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PMID: 18178218 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Disruption of ROCK1 gene attenuates cardiac dilation and improves contractile function in pathological cardiac hypertrophy.

Journal of molecular and cellular cardiology ·Vol. 44 ·No. 3 ·2008-03-00 ·Pages 551-60

Shi J, Zhang YW, Summers LJ, Dorn GW, Wei L

Abstract

The development of left ventricular cardiomyocyte hypertrophy in response to increased hemodynamic load and neurohormonal stress is initially a compensatory response. However, persistent stress eventually leads to dilated heart failure, which is a common cause of heart failure in human hypertensive and valvular heart disease. We have recently reported that Rho-associated coiled-coil containing protein kinase 1 (ROCK1) homozygous knockout mice exhibited reduced cardiac fibrosis and cardiomyocyte apoptosis, while displaying a preserved compensatory hypertrophic response to pressure overload. In this study, we have tested the effects of ROCK1 deficiency on cardiac hypertrophy, dilation, and dysfunction. We have shown that ROCK1 deletion attenuated left ventricular dilation and contractile dysfunction, but not hypertrophy, in a transgenic model of Galphaq overexpression-induced hypertrophy which represents a well-characterized and highly relevant genetic mouse model of pathological hypertrophy. Although the development of cardiomyocyte hypertrophy was not affected, ROCK1 deletion in Galphaq mice resulted in a concentric hypertrophic phenotype associated with reduced induction of hypertrophic markers indicating that ROCK1 deletion could favorably modify hypertrophy without inhibiting it. Furthermore, ROCK1 deletion also improved contractile response to beta-adrenergic stimulation in Galphaq transgenic mice. Consistent with this observation, ROCK1 deletion prevented down-regulation of type V/VI adenylyl cyclase expression, which is associated with the impaired beta-adrenergic signaling in Galphaq mice. The present study establishes for the first time a role for ROCK1 in cardiac dilation and contractile dysfunction.

