A role for miR-145 in pulmonary arterial hypertension: Evidence from mouse models and patient samples

Circulation Research

Volumn 111, Issue 3, 2012, Pages 290-300

  Caruso, Paola ^a,b   Dempsie, Yvonne ^a   Stevens, Hannah C ^a   McDonald, Robert A ^a   Long, Lu ^a,b   Lu, Ruifang ^a   White, Kevin ^a   Mair, Kirsty M ^a   McClure, John D ^a   Southwood, Mark ^a,b   Upton, Paul ^a,b   Xin, Mei ^a,c   Van Rooij, Eva ^a,d   Olson, Eric N ^a,c   Morrell, Nicholas W ^a,b   MacLean, Margaret R ^a   Baker, Andrew H ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF TEXAS AT DALLAS   (United States)

^d MiRagen Therapeutics   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN 2; MICRORNA 145;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; HEART RIGHT VENTRICLE PRESSURE; HYPOXIA; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PULMONARY ARTERY; PULMONARY HYPERTENSION; QUANTITATIVE ANALYSIS;

ANIMALS; DISEASE MODELS, ANIMAL; DOWN-REGULATION; FEMALE; GENE KNOCK-IN TECHNIQUES; HUMANS; HYPERTENSION, PULMONARY; LUNG; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; MICRORNAS;

EID: 84864229176     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.112.267591     Document Type: Article

References (36)

