Journal of Molecular and Cellular Cardiology
Volume 47, Issue 6 , Pages 810-818 , December 2009

Nitric oxide inhibits endothelin-1-induced neonatal cardiomyocyte hypertrophy via a RhoA-ROCK-dependent pathway

Received 27 May 2009 ,Revised 16 September 2009 ,Accepted 18 September 2009.

References 

  1. American Heart Association. 2008 Heart and Stroke Statistical Update. Dallas, TX: American Heart Association; 2008;
  2. Kuwahara K, Saito Y, Nakagawa O, Kishimoto I, Harada M, Ogawa E, et al. 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;452:314–318
  3. Murthy KS, Zhou H, Grider JR, Makhlouf GM. Inhibition of sustained smooth muscle contraction by PKA and PKG preferentially mediated by phosphorylation of RhoA. Am. J. Physiol., Gastrointest. Liver Physiol. 2003;284:G1006–G1016
  4. Sauzeau V, Le JH, Cario-Toumaniantz C, Smolenski A, Lohmann SM, Bertoglio J, et al. Cyclic GMP-dependent protein kinase signaling pathway inhibits RhoA-induced Ca2+ sensitization of contraction in vascular smooth muscle. J. Biol. Chem. 2000;275:21722–21729
  5. Hamid SA, Bower HS, Baxter GF. Rho kinase activation plays a major role as a mediator of irreversible injury in reperfused myocardium. Am. J. Physiol. Heart Circ. Physiol. 2007;292:H2598–H2606
  6. Zeidan A, Javadov S, Karmazyn M. Essential role of Rho/ROCK-dependent processes and actin dynamics in mediating leptin-induced hypertrophy in rat neonatal ventricular myocytes. Cardiovasc. Res. 2006;72:101–111
  7. Phrommintikul A, Tran L, Kompa A, Wang B, Adrahtas A, Cantwell D, et al. Effects of a Rho kinase inhibitor on pressure overload induced cardiac hypertrophy and associated diastolic dysfunction. Am. J. Physiol. Heart. Circ. Physiol. 2008;294:H1804–H1814
  8. Aoki H, Izumo S, Sadoshima J. Angiotensin II activates RhoA in cardiac myocytes: a critical role of RhoA in angiotensin II-induced premyofibril formation. Circ. Res. 1998;82:666–676
  9. Aikawa R, Komuro I, Nagai R, Yazaki Y. Rho plays an important role in angiotensin II-induced hypertrophic responses in cardiac myocytes. Mol. Cell. Biochem. 2000;212:177–182
  10. Pan J, Singh US, Takahashi T, Oka Y, Palm-Leis A, Herbelin BS, et al. PKC mediates cyclic stretch-induced cardiac hypertrophy through Rho family GTPases and mitogen-activated protein kinases in cardiomyocytes. J. Cell. Physiol. 2005;202:536–553
  11. Zeidan A, Javadov S, Chakrabarti S, Karmazyn M. Leptin-induced cardiomyocyte hypertrophy involves selective caveolae and RhoA/ROCK-dependent p38 MAPK translocation to nuclei. Cardiovasc. Res. 2008;77:64–72
  12. Kuwahara K, Teg Pipes GC, McAnally J, Richardson JA, Hill JA, Bassel-Duby R, et al. Modulation of adverse cardiac remodeling by STARS, a mediator of MEF2 signaling and SRF activity. J. Clin. Invest. 2007;117:1324–1334
  13. Massion PB, Pelat M, Belge C, Balligand JL. Regulation of the mammalian heart function by nitric oxide. Comp. Biochem. Physiol., A Mol. Integr. Physiol. 2005;142:144–150
  14. Saraiva RM, Hare JM. Nitric oxide signaling in the cardiovascular system: implications for heart failure. Curr. Opin. Cardiol. 2006;21:221–228
  15. Scherrer-Crosbie M, Ullrich R, Bloch KD, Nakajima H, Nasseri B, Aretz HT, et al. Endothelial nitric oxide synthase limits left ventricular remodeling after myocardial infarction in mice. Circulation. 2001;104:1286–1291
  16. Janssens S, Pokreisz P, Schoonjans L, Pellens M, Vermeersch P, Tjwa M, et al. Cardiomyocyte-specific overexpression of nitric oxide synthase 3 improves left ventricular performance and reduces compensatory hypertrophy after myocardial infarction. Circ. Res. 2004;94:1256–1262
