; Wang, J.X.; Wang, M.; Zhao, B.; Zhao, W.K.; Xu, S.J.; Fan, L.H.; Zhang, X.J.; et al. APF lncRNA regulates autophagy and myocardial infarction by targeting miR-188-3p. Nat. Commun. 2015, 6, 6779.
49. Zangrando, J.; Zhang, L.; Vausort, M.; Maskali, F.; Marie, P.Y.; Wagner, D.R.; Devaux, Y. Identification of candidate long non-coding RNAs in response to myocardial infarction. BMC Genom. 2014, 15, 460.
50. Bondue, A.; Lapouge, G.; Paulissen, C.; Semeraro, C.; Iacovino, M.; Kyba, M.; Blanpain, C. Mesp1 acts as a master regulator of multipotent cardiovascular progenitor specification. Cell Stem Cell 2008, 3, 69-84.
51. Thum, T.; Condorelli, G. Long noncoding RNAs and microRNAs in cardiovascular pathophysiology. Circ. Res. 2015, 116, 751-762.
52. Mattick, J.S. Challenging the dogma: The hidden layer of non-protein-coding RNAs in complex organisms. Bioessays 2003, 25, 930-939.
53. Wu, C.; Arora, P. Long noncoding Mhrt RNA molecular crowbar unravel insights into heart failure treatment. Circ. Cardiovasc. Genet. 2015, 8, 213-215.
54. Sara, J.D.; Eleid, M.F.; Gulati, R.; Holmes, D.R. Sudden cardiac death from the perspective of coronary artery disease. Mayo Clin. Proc. 2014, 89, 1685-1698.
55. Shemirani, H.; Nayeri-Torshizi, E. Electrocardiographic characteristics of posterior myocardial infarction in comparison to angiographic findings. ARYA Atheroscler. 2015, 11, 30-35.
56. Visscher, P.M.; Brown, M.A.; McCarthy, M.I.; Yang, J. Five years of GWAS discovery. Am. J. Hum. Genet. 2012, 90, 7-24.
57. McPherson, R.; Pertsemlidis, A.; Kavaslar, N.; Stewart, A.; Roberts, R.; Cox, D.R.; Hinds, D.A.; Pennacchio, L.A.; Tybjaerg-Hansen, A.; Folsom, A.R. A common allele on chromosome 9 associated with coronary heart disease. Science 2007, 316, 1488-1491.
58. Yasuno, K.; Bilguvar, K.; Bijlenga, P.; Low, S.K.; Krischek, B.; Auburger, G.; Simon, M.; Krex, D.; Arlier, Z.; Nayak, N. Genome-wide association study of intracranial aneurysm identifies three new risk loci. Nat. Genet. 2010, 42, 420-425.
59. Turnbull, C.; Ahmed, S.; Morrison, J.; Pernet, D.; Renwick, A.; Maranian, M.; Seal, S.; Ghoussaini, M.; Hines, S.; Healey, C.S. Genome-wide association study identifies five new breast cancer susceptibility loci. Nat. Genet. 2010, 42, 504-507.
60. Shete, S.; Hosking, F.J.; Robertson, L.B.; Dobbins, S.E.; Sanson, M.; Malmer, B.; Simon, M.; Marie, Y.; Boisselier, B.; Delattre, J.Y. Genome-wide association study identifies five susceptibility loci for glioma. Nat. Genet. 2009, 41, 899-904.
61. Stacey, S.N.; Sulem, P.; Masson, G.; Gudjonsson, S.A.; Thorleifsson, G.; Jakobsdottir, M.; Sigurdsson, A.; Gudbjartsson, D.F.; Sigurgeirsson, B.; Benediktsdottir, K.R. New common variants affecting susceptibility to basal cell carcinoma. Nat. Genet. 2009, 41, 909-914.
62. Go, A.S.; Mozaffarian, D.; Roger, V.L.; Benjamin, E.J.; Berry, J.D.; Borden, W.B.; Bravata, D.M.; Dai, S.; Ford, E.S.; Fox, C.S. Heart disease and stroke statistics-2013 update: A report from the American Heart Association. Circulation 2013, 127, e6-e245.
63. Groyer, E.; Caligiuri, G.; Laschet-Khallou, J.; Nicoletti, A. Immunological aspects of atherosclerosis. Presse Med. 2006, 35, 475-486.
64. Moore, K.J.; Tabas, I. Macrophages in the pathogenesis of atherosclerosis. Cell 2011, 145, 341-355.
65. Aryal, B.; Rotllan, N.; Fernández-Hernando, C. Noncoding RNAs and atherosclerosis. Curr. Atheroscler. Rep. 2014, 16, 1-11.
66. Heo, K.S.; Le, N.T.; Cushman, H.J.; Giancursio, C.J.; Chang, E.; Woo, C.H.; Sullivan, M.A.; Taunton, J.; Yeh, E.T.H.; Fujiwara, K. Disturbed flow-activated p90RSK kinase accelerates atherosclerosis by inhibiting SENP2 function. J. Clin. Investig. 2015, 125, 1299-1310.
67. Deneen, B.; Ho, R.; Lukaszewicz, A.; Hochstim, C.J.; Gronostajski, R.M.; Anderson, D.J. The transcription factor NFIA controls the onset of gliogenesis in the developing spinal cord. Neuron 2006, 52, 953-968.
68. Gronostajski, R.M. Analysis of nuclear factor I binding to DNA using degenerate oligonucleotides. Nucleic Acids Res. 1986, 14, 9117-9132.
69. Waki, H.; Nakamura, M.; Yamauchi, T.; Wakabayashi, K.I.; Yu, J.; Hirose-Yotsuya, L.; Take, K.; Sun, W.; Iwabu, M.; Okada-Iwabu, M. Global mapping of cell type-specific open chromatin by FAIRE-seq reveals the regulatory role of the NFI family in adipocyte differentiation. PLoS Genet. 2011, 7, e1002311.
70. Ye, D.; Lammers, B.; Zhao, Y.; Meurs, I.; van Berkel, T.J.; van Eck, M. ATP-binding cassette transporters A1 and G1, HDL metabolism, cholesterol efflux, and inflammation: Important targets for the treatment of atherosclerosis. Curr. Drug Targets 2011, 12, 647-660.
71. Callam, M.J. Epidemiology of varicose veins. Br. J. Surg. 1994, 81, 167-173.
72. Li, X.; Jiang, X.Y.; Ge, J.; Wang, J.; Chen, G.J.; Xu, L.; Xie, D.Y.; Yuan, T.Y.; Zhang, D.S.; Zhang, H. Aberrantly expressed lncRNAs in primary varicose great saphenous veins. PLoS ONE 2014, 9, e86156.
73. Li, D.; Chen, G.; Yang, J.; Fan, X.; Gong, Y.; Xu, G.; Cui, Q.; Geng, B. Transcriptome analysis reveals distinct patterns of long noncoding RNAs in heart and plasma of mice with heart failure. PLoS ONE 2013, 8, e77938.