Long-Term Inhibition of Rho-Kinase Suppresses Angiotensin II-Induced Cardiovascular Hypertrophy in Rats In Vivo: Effect on Endothelial NAD(P)H Oxidase System

Circulation Research

Volumn 93, Issue 8, 2003, Pages 767-775

  Higashi, Midoriko ^a   Shimokawa, Hiroaki ^a   Hattori, Tsuyoshi ^a   Hiroki, Junko ^a   Mukai, Yasushi ^a   Morikawa, Keiko ^a   Ichiki, Toshihiro ^a   Takahashi, Shosuke ^a   Takeshita, Akira ^a  

^a KYUSHU UNIVERSITY   (Japan)

Author keywords

Angiotensin II; Arteriosclerosis; Cardiovascular hypertrophy; Rho kinase; Superoxide anion

Indexed keywords

ANGIOTENSIN; ENZYME INHIBITOR; FASUDIL; GUANOSINE TRIPHOSPHATASE; HYDROXYFASUDIL; INDOMETACIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; RHO KINASE; SUPEROXIDE; UNCLASSIFIED DRUG; 1 (5 ISOQUINOLINESULFONYL) 2 METHYLPIPERAZINE; ANGIOTENSIN II; DRUG DERIVATIVE; PROTEIN SERINE THREONINE KINASE; RHO-ASSOCIATED KINASE; SIGNAL PEPTIDE; VASOCONSTRICTOR AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERIOLOSCLEROSIS; ARTICLE; CELL FUNCTION; CONTROLLED STUDY; DOSE RESPONSE; DRUG EFFECT; DRUG MECHANISM; DRUG SCREENING; ENZYME ACTIVATION; ENZYME INHIBITION; GENE EXPRESSION; HEART HYPERTROPHY; IN VITRO STUDY; IN VIVO STUDY; LONG TERM CARE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SMOOTH MUSCLE CONTRACTION; UPREGULATION; VASCULAR SMOOTH MUSCLE; VASODILATATION; ANIMAL; CARDIOMEGALY; CELL MOTION; CHEMICALLY INDUCED DISORDER; CORONARY BLOOD VESSEL; CYTOLOGY; DRUG ANTAGONISM; ENZYMOLOGY; HYPERTENSION; MACROPHAGE; MALE; METABOLISM; ORGAN CULTURE TECHNIQUE; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; THORACIC AORTA; VASCULAR ENDOTHELIUM; WISTAR KYOTO RAT;

1-(5-ISOQUINOLINESULFONYL)-2-METHYLPIPERAZINE; ANGIOTENSIN II; ANIMALS; AORTA, THORACIC; CARDIOMEGALY; CELL MOVEMENT; CORONARY VESSELS; ENDOTHELIUM, VASCULAR; ENZYME INHIBITORS; HYPERTENSION; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MACROPHAGES; MALE; NADPH OXIDASE; ORGAN CULTURE TECHNIQUES; PROTEIN-SERINE-THREONINE KINASES; RATS; RATS, INBRED WKY; SUPEROXIDES; VASOCONSTRICTOR AGENTS; VASODILATION;

EID: 0142120102     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.RES.0000096650.91688.28     Document Type: Article

References (53)

