Crucial role of rho-kinase in pressure overload-induced right ventricular hypertrophy and dysfunction in mice

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 34, Issue 6, 2014, Pages 1260-1271

  Ikeda, Shohei ^a   Satoh, Kimio ^a   Kikuchi, Nobuhiro ^a   Miyata, Satoshi ^a   Suzuki, Kota ^a   Omura, Junichi ^a   Shimizu, Toru ^a   Kobayashi, Kenta ^b   Kobayashi, Kazuto ^b   Fukumoto, Yoshihiro ^a   Sakata, Yasuhiko ^a   Shimokawa, Hiroaki ^a  

^a TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b FUKUSHIMA MEDICAL UNIVERSITY   (Japan)

Author keywords

heart failure, right sided; hypertrophy, right ventricular; oxidative stress; rho associated kinases

Indexed keywords

MEMBRANE PROTEIN; RHO KINASE; ROCK 2 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; AORTA CONSTRICTION; ARTICLE; CONTROLLED STUDY; HEART DISEASE; HEART RIGHT VENTRICLE HYPERTROPHY; HEART RIGHT VENTRICLE OVERLOAD; HEART RIGHT VENTRICULAR DYSFUNCTION; LONG TERM SURVIVAL; MICROARRAY ANALYSIS; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PULMONARY ARTERY OCCLUSION; UPREGULATION;

HEART FAILURE, RIGHT-SIDED; HYPERTROPHY, RIGHT VENTRICULAR; OXIDATIVE STRESS; RHO-ASSOCIATED KINASES;

ANIMALS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FIBROSIS; GATA4 TRANSCRIPTION FACTOR; HYPERTENSION, PULMONARY; HYPERTROPHY, RIGHT VENTRICULAR; MALE; MICE; MICE, INBRED C57BL; OXIDATIVE STRESS; RHO-ASSOCIATED KINASES; SIGNAL TRANSDUCTION; VENTRICULAR DYSFUNCTION, RIGHT;

EID: 84901328508     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.114.303320     Document Type: Article

References (44)

