Fasudil, a Rho-kinase inhibitor, attenuates angiotensin II-induced abdominal aortic aneurysm in apolipoprotein E-deficient mice by inhibiting apoptosis and proteolysis

Circulation

Volumn 111, Issue 17, 2005, Pages 2219-2226

  Wang, Yi Xin ^a   Martin McNulty, Baby ^a   Da Cunha, Valdeci ^a   Vincelette, Jon ^a   Lu, Xiangru ^b   Feng, Qingping ^b   Halks Miller, Meredith ^a   Mahmoudi, Mithra ^a   Schroeder, Miriam ^a   Subramanyam, Babu ^a   Tseng, Jih Lie ^a   Deng, Gary D ^a   Schirm, Sabine ^a   Johns, Anthony ^a   Kauser, Katalin ^a   Dole, William P ^a   Light, David R ^a  

^a BAYER AG   (Germany)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

Abdominal; Angiotensin II; Aortic aneurysm; Apoptosis; Metalloproteinases; Mice, knockout

Indexed keywords

ANGIOTENSIN; APOLIPOPROTEIN E; CASPASE 3; DEOXYURIDINE TRIPHOSPHATE PYROPHOSPHATASE; DNA FRAGMENT; DNA NUCLEOTIDYLEXOTRANSFERASE; FASUDIL; GELATINASE A; HISTONE; RHO KINASE INHIBITOR;

ABDOMINAL AORTA ANEURYSM; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTERY DIAMETER; ARTICLE; ATHEROSCLEROSIS; BLOOD PRESSURE; CONTROLLED STUDY; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; HYPERLIPOPROTEINEMIA TYPE 3; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; ZYMOGRAPHY;

1-(5-ISOQUINOLINESULFONYL)-2-METHYLPIPERAZINE; ANGIOTENSIN II; ANIMALS; AORTIC ANEURYSM, ABDOMINAL; APOLIPOPROTEINS E; APOPTOSIS; ENDOTHELIUM, VASCULAR; EXTRACELLULAR MATRIX; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, KNOCKOUT; PROTEASE INHIBITORS; PROTEIN KINASE INHIBITORS; PROTEIN-SERINE-THREONINE KINASES;

EID: 20944444181     PISSN: 00097322     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.CIR.0000163544.17221.BE     Document Type: Article

References (51)

