Holding our breath: The emerging and anticipated roles of microRNA in pulmonary hypertension

Pulmonary Circulation

Volumn 2, Issue 3, 2012, Pages 278-290

  White, Kevin ^a   Loscalzo, Joseph ^a   Chan, Stephen Y ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Hypoxia; MicroRNA; Network biology; Pulmonary hypertension

Indexed keywords

EID: 84880758429     PISSN: 20458932     EISSN: 20458940     Source Type: Journal    
DOI: 10.4103/2045-8932.101395     Document Type: Review

References (83)

1. Moss EG, Lee RC, Ambros V. The cold shock domain protein LIN-28 controls developmental timing in C. elegans and is regulated by the lin-4 RNA. Cell 1997;88:637-46.
2. Reinhart BJ, Slack FJ, Basson M, Pasquinelli AE, Bett inger JC, Rougvie AE, et al. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 2000;403:901-6.
3. Chan SY, Loscalzo J. Pathogenic mechanisms of pulmonary arterial hypertension. J Mol Cell Cardiol 2008;44:14-30.
4. Morrell NW, Adnot S, Archer SL, Dupuis J, Jones PL, MacLean MR, et al. Cellular and molecular basis of pulmonary arterial hypertension. J Am Coll Cardiol 2009;54:S20-31.
5. Tuder RM. Pathology of pulmonary arterial hypertension. Semin Respir Crit Care Med 2009;30:376-85.
6. Wu X, Chang M, Mitsialis S, Kourembanas S. Hypoxia regulates bone morphogenetic protein signaling through C-terminal-binding protein 1. Circ Res 2006;99:240-7.
7. Hagen M, Fagan K, Steudel W, Carr M, Lane K, Rodman DM, et al. Interaction of interleukin-6 and the BMP pathway in pulmonary smooth muscle. Am J Physiol Lung Cell Mol Physiol 2007;292:L1473-9.
8. Bartel DP. MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell 2004;116:281-97.
9. Small EM, Olson EN. Pervasive roles of microRNAs in cardiovascular biology. Nature 2011;469:336-42.
10. Esteller M. Non-coding RNAs in human disease. Nat Rev Genet 2011;12:861-74.
11. Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, oft en flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005;120:15-20.
12. Friedman RC, Farh KK, Burge CB, Bartel DP. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 2009;19:92-105.
13. Grimson A, Farh K, Johnston W, Garrett-Engele P, Lim L, Bartel D. MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol Cell 2007;27:91-105.
14. Kiriakidou M, Nelson PT, Kouranov A, Fitziev P, Bouyioukos C, Mourelatos Z, et al. A combined computational-experimental approach predicts human microRNA targets. Genes Dev 2004;18:1165-78.
15. Abdellatif M. Differential expression of microRNAs in different disease states. Circ Res 2012;110:638-50.
16. Morrell NW, Yang X, Upton PD, Jourdan KB, Morgan N, Sheares KK, et al. Altered growth responses of pulmonary artery smooth muscle cells from patients with primary pulmonary hypertension to transforming growth factor-beta(1) and bone morphogenetic proteins. Circulation 2001;104:790-5.
17. Takemoto M, Sun J, Hiroki J, Shimokawa H, Liao J. Rho-kinase mediates hypoxia-induced downregulation of endothelial nitric oxide synthase. Circulation 2002;106:57-62.
18. Eddahibi S, Humbert M, Fadel E, Raffestin B, Darmon M, Capron F, et al. Serotonin transporter overexpression is responsible for pulmonary artery smooth muscle hyperplasia in primary pulmonary hypertension. J Clin Invest 2001;108:1141-50.
19. Li X, Zhang X, Leathers R, Makino A, Huang C, Parsa P, et al. Notch3 signaling promotes the development of pulmonary arterial hypertension. Nat Med 2009;15:1289-97.
20. Cohen AH, Hanson K, Morris K, Fouty B, McMurty IF, Clarke W, et al. Inhibition of cyclic 3’-5’-guanosine monophosphate-specific phosphodiesterase selectively vasodilates the pulmonary circulation in chronically hypoxic rats. J Clin Invest 1996;97:172-9.
21. Giaid A, Yanagisawa M, Langleben D, Michel RP, Levy R, Shennib H, et al. Expression of endothelin-1 in the lungs of patients with pulmonary hypertension. N Engl J Med 1993;328:1732-9.