1. Sandoval J, Bauerle O, Palomar A, Gómez A, Martínez-Guerra ML, Beltrán M, Guerrero ML. Survival in primary pulmonary hypertension. Validation of a prognostic equation. Circulation. 1994;89:1733-1744.
2. Bogaard HJ, Abe K, Vonk Noordegraaf A, Voelkel NF. The right ventricle under pressure: cellular and molecular mechanisms of right-heart failure in pulmonary hypertension. Chest. 2009;135:794-804.
3. Verzi MP, McCulley DJ, De Val S, Dodou E, Black BL. The right ventricle, outflow tract, and ventricular septum comprise a restricted expression domain within the secondary/anterior heart field. Dev Biol. 2005;287: 134-145. (Pubitemid 41587484)
4. Walker LA, Buttrick PM. The right ventricle: biologic insights and response to disease. Curr Cardiol Rev. 2009;5:22-28.
5. Greyson CR. Pathophysiology of right ventricular failure. Crit Care Med. 2008;36(1 suppl):S57-S65.
6. Rockman HA, Ross RS, Harris AN, Knowlton KU, Steinhelper ME, Field LJ, Ross J Jr, Chien KR. Segregation of atrial-specific and inducible expression of an atrial natriuretic factor transgene in an In vivo murine model of cardiac hypertrophy. Proc Natl Acad Sci U S A. 1991;88:8277-8281. (Pubitemid 21915339)
7. Urashima T, Zhao M, Wagner R, Fajardo G, Farahani S, Quertermous T, Bernstein D. Molecular and physiological characterization of RV remodeling in a murine model of pulmonary stenosis. Am J Physiol Heart Circ Physiol. 2008;295:H1351-H1368.
8. Chen Y, Guo H, Xu D, Xu X, Wang H, Hu X, Lu Z, Kwak D, Xu Y, Gunther R, Huo Y, Weir EK. Left ventricular failure produces profound lung remodeling and pulmonary hypertension in mice: heart failure causes severe lung disease. Hypertension. 2012;59:1170-1178.
9. Hein S, Arnon E, Kostin S, Schönburg M, Elsässer A, Polyakova V, Bauer EP, Klövekorn WP, Schaper J. Progression from compensated hypertrophy to failure in the pressure-overloaded human heart: structural deterioration and compensatory mechanisms. Circulation. 2003;107:984-991. (Pubitemid 36258721)
10. Heineke J, Molkentin JD. Regulation of cardiac hypertrophy by intracellular signalling pathways. Nat Rev Mol Cell Biol. 2006;7:589-600. (Pubitemid 44325350)
11. Takimoto E, Kass DA. Role of oxidative stress in cardiac hypertrophy and remodeling. Hypertension. 2007;49:241-248. (Pubitemid 46142995)
12. Lassègue B, San Martín A, Griendling KK. Biochemistry, physiology, and pathophysiology of NADPH oxidases in the cardiovascular system. Circ Res. 2012;110:1364-1390.
13. Takano H, Zou Y, Hasegawa H, Akazawa H, Nagai T, Komuro I. Oxidative stress-induced signal transduction pathways in cardiac myocytes: involvement of ROS in heart diseases. Antioxid Redox Signal. 2003;5:789-794. (Pubitemid 37462062)
14. Higashi M, Shimokawa H, Hattori T, Hiroki J, Mukai Y, Morikawa K, Ichiki T, Takahashi S, Takeshita A. Long-term inhibition of Rho-kinase suppresses angiotensin II-induced cardiovascular hypertrophy in rats in vivo: effect on endothelial NAD(P)H oxidase system. Circ Res. 2003;93:767-775. (Pubitemid 37288672)
15. Zhou Q, Gensch C, Liao JK. Rho-associated coiled-coil-forming kinases (ROCKs): potential targets for the treatment of atherosclerosis and vascular disease. Trends Pharmacol Sci. 2011;32:167-173.
16. Brakebusch C, Fässler R. The integrin-actin connection, an eternal love affair. EMBO J. 2003;22:2324-2333. (Pubitemid 36604972)
17. Zhao XH, Laschinger C, Arora P, Szászi K, Kapus A, McCulloch CA. Force activates smooth muscle alpha-actin promoter activity through the Rho signaling pathway. J Cell Sci. 2007;120(Pt 10):1801-1809. (Pubitemid 46930418)
18. Nagai T, Anzai T, Kaneko H, Mano Y, Anzai A, Maekawa Y, Takahashi T, Meguro T, Yoshikawa T, Fukuda K. C-reactive protein overexpression exacerbates pressure overload-induced cardiac remodeling through enhanced inflammatory response. Hypertension. 2011;57:208-215.
19. Patel VB, Wang Z, Fan D, Zhabyeyev P, Basu R, Das SK, Wang W, Desaulniers J, Holland SM, Kassiri Z, Oudit GY. Loss of p47phox subunit enhances susceptibility to biomechanical stress and heart failure because of dysregulation of cortactin and actin filaments. Circ Res. 2013;112:1542-1556.
20. Qipshidze N, Tyagi N, Metreveli N, Lominadze D, Tyagi SC. Autophagy mechanism of right ventricular remodeling in murine model of pulmonary artery constriction. Am J Physiol Heart Circ Physiol. 2012;302:H688-H696.
21. Kehat I, Molkentin JD. Extracellular signal-regulated kinase 1/2 (ERK1/2) signaling in cardiac hypertrophy. Ann N Y Acad Sci. 2010;1188:96-102.