  17. Buys ES, Raher MJ, Blake SL, Neilan TG, Graveline AR, Passeri JJ, et al. Cardiomyocyte-restricted restoration of nitric oxide synthase 3 attenuates left ventricular remodeling after chronic pressure overload. Am. J. Physiol., Heart Circ. Physiol. 2007;293:H620–H627
  18. Feng Q, Lu X, Jones DL, Shen J, Arnold JM. Increased inducible nitric oxide synthase expression contributes to myocardial dysfunction and higher mortality after myocardial infarction in mice. Circulation. 2001;104:700–704
  19. Calderone A, Thaik CM, Takahashi N, Chang DL, Colucci WS. Nitric oxide, atrial natriuretic peptide, and cyclic GMP inhibit the growth-promoting effects of norepinephrine in cardiac myocytes and fibroblasts. J. Clin. Invest. 1998;101:812–818
  20. Hassan MA, Ketat AF. Sildenafil citrate increases myocardial cGMP content in rat heart, decreases its hypertrophic response to isoproterenol and decreases myocardial leak of creatine kinase and troponin T. BMC Pharmacol. 2005;5:10
  21. Takimoto E, Champion HC, Li M, Belardi D, Ren S, Rodriguez ER, et al. Chronic inhibition of cyclic GMP phosphodiesterase 5A prevents and reverses cardiac hypertrophy. Nat. Med. 2005;11:214–222
  22. Sawada N, Itoh H, Yamashita J, Doi K, Inoue M, Masatsugu K, et al. cGMP-dependent protein kinase phosphorylates and inactivates RhoA. Biochem. Biophys. Res. Commun. 2001;280:798–805
  23. Rajapurohitam V, Javadov S, Purdham DM, Kirshenbaum LA, Karmazyn M. An autocrine role for leptin in mediating the cardiomyocyte hypertrophic effects of angiotensin II and endothelin-1. J. Mol. Cell. Cardiol. 2006;41:265–274
  24. Ellerbroek SM, Wennerberg K, Burridge K. Serine phosphorylation negatively regulates RhoA in vivo. J. Biol. Chem. 2003;278:19023–19031
  25. Forget MA, Desrosiers RR, Gingras D, Beliveau R. Phosphorylation states of Cdc42 and RhoA regulate their interactions with Rho GDP dissociation inhibitor and their extraction from biological membranes. Biochem. J. 2002;361:243–254
  26. Brown JH, Del Re DP, Sussman MA. The Rac and Rho hall of fame: a decade of hypertrophic signaling hits. Circ. Res. 2006;98:730–742
  27. Matsuoka H, Nakata M, Kohno K, Koga Y, Nomura G, Toshima H, et al. Chronic l-arginine administration attenuates cardiac hypertrophy in spontaneously hypertensive rats. Hypertension. 1996;27:14–18
  28. Singh RJ, Hogg N, Joseph J, Kalyanaraman B. Mechanism of nitric oxide release from S-nitrosothiols. J. Biol. Chem. 1996;271:18596–18603
  29. Saraiva RM, Minhas KM, Raju SV, Barouch LA, Pitz E, Schuleri KH, et al. Deficiency of neuronal nitric oxide synthase increases mortality and cardiac remodeling after myocardial infarction: role of nitroso-redox equilibrium. Circulation. 2005;112:3415–3422
  30. Flaherty MP, Brown M, Grupp IL, Schultz JE, Murphree SS, Jones WK. eNOS deficient mice develop progressive cardiac hypertrophy with altered cytokine and calcium handling protein expression. Cardiovasc. Toxicol. 2007;7:165–177
  31. Barouch LA, Harrison RW, Skaf MW, Rosas GO, Cappola TP, Kobeissi ZA, et al. Nitric oxide regulates the heart by spatial confinement of nitric oxide synthase isoforms. Nature. 2002;416:337–339
  32. Sam F, Sawyer DB, Xie Z, Chang DL, Ngoy S, Brenner DA, et al. Mice lacking inducible nitric oxide synthase have improved left ventricular contractile function and reduced apoptotic cell death late after myocardial infarction. Circ. Res. 2001;89:351–356
  33. Zhang P, Xu X, Hu X, van Deel ED, Zhu G, Chen Y. Inducible nitric oxide synthase deficiency protects the heart from systolic overload-induced ventricular hypertrophy and congestive heart failure. Circ. Res. 2007;100:1089–1098