1. Rajagopalan S, Kurz S, Münzel T, Tarpey M, Freeman BA, Griendling KK, Harrison DG. Angiotensin II-mediated hypertension in the rat increases vascular superoxide production via membrane NADH/NADPH oxidase activation: contribution to alterations of vasomotor tone. J Clin Invest. 1996;97:1916-1923.
2. Lever AF. Angiotensin II, angiotensin-converting enzyme inhibitors, and blood vessel structure. Am J Med. 1992;92:35S-38S.
3. Capers Q 4th, Alexander RW, Lou P, De Leon H, Wilcox JN, Ishizaka N, Howard AB, Taylor WR. Monocyte chemoattractant protein-1 expression in aortic tissues of hypertensive rats. Hypertension. 1997;30:1397-1402.
4. Somlyo AP, Somlyo AV. Signal transduction by G-proteins, Rho-kinase and protein phosphatase to smooth muscle and non-muscle myosin II. J Physiol. 2000;522:177-185.
5. Uehata M, Ishizaki T, Satoh H, Ono T, Kawahara T, Morishita T, Tamakawa H, Yamagami K, Inui J, Maekawa M, Narumiya S. Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature. 1997;389:990-994.
6. Kimura K, Ito M, Amano M, Chihara K, Fukata Y, Nakafuku M, Yamamori B, Feng J, Nakano T, Okawa K, Iwamatsu A, Kaibuchi K. Regulation of myosin phosphatase by Rho and Rho-associated kinase (Rho-kinase). Science. 1996;273:245-248.
7. Nagumo H, Sasaki Y, Ono Y, Okamoto H, Seto M, Takuwa Y. Rho kinase inhibitor HA-1077 prevents Rho-mediated myosin phosphatase inhibition in smooth muscle cells. Am J Physiol. 2000;278:C57-C65.
8. Funakoshi Y, Ichiki T, Shimokawa H, Egashira K, Takeda K, Kaibuchi K, Takeya M, Yoshimura T, Takeshita A. Rho-kinase mediates angiotensin II-induced monocyte chemoattractant protein-1 expression in rat vascular smooth muscle cells. Hypertension. 2001;38:100-104.
9. Takeda K, Ichiki T. Tokunou T, Iino N, Fujii S, Kitabatake A, Shimokawa H, Takeshita A. Critical role of Rho-kinase and MEK/ERK pathways for angiotensin II-induced plasminogen activator inhibitor type-1 gene expression. Arterioscler Thromb Vasc Biol. 2001;21:868-873.
10. Hiroki J, Kandabashi T, Hattori T, Mukai Y, Kawamura N, Ichiki T, Shimokawa H. Inflammatory stimuli upregulate Rho-kinase in human vascular smooth muscle cells: divergent effects of estrogen and nicotine. Circulation. 2002;106(suppl II):II-222. Abstract.
11. Mukai Y, Shimokawa H, Matoba T, Kandabashi T, Satoh S, Hiroki J, Kaibuchi K, Takeshita A. Involvement of Rho-kinase in hypertensive vascular disease: a novel therapeutic target in hypertension. FASEB J. 2001;15:1062-1064.
12. Shimokawa H, Seto M, Katsumata N, Amano M, Kozai T, Yamawaki T, Kuwata K, Kandabashi T, Egashira K, Ikegaki I, Asano T, Kaibuchi K, Takeshita A. Rho-kinase-mediated pathway induces enhanced myosin light chain phosphorylations in a swine model of coronary artery spasm. Cardiovasc Res. 1999;43:1029-1039.
13. Morishige K, Shimokawa H, Eto Y, Kandabashi T, Miyata K, Matsumoto Y, Hoshijima M, Kaibuchi K, Takeshita A. Adenovirus-mediated transfer of dominant-negative Rho-kinase induces a regression of coronary arteriosclerosis in pigs in vivo. Arterioscler Thromb Vasc Biol. 2001;21: 548-554.
14. Oshiro N, Fukara Y, Kaibuchi K. Phosphorylation of moesin by Rho-associated kinase (Rho-kinase) plays a crucial role in the formation of microvilli-like structures. J Biol Chem. 1998;273:34663-34666.
15. Urakami-Harasawa L, Shimokawa H, Nakashima M, Egashira K, Takeshita A. Importance of endothelium-derived hyperpolarizing factor in human arteries. J Clin Invest. 1997;100:2793-2799.
16. Mukai Y, Shimokawa H, Higashi M, Morikawa K, Matoba T, Hiroki J, Kunihiro I, Talukder HM, Takeshita A. Inhibition of renin-angiotensin system ameliorates endothelial dysfunction associated with aging in rats. Arterioscler Thromb Vasc Biol. 2002;22:1445-1450.