22. Sullivan CC, Du L, Chu D, Cho AJ, Kido M, Wolf PL, et al. Induction of pulmonary hypertension by an angiopoietin 1/TIE2/serotonin pathway. Proc Natl Acad Sci, USA 2003;100:12331-6.
23. Parikh VN, Chan SY. Inflammatory Mechanisms in Pulmonary hypertension. In: Wang YX, editor. Recent Advances in Pulmonary Vascular Biology. Kerala, India: Research Signpost; 2012.
24. Chan SY, Loscalzo J. MicroRNA-210: A unique and pleiotropic hypoxamir. Cell Cycle 2010;9:107-83.
25. Kulshreshtha R, Ferracin M, Wojcik SE, Garzon R, Alder H, Agosto-Perez FJ, et al. A microRNA signature of hypoxia. Mol Cell Biol 2007;27:1859-67.
26. Taganov K, Boldin M, Chang K, Baltimore D. NF-kappaB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc Natl Acad Sci U S A 2006;103:12481-6.
27. Sun X, Icli B, Wara AK, Belkin N, He S, Kobzik L, et al. MicroRNA-181b regulates NF-kappaB-mediated vascular inflammation. J Clin Invest 2012;122:1973-90.
28. Ghosh G, Subramanian IV, Adhikari N, Zhang X, Joshi HP, Basi D, et al. Hypoxia-induced microRNA-424 expression in human endothelial cells regulates HIF-alpha isoforms and promotes angiogenesis. J Clin Invest 2010;120:4141-54.
29. Hu S, Huang M, Li Z, Jia F, Ghosh Z, Lij kwan MA, et al. MicroRNA-210 as a novel therapy for treatment of ischemic heart disease. Circulation 2010;122:S124-31.
30. Biswas S, Roy S, Banerjee J, Hussain SR, Khanna S, Meenakshisundaram G, et al. Hypoxia inducible microRNA 210 attenuates keratinocyte proliferation and impairs closure in a murine model of ischemic wounds. Proc Natl Acad Sci U S A 2010;107:6976-81.
31. Huang X, Ding L, Bennewith KL, Tong RT, Welford SM, Ang KK, et al. Hypoxia-inducible mir-210 regulates normoxic gene expression involved in tumor initiation. Mol Cell 2009;35:856-67.
32. Chan SY, Zhang YY, Hemann C, Mahoney CE, Zweier JL, Loscalzo J. MicroRNA-210 controls mitochondrial metabolism during hypoxia by repressing the iron-sulfur cluster assembly proteins ISCU1/2. Cell Metab 2009;10:273-84.
33. Tuder RM, Davis LA, Graham BB. Targeting energetic metabolism: a new frontier in the pathogenesis and treatment of pulmonary hypertension. Am J Respir Crit Care Med 2011;185:260-6.
34. Davis BN, Hilyard AC, Lagna G, Hata A. SMAD proteins control DROSHA-mediated microRNA maturation. Nature 2008;454:56-61.
35. Drake KM, Zygmunt D, Mavrakis L, Harbor P, Wang L, Comhair SA, et al. Altered microRNA Processing in Heritable Pulmonary Arterial Hypertension: an Important Role for Smad-8. Am J Respir Crit Care Med 2011;184:1400-8.
36. Mendell JT. miRiad roles for the miR-17-92 cluster in development and disease. Cell 2008;133:217-22.
37. Bonauer A, Carmona G, Iwasaki M, Mione M, Koyanagi M, Fischer A, et al. MicroRNA-92a controls angiogenesis and functional recovery of ischemic tissues in mice. Science 2009;324:1710-3.
38. Brock M, Trenkmann M, Gay RE, Michel BA, Gay S, Fischler M, et al. Interleukin-6 modulates the expression of the bone morphogenic protein receptor type II through a novel STAT3-microRNA cluster 17/92 pathway. Circ Res 2009;104:1184-91.
39. Caruso P, MacLean MR, Khanin R, McClure J, Soon E, Southgate M, et al. Dynamic changes in lung microRNA profiles during the development of pulmonary hypertension due to chronic hypoxia and monocrotaline. Arterioscler Thromb Vasc Biol 2010;30:716-23.
40. Yang S, Banerjee S, Freitas AD, Cui H, Xie N, Abraham E, et al. miR-21 regulates chronic hypoxia-induced pulmonary vascular remodeling. Am J Physiol Lung Cell Mol Physiol 2012;302:L521-2s9.
41. Bockmeyer CL, Maegel L, Janciauskiene S, Rische J, Lehmann U, Maus UA, et al. Plexiform vasculopathy of severe pulmonary arterial hypertension and microRNA expression. J Heart Lung Transplant 2012;31:764-72.