22. Nishida M, Maruyama Y, Tanaka R, Kontani K, Nagao T, Kurose H. Gα(i) and Gα(o) are target proteins of reactive oxygen species. Nature. 2000;408:492-495.
23. Scherz-Shouval R, Elazar Z. Regulation of autophagy by ROS: physiology and pathology. Trends Biochem Sci. 2011;36:30-38.
24. Okamoto R, Li Y, Noma K, Hiroi Y, Liu PY, Taniguchi M, Ito M, Liao JK. FHL2 prevents cardiac hypertrophy in mice with cardiac-specific deletion of ROCK2. FASEB J. 2013;27:1439-1449.
25. Zhang YM, Bo J, Taffet GE, Chang J, Shi J, Reddy AK, Michael LH, Schneider MD, Entman ML, Schwartz RJ, Wei L. Targeted deletion of ROCK1 protects the heart against pressure overload by inhibiting reactive fibrosis. FASEB J. 2006;20:916-925. (Pubitemid 44943949)
26. Brooks WW, Bing OH, Blaustein AS, Allen PD. Comparison of contractile state and myosin isozymes of rat right and left ventricular myocardium. J Mol Cell Cardiol. 1987;19:433-440. (Pubitemid 17087460)
27. Litten RZ, Martin BJ, Buchthal RH, Nagai R, Low RB, Alpert NR. Heterogeneity of myosin isozyme content of rabbit heart. Circ Res. 1985;57:406-414. (Pubitemid 16217983)
28. Takefuji M, Krüger M, Sivaraj KK, Kaibuchi K, Offermanns S, Wettschureck N. RhoGEF12 controls cardiac remodeling by integrating G protein- and integrin-dependent signaling cascades. J Exp Med. 2013;210:665-673.
29. Shi J, Wei L. Rho kinase in the regulation of cell death and survival. Arch Immunol Ther Exp (Warsz). 2007;55:61-75. (Pubitemid 46559196)
30. Thumkeo D, Keel J, Ishizaki T, Hirose M, Nonomura K, Oshima H, Oshima M, Taketo MM, Narumiya S. Targeted disruption of the mouse rho-associated kinase 2 gene results in intrauterine growth retardation and fetal death. Mol Cell Biol. 2003;23:5043-5055. (Pubitemid 36793348)
31. Liang Q, Wiese RJ, Bueno OF, Dai YS, Markham BE, Molkentin JD. The transcription factor GATA4 is activated by extracellular signal-regulated kinase 1- and 2-mediated phosphorylation of serine 105 in cardiomyocytes. Mol Cell Biol. 2001;21:7460-7469. (Pubitemid 32953496)
32. Akazawa H, Komuro I. Roles of cardiac transcription factors in cardiac hypertrophy. Circ Res. 2003;92:1079-1088. (Pubitemid 36665853)
33. Perrino C, Rockman HA. GATA4 and the two sides of gene expression reprogramming. Circ Res. 2006;98:715-716.
34. Suzuki YJ. Cell signaling pathways for the regulation of GATA4 transcription factor: Implications for cell growth and apoptosis. Cell Signal. 2011;23:1094-1099.
35. Yanazume T, Hasegawa K, Wada H, Morimoto T, Abe M, Kawamura T, Sasayama S. Rho/ROCK pathway contributes to the activation of extracellular signal-regulated kinase/GATA-4 during myocardial cell hypertrophy. J Biol Chem. 2002;277:8618-8625. (Pubitemid 34968328)
36. Lawrie A, Spiekerkoetter E, Martinez EC, Ambartsumian N, Sheward WJ, MacLean MR, Harmar AJ, Schmidt AM, Lukanidin E, Rabinovitch M. Interdependent serotonin transporter and receptor pathways regulate S100A4/Mts1, a gene associated with pulmonary vascular disease. Circ Res. 2005;97:227-235. (Pubitemid 41105448)
37. Liu Y, Suzuki YJ, Day RM, Fanburg BL. Rho kinase-induced nuclear translocation of ERK1/ERK2 in smooth muscle cell mitogenesis caused by serotonin. Circ Res. 2004;95:579-586. (Pubitemid 39274372)
38. Nakai A, Yamaguchi O, Takeda T, Higuchi Y, Hikoso S, Taniike M, Omiya S, Mizote I, Matsumura Y, Asahi M, Nishida K, Hori M, Mizushima N, Otsu K. The role of autophagy in cardiomyocytes in the basal state and in response to hemodynamic stress. Nat Med. 2007;13:619-624. (Pubitemid 46828485)
39. Nishida K, Kyoi S, Yamaguchi O, Sadoshima J, Otsu K. The role of autophagy in the heart. Cell Death Differ. 2009;16:31-38.
40. Satoh K, Fukumoto Y, Shimokawa H. Rho-kinase: important new therapeutic target in cardiovascular diseases. Am J Physiol Heart Circ Physiol. 2011;301:H287-H296.
41. Fukumoto Y, Yamada N, Matsubara H, et al. Double-blind, placebo-controlled clinical trial with a rho-kinase inhibitor in pulmonary arterial hypertension. Circ J. 2013;77:2619-2625.
42. Simon MA. Assessment and treatment of right ventricular failure. Nat Rev Cardiol. 2013;10:204-218.
43. Hardziyenka M, Campian ME, Reesink HJ, Surie S, Bouma BJ, Groenink M, Klemens CA, Beekman L, Remme CA, Bresser P, Tan HL. Right ventricular failure following chronic pressure overload is associated with reduction in left ventricular mass: evidence for atrophic remodeling. J Am Coll Cardiol. 2011;57:921-928.
44. Ross J Jr. Acute displacement of the diastolic pressure-volume curve of the left ventricle: role of the pericardium and the right ventricle. Circulation. 1979;59:32-37. (Pubitemid 9082397)