  34. Loyer X, Gomez AM, Milliez P, Fernandez-Velasco M, Vangheluwe P, Vinet L, et al. Cardiomyocyte overexpression of neuronal nitric oxide synthase delays transition toward heart failure in response to pressure overload by preserving calcium cycling. Circulation. 2008;117:3187–3198
  35. Mungrue IN, Gros R, You X, Pirani A, Azad A, Csont T, et al. Cardiomyocyte overexpression of iNOS in mice results in peroxynitrite generation, heart block, and sudden death. J. Clin. Invest. 2002;109:735–743
  36. Champion HC, Skaf MW, Hare JM. Role of nitric oxide in the pathophysiology of heart failure. Heart Fail. Rev. 2003;8:35–46
  37. Moens AL, Takimoto E, Tocchetti CG, Chakir K, Bedja D, Cormaci G, et al. Reversal of cardiac hypertrophy and fibrosis from pressure overload by tetrahydrobiopterin: efficacy of recoupling nitric oxide synthase as a therapeutic strategy. Circulation. 2008;117:2626–2636
  38. Cheng TH, Shih NL, Chen SY, Lin JW, Chen YL, Chen CH, et al. Nitric oxide inhibits endothelin-1-induced cardiomyocyte hypertrophy through cGMP-mediated suppression of extracellular-signal regulated kinase phosphorylation. Mol. Pharmacol. 2005;68:1183–1192
  39. Ritchie RH, Schiebinger RJ, LaPointe MC, Marsh JD. Angiotensin II-induced hypertrophy of adult rat cardiomyocytes is blocked by nitric oxide. Am. J. Physiol. 1998;275:1370–1374
  40. Ruiz-Hurtado G, Fernandez-Velasco M, Mourelle M, Delgado C. LA419, a novel nitric oxide donor, prevents pathological cardiac remodeling in pressure-overloaded rats via endothelial nitric oxide synthase pathway regulation. Hypertension. 2007;50:1049–1056
  41. Fiedler B, Lohmann SM, Smolenski A, Linnemuller S, Pieske B, Schroder F, et al. Inhibition of calcineurin-NFAT hypertrophy signaling by cGMP-dependent protein kinase type I in cardiac myocytes. Proc. Natl. Acad. Sci. U. S. A. 2002;99:11363–11368
  42. Zuckerbraun BS, Stoyanovsky DA, Sengupta R, Shapiro RA, Ozanich BA, Rao J, et al. Nitric oxide-induced inhibition of smooth muscle cell proliferation involves S-nitrosation and inactivation of RhoA. Am. J. Physiol., Cell Physiol. 2007;292:C824–C831
  43. Kempf T, Wollert KC. Nitric oxide and the enigma of cardiac hypertrophy. BioEssays. 2004;26:608–615
  44. Heineke J, Kempf T, Kraft T, Hilfiker A, Morawietz H, Scheubel RJ, et al. Downregulation of cytoskeletal muscle LIM protein by nitric oxide: impact on cardiac myocyte hypertrophy. Circulation. 2003;107:1424–1432
  45. Aikawa R, Nagai T, Tanaka M, Zou Y, Ishihara T, Takano H, et al. Reactive oxygen species in mechanical stress-induced cardiac hypertrophy. Biochem. Biophys. Res. Commun. 2001;289:901–907
  46. Clerk A, Pham FH, Fuller SJ, Sahai E, Aktories K, Marais R, et al. Regulation of mitogen-activated protein kinases in cardiac myocytes through the small G protein Rac1. Mol. Cell. Biol. 2001;21:1173–1184
  47. Huang TY, DerMardirossian C, Bokoch GM. Cofilin phosphatases and regulation of actin dynamics. Curr. Opin. Cell. Biol. 2006;18:26–31
  48. Wang Y, Shibasaki F, Mizuno K. Calcium signal-induced cofilin dephosphorylation is mediated by Slingshot via calcineurin. J. Biol. Chem. 2005;280:12683–12689
  49. Loirand G, Guilluy C, Pacaud P. Regulation of Rho proteins by phosphorylation in the cardiovascular system. Trends Cardiovasc. Med. 2006;16:199–204
  50. Begum N, Sandu OA, Duddy N. Negative regulation of Rho signaling by insulin and its impact on actin cytoskeleton organization in vascular smooth muscle cells: role of nitric oxide and cyclic guanosine monophosphate signaling pathways. Diabetes. 2002;51:2256–2263

PII: S0022-2828(09)00411-8

doi: 10.1016/j.yjmcc.2009.09.012

Journal of Molecular and Cellular Cardiology
Volume 47, Issue 6 , Pages 810-818 , December 2009