MeSH Terms
Adenylyl Cyclases/metabolism Animals Blotting, Western Cardiomegaly/genetics,pathology,physiopathology Dilatation, Pathologic Echocardiography GTP-Binding Protein alpha Subunits, Gq-G11/genetics,physiology Hypertrophy, Left Ventricular/genetics,pathology,physiopathology Isoenzymes/metabolism Mice Mice, Knockout Mice, Transgenic Models, Biological Models, Genetic Muscle Contraction/genetics,physiology rho-Associated Kinases/genetics,physiology
Chemicals
Isoenzymes Rock1 protein, mouse rho-Associated Kinases GTP-Binding Protein alpha Subunits, Gq-G11 Adenylyl Cyclases adenylyl cyclase 6 adenylyl cyclase type V
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Shi Jianjian
Herman B Wells Center for Pediatric Research, Division of Pediatric Cardiology, Department of Pediatrics, Indiana University, School of Medicine, Indianapolis, IN, USA.
Zhang Yi-Wei
Summers Lelia J
Dorn Gerald W
Wei Lei
References (40)
40 references, click to expand
  1. Critical role of Rho-kinase pathway for cardiac performance and remodeling in failing rat hearts.
    Cardiovasc Res. 2002 Sep;55(4):757-67 PMID: 12176125
  2. Decompensation of pressure-overload hypertrophy in G alpha q-overexpressing mice.
    Circulation. 1998 Apr 21;97(15):1488-95 PMID: 9576430
  3. Pharmacological properties of Y-27632, a specific inhibitor of rho-associated kinases.
    Mol Pharmacol. 2000 May;57(5):976-83 PMID: 10779382
  4. Epsilon protein kinase C in pathological myocardial hypertrophy. Analysis by combined transgenic expression of translocation modifiers and Galphaq.
    J Biol Chem. 2000 Sep 29;275(39):29927-30 PMID: 10899155
  5. Cardiomyocyte apoptosis induced by Galphaq signaling is mediated by permeability transition pore formation and activation of the mitochondrial death pathway.
    Circ Res. 2000 Dec 8;87(12):1180-7 PMID: 11110776
  6. RGS4 reduces contractile dysfunction and hypertrophic gene induction in Galpha q overexpressing mice.
    J Mol Cell Cardiol. 2001 Feb;33(2):209-18 PMID: 11162127
  7. Absence of pressure overload induced myocardial hypertrophy after conditional inactivation of Galphaq/Galpha11 in cardiomyocytes.
    Nat Med. 2001 Nov;7(11):1236-40 PMID: 11689889
  8. Rho/ROCK pathway contributes to the activation of extracellular signal-regulated kinase/GATA-4 during myocardial cell hypertrophy.
    J Biol Chem. 2002 Mar 8;277(10):8618-25 PMID: 11739382
  9. MEKK1 is essential for cardiac hypertrophy and dysfunction induced by Gq.
    Proc Natl Acad Sci U S A. 2002 Mar 19;99(6):3866-71 PMID: 11891332
  10. Inhibition of Rho family GTPases by Rho GDP dissociation inhibitor disrupts cardiac morphogenesis and inhibits cardiomyocyte proliferation.
    Development. 2002 Apr;129(7):1705-14 PMID: 11923206
  11. Mitochondrial death protein Nix is induced in cardiac hypertrophy and triggers apoptotic cardiomyopathy.
    Nat Med. 2002 Jul;8(7):725-30 PMID: 12053174
  12. Chronic inhibition of Rho kinase blunts the process of left ventricular hypertrophy leading to cardiac contractile dysfunction in hypertension-induced heart failure.
    J Mol Cell Cardiol. 2003 Jan;35(1):59-70 PMID: 12623300
  13. Phenotyping hypertrophy: eschew obfuscation.
    Circ Res. 2003 Jun 13;92(11):1171-5 PMID: 12805233
  14. Disruption of type 5 adenylyl cyclase gene preserves cardiac function against pressure overload.
    Proc Natl Acad Sci U S A. 2003 Aug 19;100(17):9986-90 PMID: 12904575
  15. 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 Oct 17;93(8):767-75 PMID: 14500337
  16. Protein kinase Calpha negatively regulates systolic and diastolic function in pathological hypertrophy.
    Circ Res. 2003 Nov 28;93(11):1111-9 PMID: 14605019
  17. Protein kinase A in complex with Rho-kinase inhibitors Y-27632, Fasudil, and H-1152P: structural basis of selectivity.
    Structure. 2003 Dec;11(12):1595-607 PMID: 14656443
  18. Inhibition of cardiac myocyte apoptosis improves cardiac function and abolishes mortality in the peripartum cardiomyopathy of Galpha(q) transgenic mice.
    Circulation. 2003 Dec 16;108(24):3036-41 PMID: 14638549
  19. Lysophospholipid signaling in cardiac myocyte hypertrophy.
    J Mol Cell Cardiol. 2004 Apr;36(4):465-8 PMID: 15081306
  20. Enhanced Galphaq signaling: a common pathway mediates cardiac hypertrophy and apoptotic heart failure.