17. Kashiwagi A, Shinozaki K, Nishio Y, Maegawa H, Maeno Y, Kanazawa A, Kojima H, Haneda M, Hidaka H, Yasuda H, Kikkawa R. Endothelium-specific activation of NAD(P)H oxidase in aortas of exogenously hyperinsulinemic rats. Am J Physiol. 1999;277:E976-E983.
18. phox homologues in vascular smooth muscle cells: nox1 mediates angiotensin II-induced superoxide formation and redox-sensitive signaling pathways. Circ Res. 2001;88: 888-894.
19. Griffin SA, Brown WCB, MacPherson F, MacGrath JC, Wilson VG, Korsgaard N, Mulvany MJ, Lever AF. Angiotensin causes vascular hypertrophy in part by a non-pressor mechanism. Hypertension. 1991;17: 626-635.
20. Daemen MJ, Lombardi DM, Bosman FT, Schwartz SM. Angiotensin II induces smooth muscle cell proliferation in the normal and injured rat arterial wall. Circ Res. 1991;68:450-456.
21. Lnag D, Mosfer SI, Shakesby A, Donaldson F, Lewis MJ. Coronary microvascular endothelial cell redox state in left ventricular hypertrophy: the role of angiotensin II. Circ Res. 2000;86:463-469.
22. Phox-containing NADPH oxidase in angiotensin II-induced cardiac hypertrophy in mice. Circulation. 2002;105:293-296.
23. Babior BM. NADPH oxidase: an update. Blood. 1999;93:1464-1476.
24. Griendling KK, Minieri CA, Ollerenshaw JD, Alexander RW. Angiotensin II stimulates NADH and NADPH oxidase activity in cultured vascular smooth muscle cells. Circ Res. 1994;74:1141-1148.
25. Pagano PJ, Clark JK, Cifuentes-Pagano ME, Clark SM, Callis GM, Quinn MT. Localization of constitutively active, phagocyte-like NADPH oxidase in rabbit aortic adventitia: enhancement by angiotensin II. Proc Natl Acad Sci USA. 1997;94:14483-14488.
26. Wiener J, Lombardi DM, Su JE, Schwartz SM. Immunohistochemical and molecular characterization of the differential response of the rat mesenteric microvasculature to angiotensin-II infusion. J Vasc Res. 1996; 33:195-208.
27. Kato H, Hou J, Chobanian AV, Brecher P. Effects of angiotensin II infusion and inhibition of nitric oxide synthase on the rat aorta. Hypertension. 1996;28:153-158.
28. Chen XL, Tummala PE, Olbrych MT, Alexander RW, Medford RM. Angiotensin II induces monocyte chemoattractant protein-1 gene expression in rat vascular smooth muscle cells. Circ Res. 1998;83: 952-959.
29. Shimokawa H. Rho-kinase as a novel therapeutic target in treatment of cardiovascular diseases. J Cardiovasc Pharmacol. 2002;39:319-327.
30. Yamakawa T, Tanaka S, Numaguchi K, Yamakawa Y, Motley ED, Ichihara S, Inagami T. Involvement of Rho-kinase in angiotensin II-induced hypertrophy of rat vascular smooth muscle cells. Hypertension. 2000;35:313-318.
31. Shimokawa H. Cellular and molecular mechanisms of coronary artery spasm: lessons from animal models. Jpn Circ J. 2000;64:1-12.
32. van Nieuw Amerongen GP, van Delft S, Vermeer MA, Collard JG, van Hinsbergh VWM. Activation of Rho A by thrombin in endothelial hyperpermeability: role of Rho kinase and protein tyrosine kinases. Circ Res. 2000;87:335-340.
33. Seasholtz TM, Majumdar M, Kaplan DD, Brown JH. Rho and Rho kinase mediate thrombin-stimulated vascular smooth muscle cell DNA synthesis and migration. Circ Res. 1999;84:1186-1193.
34. Yamamoto Y, Ikegaki I, Sasaki Y, Uchida T. The protein kinase inhibitor fasudil protects against ischemic myocardial injury induced by endothelin-1 in the rabbit. J Cardiovasc Pharmacol. 2000;35:203-211.
35. Tangkijvanich P, Tam SP, Yee HF Jr. Wound-induced migration of rat hepatic stellate cells is modulated by endothelin-1 through rho-kinase-mediated alterations in the acto-myosin cytoskeleton. Hepatology. 2001; 33:74-80.
36. 2+ handling of human small arteries. Am J Physiol. 2000;279:H1228-H1238.