42. Courboulin A, Paulin R, Giguère NJ, Saksouk N, Perreault T, Meloche J, et al. Role for miR-204 in human pulmonary arterial hypertension. J Exp Med 2011;208:535-48.
43. Lee Y, Yang X, Huang Y, Fan H, Zhang Q, Wu Y, et al. Network modeling identifies molecular functions targeted by miR-204 to suppress head and neck tumor metastasis. PLoS Comput Biol 2010;6:e1000730.
44. Wang FE, Zhang C, Maminishkis A, Dong L, Zhi C, Li R, et al. MicroRNA-204/211 alters epithelial physiology. FASEB J 2010;24:1552-71.
45. Ryan J, Bloch K, Archer SL. Rodent models of pulmonary hypertension: Harmonisation with the world health organisation’s categorisation of human PH. Int J Clin Pract Suppl 2011;172:15-34.
46. Barabasi AL, Gulbahce N, Loscalzo J. Network medicine: A network-based approach to human disease. Nat Rev Genet 2011;12:56-68.
47. Chan SY, White K, Loscalzo J. Deciphering the molecular basis of human cardiovascular disease through network biology. Curr Opin Cardiol 2012;27:202-9.
48. van Rooij E, Sutherland LB, Thatcher JE, DiMaio JM, Naseem RH, Marshall WS, et al. Dysregulation of microRNAs aft er myocardial infarction reveals a role of miR-29 in cardiac fibrosis. Proc Natl Acad Sci U S A 2008;105: 13027-32.
49. Shirdel EA, Xie W, Mak TW, Jurisica I. NAViGaTing the micronome--using multiple microRNA prediction databases to identify signalling pathway-associated microRNAs. PLoS One 2011;6:e17429.
50. Gennarino VA, D’Angelo G, Dharmalingam G, Fernandez S, Russolillo G, Sanges R, et al. Identification of microRNA-regulated gene networks by expression analysis of target genes. Genome Res 2012;22:1163-72.
51. Rual JF, Venkatesan K, Hao T, Hirozane-Kishikawa T, Dricot A, Li N, et al. Towards a proteome-scale map of the human protein-protein interaction network. Nature 2005;437:1173-8.
52. Stelzl U, Worm U, Lalowski M, Haenig C, Brembeck FH, Goehler H, et al. A human protein-protein interaction network: a resource for annotating the proteome. Cell 2005;122:957-68.
53. Cusick ME, Yu H, Smolyar A, Venkatesan K, Carvunis AR, Simonis N, et al. Literature-curated protein interaction datasets. Nat Methods 2009;6:39-46.
54. Aranda B, Achuthan P, Alam-Faruque Y, Armean I, Bridge A, Derow C, et al. The IntAct molecular interaction database in 2010. Nucleic Acids Res 2010;38:D525-31.
55. Ceol A, Chatr Aryamontri A, Licata L, Peluso D, Briganti L, Perfett o L, et al. MINT, the molecular interaction database: 2009 update. Nucleic Acids Res 2009;38:D532-9.
56. Wingender E, Chen X, Fricke E, Geffers R, Hehl R, Liebich I, et al. The TRANSFAC system on gene expression regulation. Nucleic Acids Res 2001;29:281-3.
57. Diella F, Gould CM, Chica C, Via A, Gibson TJ. Phospho.ELM: A database of phosphorylation sites—update 2008. Nucleic Acids Res 2008;36:D240-4.
58. Hornbeck PV, Chabra I, Kornhauser JM, Skrzypek E, Zhang B. PhosphoSite: A bioinformatics resource dedicated to physiological protein phosphorylation. Proteomics 2004;4:1551-61.
59. Hong KH, Lee YJ, Lee E, Park SO, Han C, Beppu H, et al. Genetic ablation of the BMPR2 gene in pulmonary endothelium is sufficient to predispose to pulmonary arterial hypertension. Circulation 2008;118:722-30.
60. Pullamsett i SS, Doebele C, Fischer A, Savai R, Kojonazarov B, Dahal BK, et al. Inhibition of microRNA-17 improves lung and heart function in experimental pulmonary hypertension. Am J Respir Crit Care Med 2011;185:409-19.
61. Joshi SR, Abe K, Oka M, McMurtry IF, Gerthoffer WT. Mir-145 in vascular smooth muscle phenotype in pulmonary arterial hypertension. Am J Respir Crit Care Med 2011;183:A3448.
62. Ji R, Cheng Y, Yue J, Yang J, Liu X, Chen H, et al. MicroRNA expression signature and antisense-mediated depletion reveal an essential role of MicroRNA in vascular neointimal lesion formation. Circ Res 2007;100:1579-88.