    Proc Natl Acad Sci U S A. 1998 Aug 18;95(17):10140-5 PMID: 9707614
  21. Low- and high-level transgenic expression of beta2-adrenergic receptors differentially affect cardiac hypertrophy and function in Galphaq-overexpressing mice.
    Proc Natl Acad Sci U S A. 1999 May 25;96(11):6400-5 PMID: 10339599
  22. Cardiac-directed adenylyl cyclase expression improves heart function in murine cardiomyopathy.
    Circulation. 1999 Jun 22;99(24):3099-102 PMID: 10377071
  23. The effects of the selective ROCK inhibitor, Y27632, on ET-1-induced hypertrophic response in neonatal rat cardiac myocytes--possible involvement of Rho/ROCK pathway in cardiac muscle cell hypertrophy.
    FEBS Lett. 1999 Jun 11;452(3):314-8 PMID: 10386613
  24. Transgenic replacement of type V adenylyl cyclase identifies a critical mechanism of beta-adrenergic receptor dysfunction in the G alpha q overexpressing mouse.
    FEBS Lett. 1999 Sep 17;458(2):236-40 PMID: 10481072
  25. Protein kinase cascades in the regulation of cardiac hypertrophy.
    J Clin Invest. 2005 Mar;115(3):527-37 PMID: 15765134
  26. Decreased perivascular fibrosis but not cardiac hypertrophy in ROCK1+/- haploinsufficient mice.
    Circulation. 2005 Nov 8;112(19):2959-65 PMID: 16260635
  27. Regulatory properties of adenylate cyclases type 5 and 6: A progress report.
    Eur J Pharmacol. 2006 Mar 27;535(1-3):1-12 PMID: 16527269
  28. Targeted deletion of ROCK1 protects the heart against pressure overload by inhibiting reactive fibrosis.
    FASEB J. 2006 May;20(7):916-25 PMID: 16675849
  29. Increased cardiac adenylyl cyclase expression is associated with increased survival after myocardial infarction.
    Circulation. 2006 Aug 1;114(5):388-96 PMID: 16864723
  30. Activation of Rho-associated coiled-coil protein kinase 1 (ROCK-1) by caspase-3 cleavage plays an essential role in cardiac myocyte apoptosis.
    Proc Natl Acad Sci U S A. 2006 Sep 26;103(39):14495-500 PMID: 16983089
  31. Disruption of type 5 adenylyl cyclase enhances desensitization of cyclic adenosine monophosphate signal and increases Akt signal with chronic catecholamine stress.
    Circulation. 2007 Oct 16;116(16):1776-83 PMID: 17893275
  32. Disruption of Rho signaling results in progressive atrioventricular conduction defects while ventricular function remains preserved.
    FASEB J. 2004 May;18(7):857-9 PMID: 15033930
  33. Long-term inhibition of Rho-kinase suppresses left ventricular remodeling after myocardial infarction in mice.
    Circulation. 2004 May 11;109(18):2234-9 PMID: 15096457
  34. Assessment of cardiomyocyte DNA synthesis in normal and injured adult mouse hearts.
    Am J Physiol. 1997 Jan;272(1 Pt 2):H220-6 PMID: 9038941
  35. The cellular and molecular response of cardiac myocytes to mechanical stress.
    Annu Rev Physiol. 1997;59:551-71 PMID: 9074777
  36. Transgenic Galphaq overexpression induces cardiac contractile failure in mice.
    Proc Natl Acad Sci U S A. 1997 Jul 22;94(15):8121-6 PMID: 9223325
  37. Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension.
    Nature. 1997 Oct 30;389(6654):990-4 PMID: 9353125
  38. The low molecular weight GTPase Rho regulates myofibril formation and organization in neonatal rat ventricular myocytes. Involvement of Rho kinase.
    J Biol Chem. 1998 Mar 27;273(13):7725-30 PMID: 9516480
  39. Targeting the receptor-Gq interface to inhibit in vivo pressure overload myocardial hypertrophy.
    Science. 1998 Apr 24;280(5363):574-7 PMID: 9554846
  40. Mechanisms of impaired beta-adrenergic receptor signaling in G(alphaq)-mediated cardiac hypertrophy and ventricular dysfunction.
    Mol Pharmacol. 2000 Feb;57(2):278-87 PMID: 10648637
Article Info
Journal
Journal of molecular and cellular cardiology
Abbr.
J Mol Cell Cardiol
ISSN
1095-8584
Published
2008-03-00
Epub
2007-00-08
Pages
551-60
Language
English
Region
England
NLM ID
0262322
PMCID
PMC2728597
Subset
IM
Grants
NHLBI NIH HHS · R01 HL072897-04 · United States
NHLBI NIH HHS · R01 HL072897 · United States
NHLBI NIH HHS · P01 HL085098-01A10002 · United States
NHLBI NIH HHS · R01 HL072897-05 · United States
NHLBI NIH HHS · R01 HL059888 · United States
NHLBI NIH HHS · P01 HL085098-01A19001 · United States
NHLBI NIH HHS · P01 HL085098 · United States
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