37. Kishi H, Bao J, Kohama K. Inhibitory effects of ML-9, wortmannin, and Y-27632 on the chemotaxis of vascular smooth muscle cells in response to platelet-derived growth factor-BB. J Biochem. 2000;128:719-722.
38. Eto Y, Shimokawa H, Hiroki J, Morishige K, Kandabashi T, Matsumoto Y, Amano M, Hoshijima M, Kaibuchi K, Takeshita A. Gene transfer of dominant negative Rho kinase suppresses neointimal formation after balloon injury in pigs. Am J Physiol. 2000;278:H1744-H1750.
39. Miyata K, Shimokawa H, Kandabashi T, Higo T, Morishige K, Eto Y, Egashira K, Kaibuchi K, Takeshita A. Rho-kinase is involved in macrophage-mediated formation of coronary vascular lesions in pigs in vivo. Arterioscler Thromb Vasc Biol. 2000;20:2351-2358.
40. Kandabashi T, Shimokawa H, Miyata K, Kunihiro I, Kawano Y, Fukata Y, Higo T, Egashira K, Takahashi S, Kaibuchi K, Takeshita A. Inhibition of myosin phosphatase by upregulated Rho-kinase plays a key role for coronary artery spasm in a porcine model with interleukin-1β. Circulation. 2000;101:1319-1323.
41. Sawada N, Itoh H, Ueyama K, Yamashita J, Doi K, Chun TH, Inoue M, Masatsugu K, Saito T, Fukunaga Y, Sakaguchi S, Arai H, Ohno N, Komeda M, Nakao K. Inhibition of Rho-associated kinase results in suppression of neointimal formation of balloon-injured arteries. Circulation. 2000;101:2030-2033.
42. Kaibuchi K, Kuroda S, Amano M. Regulation of cytoskeleton and cell adhesion by the Rho family GTPases in mammalian cells. Annu Rev Biochem. 1999;68:459-486.
43. Wójciak-Stothard B, Williams L, Ridley AJ. Monocyte adhesion and spreading on human endothelial cells is dependent on Rho-regulated receptor clustering. J Cell Biol. 1999;145:1293-1307.
44. Görlach A, Brandes RP, Nguyen K, Amidi M, Dehghani F, Busse R. A gp91phox containing NADPH oxidase selectively expressed in endothelial cells is a major source of oxygen radical generation in the arterial wall. Circ Res. 2000;87:26-32.
45. Suh YA, Arnold RS, Lassègue B, Shi J, Xu X, Sorescu D, Chung AB, Griendling KK, Lambeth JD. Cell transformation by the superoxide-generating oxidase moxl. Nature. 1999;401:79-82.
46. Mollnau H, Wendt M, Szöcs K, Lassègue B, Schulz E, Oelze M, Li H, Bodenschatz M, August M, Kleschyov AL, Tsilimingas N, Walter U, Förstermann U, Meinertz T, Griendling K, Münzel T. Effects of angiotensin II infusion on the expression and function of NAD(P)H oxidase and components of nitric oxide/cGMP signaling. Circ Res. 2002;90: e58-e65.
47. Wingler K, Wünsch S, Kreutz R, Rothermund L, Paul M, Schmidt HH. Upregulation of the vascular NAD(P)H-oxidase isoforms nox1 and nox4 by the renin-angiotensin system in vitro and in vivo. Free Radic Biol Med. 2001;31:1456-1464.
48. Fukui R, Ishizaka N, Rajagopalan S, Laursen JB, Capers Q 4th, Taylor WR, Harrison DG, de Leon H, Wilcox JN, Griendling KK. p22phox mRNA expression and NADPH oxidase activity are increased in aortas from hypertensive rats. Circ Res. 1997;80:45-51.
49. phox mRNA expression and NADPH oxidase superoxide generation in rabbit aortic adventitial fibroblasts. Hypertension. 1998;32: 331-337.
50. phox is a critical component of the superoxide-generating NADH/NADPH oxidase system and regulates angiotensin II-induced hypertrophy in vascular smooth muscle cells. J Biol Chem. 1996;271:23317-23321.
51. Shimokawa H. Primary endothelial dysfunction: atherosclerosis. J Mol Cell Cardiol. 1999;31:23-37.
52. Laufs U, Liao JK. Post-transcriptional regulation of endothelial nitric oxide synthase mRNA stability by Rho GTPase. J Biol Chem. 1998;273: 24266-24271.
53. Takemoto M, Sun J, Hiroki J, Shimokawa H, Liao JK. Rho-kinase mediates hypoxia-induced downregulation of endothelial nitric oxide synthase. Circulation. 2002;106:57-62.