63. Sarkar J, Gou D, Turaka P, Viktorova E, Ramchandran R, Raj JU. MicroRNA-21 plays a role in hypoxia-mediated pulmonary artery smooth muscle cell proliferation and migration. Am J Physiol Lung Cell Mol Physiol 2010;299:L861-71.
64. Krichevsky AM, Gabriely G. miR-21: a small multi-faceted RNA. J Cell Mol Med 2009;13:39-53.
65. Thum T, Gross C, Fiedler J, Fischer T, Kissler S, Bussen M, et al. MicroRNA-21 contributes to myocardial disease by stimulating MAP kinase signalling in fibroblasts. Nature 2008;456:980-4.
66. Maegdefessel L, Azuma J, Toh R, Deng A, Merk DR, Raiesdana A, et al. MicroRNA-21 blocks abdominal aortic aneurysm development and nicotine-augmented expansion. Sci Transl Med 2012;4:122ra22.
67. Gorospe M, Tominaga K, Wu X, Fahling M, Ivan M. Post-transcriptional control of the hypoxic response by RNA-binding proteins and microRNAs. Front Mol Neurosci 2011;4:7.
68. Löffler D, Brocke-Heidrich K, Pfeifer G, Stocsits C, Hackermüller J, Kretzschmar AK, et al. Interleukin-6 dependent survival of multiple myeloma cells involves the Stat3-mediated induction of microRNA-21 through a highly conserved enhancer. Blood 2007;110:1330-3.
69. Iliopoulos D, Jaeger SA, Hirsch HA, Bulyk ML, Struhl K. STAT3 activation of miR-21 and miR-181b-1 via PTEN and CYLD are part of the epigenetic switch linking inflammation to cancer. Mol Cell 2010;39:493-506.
70. Wojciak-Stothard B, Zhao L, Oliver E, Dubois O, Wu Y, Kardassis D, et al. Role of RhoB in the regulation of pulmonary endothelial and smooth muscle cell responses to hypoxia. Circ Res 2012;110:1423-34.
71. Patrick DM, Montgomery RL, Qi X, Obad S, Kauppinen S, Hill JA, et al. Stress-dependent cardiac remodeling occurs in the absence of microRNA-21 in mice. J Clin Invest 2010;120:3912-6.
72. Kang H, Davis-Dusenbery BN, Nguyen PH, Lal A, Lieberman J, Van Aelst L, et al. Bone morphogenetic protein 4 promotes vascular smooth muscle contractility by activating microRNA-21 (miR-21), which down-regulates expression of family of dedicator of cytokinesis (DOCK) proteins. J Biol Chem 2012;287:3976-86.
73. Thum T, Chau N, Bhat B, Gupta SK, Linsley PS, Bauersachs J, et al. Comparison of different miR-21 inhibitor chemistries in a cardiac disease model. J Clin Invest 2011;121:461-2.
74. Morrisey EE. The magic and mystery of miR-21. J Clin Invest 2010;120:3817-9.
75. Parikh VN, Jin RC, Rabello S, Gulbahce N, White K, Hale A, et al. MicroRNA-21 Integrates pathogenic signaling to control pulmonary hypertension: Results of a network bioinformatics approach. Circulation 2012;125:1520-32.
76. Prosser HM, Koike-Yusa H, Cooper JD, Law FC, Bradley A. A resource of vectors and ES cells for targeted deletion of microRNAs in mice. Nat Biotechnol 2011;29:840-5.
77. Zhang Y, Liu D, Chen X, Li J, Li L, Bian Z, et al. Secreted monocytic miR-150 enhances targeted endothelial cell migration. Mol Cell 2010;39:133-44.
78. Pegtel DM, Cosmopoulos K, Thorley-Lawson DA, et al. Functional delivery of viral miRNAs via exosomes. Proc Natl Acad Sci U S A 2010;107:6328-33.
79. Vickers KC, Palmisano BT, Shoucri BM, Shamburek RD, Remaley AT. MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat Cell Biol 2011;13:423-33.
80. Mitt elbrunn M, Gutiérrez-Vázquez C, Villarroya-Beltri C, González S, Sánchez-Cabo F, González MÁ, et al. Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells. Nat Commun 2011;2:282.
81. Hergenreider E, Heydt S, Tréguer K, Boett ger T, Horrevoets AJ, Zeiher AM, et al. Atheroprotective communication between endothelial cells and smooth muscle cells through miRNAs. Nat Cell Biol 2012;14:249-56.
82. van Rooij E, Olson E. MicroRNAs: Powerful new regulators of heart disease and provocative therapeutic targets. J Clin Investig 2007;117 2369-76.
83. Urbich C, Kuehbacher A, Dimmeler S. Role of microRNAs in vascular diseases, inflammation, and angiogenesis. Cardiovasc Res 2008;79:581-8.