1. Rich S, Dantzker DR, Ayres SM, Bergofsky EH, Brundage BH, Detre KM, Fishman AP, Goldring RM, Groves BM, Koerner SK. Primary pulmonary hypertension: a national prospective study. Ann Intern Med. 1987;107:216-223. (Pubitemid 17137857)
2. Jeffery TK, Morrell NW. Molecular and cellular basis of pulmonary vascular remodeling in pulmonary hypertension. Prog Cardiovasc Dis. 2002;45:173-202. (Pubitemid 36139815)
3. Eddahibi S, Morrell N, dâOrtho MP, Naeije R, Adnot S. Pathobiology of pulmonary arterial hypertension. Eur Respir J. 2002;20:1559-1572. (Pubitemid 35460627)
4. Morrell NW, Yang X, Upton PD, Jourdan KB, Morgan N, Sheares KK, Trembath RC. 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; 104:790-795. (Pubitemid 32762677)
5. Yang X, Long L, Southwood M, Rudarakanchana N, Upton PD, Jeffery TK, Atkinson C, Chen H, Trembath RC, Morrell NW. Dysfunctional Smad signaling contributes to abnormal smooth muscle cell proliferation in familial pulmonary arterial hypertension. Circ Res. 2005;96: 1053-1063. (Pubitemid 40791377)
6. Teichert-Kuliszewska K, Kutryk MJ, Kuliszewski MA, Karoubi G, Courtman DW, Zucco L, Granton J, Stewart DJ. Bone morphogenetic protein receptor-2 signaling promotes pulmonary arterial endothelial cell survival: implications for loss-of-function mutations in the pathogenesis of pulmonary hypertension. Circ Res. 2006;98:209-217.
7. Mandegar M, Fung YC, Huang W, Remillard CV, Rubin LJ, Yuan JX. Cellular and molecular mechanisms of pulmonary vascular remodeling: role in the development of pulmonary hypertension. Microvasc Res. 2004;68:75-103. (Pubitemid 39093882)
8. Ambros V. The functions of animal microRNAs. Nature. 2004;431: 350-355. (Pubitemid 39265675)
9. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell. 2009;136:215-233.
10. Guo H, Ingolia NT, Weissman JS, Bartel DP. Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature. 2010;466: 835-840.
11. Kartha RV, Subramanian S. MicroRNAs in cardiovascular diseases: biology and potential clinical applications. J Cardiovasc Transl Res. 2010;3:256-270.
12. Urbich C, Kuehbacher A, Dimmeler S. Role of microRNAs in vascular diseases, inflammation, and angiogenesis. Cardiovasc Res. 2008;79: 581-588.
13. Cheng Y, Liu X, Yang J, Lin Y, Xu DZ, Lu Q, Deitch EA, Huo Y, Delphin ES, Zhang C. MicroRNA-145, a novel smooth muscle cell phenotypic marker and modulator, controls vascular neointimal lesion formation. Circ Res. 2009;105:158-166.
14. Iio A, Nakagawa Y, Hirata I, Naoe T, Akao Y. Identification of noncoding RNAs embracing microRNA-143/145 cluster. Mol Cancer. 2010; 9:136.
15. Xin M, Small EM, Sutherland LB, Qi X, McAnally J, Plato CF, Richardson JA, Bassel-Duby R, Olson EN. MicroRNAs miR-143 and miR-145 modulate cytoskeletal dynamics and responsiveness of smooth muscle cells to injury. Genes Dev. 2009;23:2166-2178.
16. Elia L, Quintavalle M, Zhang J, Contu R, Cossu L, Latronico MV, Peterson KL, Indolfi C, Catalucci D, Chen J, Courtneidge SA, Condorelli G. The knockout of miR-143 and -145 alters smooth muscle cell maintenance and vascular homeostasis in mice: correlates with human disease. Cell Death Differ. 2009;16:1590-1598.
17. Davis-Dusenbery BN, Chan MC, Reno KE, Weisman AS, Layne MD, Lagna G, Hata A. downregulation of Kruppel-like factor-4 (KLF4) by microRNA-143/145 is critical for modulation of vascular smooth muscle cell phenotype by transforming growth factor-beta and bone morphogenetic protein 4. J Biol Chem. 2011;286:28097-28110.
18. Long X, Miano JM. Transforming growth factor-beta1 (TGF-beta1) utilizes distinct pathways for the transcriptional activation of microRNA 143/145 in human coronary artery smooth muscle cells. J Biol Chem. 2011;286:30119-30129.
19. McDonald RA, Hata A, MacLean M, Morrell NW, Baker AH. MicroRNA and vascular remodelling in acute vascular injury and pulmonary vascular remodelling Cardiovasc Res. 2011;93:594-604.
20. Caruso P, MacLean MR, Khanin R, McClure J, Soon E, Southgate M, MacDonald RA, Greig JA, Robertson KE, Masson R, Denby L, Dempsie Y, Long L, Morrell NW, Baker AH. Dynamic changes in lung microRNA profiles during the development of pulmonary hypertension due to chronic hypoxia and monocrotaline. Arterioscler Thromb Vasc Biol. 2010;30:716-723.
21. West J, Harral J, Lane K, Deng Y, Ickes B, Crona D, Albu S, Stewart D, Fagan K. Mice expressing BMPR2R899X transgene in smooth muscle develop pulmonary vascular lesions. Am J Physiol Lung Cell Mol Physiol. 2008;295:L744-755.
22. Boettger T, Beetz N, Kostin S, Schneider J, Kruger M, Hein L, Braun T. Acquisition of the contractile phenotype by murine arterial smooth muscle cells depends on the Mir143/145 gene cluster. J Clin Invest. 2009;119:2634-2647.
23. Kano M, Seki N, Kikkawa N, Fujimura L, Hoshino I, Akutsu Y, Chiyomaru T, Enokida H, Nakagawa M, Matsubara H. miR-145, miR-133a and miR-133b: tumor-suppressive miRNAs target FSCN1 in esophageal squamous cell carcinoma. Int J Cancer. 2010;127:2804-2814.
24. Xu N, Papagiannakopoulos T, Pan G, Thomson JA, Kosik KS. MicroRNA-145 regulates OCT4, SOX2, and KLF4 and represses pluripotency in human embryonic stem cells. Cell. 2009;137:647-658.
25. Quintavalle M, Elia L, Condorelli G, Courtneidge SA. J Cell Biol. 2010;189:13-22.
26. Cordes KR, Sheehy NT, White MP, Berry EC, Morton SU, Muth AN, Lee TH, Miano JM, Ivey KN, Srivastava D. miR-145 and miR-143 regulate smooth muscle cell fate and plasticity. Nature. 2009;460: 705-710.
27. Hergenreider E, Heydt S, Treguer K, Boettger T, Horrevoets AJG, Zeiher AM, Scheffer MP, Frangakis AS, Yin Z, Mayr M, Braun T, Urbich C, Boon RA, Dimmeler S. Atheroprotective communication between endothelial cells and smooth muscle cells through miRNAs. Nat Cell Biol. 2012;14:249-256.
28. Davis BN, Hilyard AC, Lagna G, Hata A. SMAD proteins control DROSHA-mediated microRNA maturation. Nature. 2008;454:56-61. (Pubitemid 351931982)
29. Courboulin A, Paulin R, Giguere NJ, Saksouk N, Perreault T, Meloche J, Paquet ER, Biardel S, Provencher S, Cote J, Simard MJ, Bonnet S. Role for miR-204 in human pulmonary arterial hypertension. J Exp Med. 2011;208:535-548.
30. Mayorga ME, Penn MS. miR-145 is differentially regulated by TGFbeta1 and ischemia and targets disabled-2 expression and wnt/beta-catenin activity. J Cell Mol Med. 2012;16:1106-1113.
31. Leyns L, Bouwmeester T, Kim SH, Piccolo S, De Robertis EM. Frzb-1 is a secreted antagonist of Wnt signaling expressed in the Spemann organizer. Cell. 1997;88:747-756. (Pubitemid 27164263)
32. Hsieh JC, Kodjabachian L, Rebbert ML, Rattner A, Smallwood PM, Samos CH, Nusse R, Dawid IB, Nathans J. A new secreted protein that binds to Wnt proteins and inhibits their activities. Nature. 1999;398: 431-436. (Pubitemid 29180376)
33. Jiang Y, Luo W, Howe PH. Dab2 stabilizes Axin and attenuates Wnt/ beta-catenin signaling by preventing protein phosphatase 1 (PP1)-Axin interactions. Oncogene. 2009;28:2999-3007.
34. Baldin V, Lukas J, Marcote MJ, Pagano M, Draetta G. Cyclin D1 is a nuclear protein required for cell cycle progression in G1. Genes Dev. 1993;7:812-821. (Pubitemid 23163585)
35. Baranwal S, Alahari SK. Molecular mechanisms controlling E-cadherin expression in breast cancer. Biochem Biophys Res Commun. 2009; 384:6-11.
36. Cohen ED, Ihida-Stansbury K, Lu MM, Panettieri RA, Jones PL, Morrisey EE. Wnt signaling regulates smooth muscle precursor development in the mouse lung via a tenascin C/PDGFR pathway. J Clin Invest. 2009;119:2538-2549.