1. Tham DM, Martin-McNulty B, Wang YX, Wilson DW, Vergona R, Sullivan ME, Dole W, Rutledge JC. Angiotensin II is associated with activation of NF-kappaB-mediated genes and downregulation of PPARs. Physiol Genomics. 2002;11:21-30.
2. Wang YX, Martin-McNulty B, Freay AD, Sukovich DA, Halks-Miller M, Li WW, Vergona R, Sullivan ME, Morser J, Dole WP, Deng GG. Angiotensin II increases urokinase-type plasminogen activator expression and induces aneurysm in the abdominal aorta of apolipoprotein E-deficient mice. Am J Pathol. 2001;159:1455-1464.
3. Daugherty A, Manning MW, Cassis LA. Angiotensin II promotes atherosclerotic lesions and aneurysms in apolipoprotein E-deficient mice. J Clin Invest. 2000;105:1605-1612.
4. Daugherty A, Cassis LA. Mechanisms of abdominal aortic aneurysm formation. Curr Atheroscler Rep. 2002;4:222-227.
5. Carmeliet P, Moons L, Lijnen R, Baes M, Lemaitre V, Tipping P, Drew A, Eeckhout Y, Shapiro S, Lupu F, Collen D. Urokinase-generated plasmin activates matrix metalloproteinases during aneurysm formation. Nat Genet. 1997;17:439-444.
6. Deng GG, Martin-McNulty B, Sukovich DA, Freay A, Halks-Miller M, Thinnes T, Loskutoff DJ, Carmeliet P, Dole WP, Wang YX. Urokinase-type plasminogen activator plays a critical role in angiotensin II-induced abdominal aortic aneurysm. Circ Res. 2003;92:510-517.
7. Thompson RW. Reflections on the pathogenesis of abdominal aortic aneurysms. Cardiovasc Surg. 2002;10:389-394.
8. Hara A, Yoshimi N, Mori H. Evidence for apoptosis in human intracranial aneurysms. Neurol Res. 1998;20:127-130.
9. Jacob T, Ascher E, Hingorani A, Gunduz Y, Kallakuri S. Initial steps in the unifying theory of the pathogenesis of artery aneurysms. J Surg Res. 2001;101:37-43.
10. Holmes DR, Lopez-Candales A, Liao S, Thompson RW. Smooth muscle cell apoptosis and p53 expression in human abdominal aortic aneurysms. Ann NY Acad Sci. 1996;800:286-287.
11. Jacob T, Hingorani A, Ascher E. Examination of the apoptotic pathway and proteolysis in the pathogenesis of popliteal artery aneurysms. Eur J Vasc Endovasc Surg. 2001;22:77-85.
12. Kondo S, Hashimoto N, Kikuchi H, Hazama F, Nagata I, Kataoka H. Apoptosis of medial smooth muscle cells in the development of saccular cerebral aneurysms in rats. Stroke. 1998;29:181-188; discussion 189.
13. Lopez-Candales A, Holmes DR, Liao S, Scott MJ, Wickline SA, Thompson RW. Decreased vascular smooth muscle cell density in medial degeneration of human abdominal aortic aneurysms. Am J Pathol. 1997;150:993-1007.
14. Nataatmadja M, West M, West J, Summers K, Walker P, Nagata M, Watanabe T. Abnormal extracellular matrix protein transport associated with increased apoptosis of vascular smooth muscle cells in Marfan syndrome and bicuspid aortic valve thoracic aortic aneurysm. Circulation. 2003;108(suppl II):II-329-II-34.
15. Stehbens WE. Apoptosis and matrix vesicles in the genesis of arterial aneurysms of cerebral arteries. Stroke. 1998;29:1478-1480.
16. Henderson EL, Geng YJ, Sukhova GK, Whittemore AD, Knox J, Libby P. Death of smooth muscle cells and expression of mediators of apoptosis by T lymphocytes in human abdominal aortic aneurysms. Circulation. 1999;99:96-104.
17. Rowe VL, Stevens SL, Reddick TT, Freeman MB, Donnell R, Carroll RC, Goldman MH. Vascular smooth muscle cell apoptosis in aneurysmal, occlusive, and normal human aortas. J Vasc Surg. 2000;31:567-576.
18. Sakaki T, Kohmura E, Kishiguchi T, Yuguchi T, Yamashita T, Hayakawa T. Loss and apoptosis of smooth muscle cells in intracranial aneurysms: studies with in situ DNA end labeling and antibody against single-stranded DNA. Acta Neurochir (Wien). 1997;139:469-474; discussion 474-45.
19. Miller FJ Jr, Sharp WJ, Fang X, Oberley LW, Oberley TD, Weintraub NL. Oxidative stress in human abdominal aortic aneurysms: a potential mediator of aneurysmal remodeling. Arterioscler Thromb Vasc Biol. 2002;22:560-565.
20. Satta J, Mennander A, Soini Y, Holmes DR, Lopez-Candales A, Liao S, Thompson RW. Increased medial TUNEL-positive staining associated with apoptotic bodies is linked to smooth muscle cell diminution during evolution of abdominal aortic aneurysms. Ann Vasc Surg. 2002;16:462-466.
21. Thompson RW, Liao S, Curci JA. Vascular smooth muscle cell apoptosis in abdominal aortic aneurysms. Coron Artery Dis. 1997;8:623-631.
22. 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.
23. Matsumoto Y, Uwatoku T, Oi K, Abe K, Hattori T, Morishige K, Eto Y, Fukumoto Y, Nakamura K, Shibata Y, Matsuda T, Takeshita A, Shimokawa H. Long-term inhibition of Rho-kinase suppresses neointimal formation after stent implantation in porcine coronary arteries: involvement of multiple mechanisms. Arterioscler Thromb Vasc Biol. 2004;24:181-186.
24. Shibata R, Kai H, Seki Y, Kato S, Morimatsu M, Kaibuchi K, Imaizumi T. Role of Rho-associated kinase in neointima formation after vascular injury. Circulation. 2001;103:284-289.
25. Johnston KW, Rutherford RB, Tilson MD, Shah DM, Hollier L, Stanley JC. Suggested standards for reporting on arterial aneurysms: Subcommittee on Reporting Standards for Arterial Aneurysms, Ad Hoc Committee on Reporting Standards, Society for Vascular Surgery and North American Chapter, International Society for Cardiovascular Surgery. J Vasc Surg. 1991;13:452-458.
26. Daugherty A, Manning MW, Cassis LA. Antagonism of AT2 receptors augments angiotensin II-induced abdominal aortic aneurysms and atherosclerosis. Br J Pharmacol. 2001;134:865-870.
27. 17β-Estradiol attenuates development of angiotensin II-induced aortic abdominal aneurysm in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol. 2003;23:1627-32.
28. Wang YX, Halks-Miller M, Vergona R, Sullivan ME, Fitch R, Mallari C, Martin-McNulty B, da Cunha V, Freay A, Rubanyi GM, Kauser K. Increased aortic stiffness assessed by pulse wave velocity in apolipoprotein E-deficient mice. Am J Physiol Heart Circ Physiol. 2000;278:H428-H434.
29. Feng Q, Song W, Lu X, Hamilton JA, Lei M, Peng T, Yee SP. Development of heart failure and congenital septal defects in mice lacking endothelial nitric oxide synthase. Circulation. 2002;106:873-879.
30. Song W, Lu X, Feng Q. Tumor necrosis factor-alpha induces apoptosis via inducible nitric oxide synthase in neonatal mouse cardiomyocytes. Cardiovasc Res. 2000;45:595-602.
31. Hartley CJ, Reddy AK, Madala S, Martin-McNulty B, Vergona R, Sullivan ME, Halks-Miller M, Taffet GE, Michael LH, Entman ML, Wang YX. Hemodynamic changes in apolipoprotein E-knockout mice. Am J Physiol Heart Circ Physiol. 2000;279:H2326-H2334.
32. Stadelmann C, Lassmann H. Detection of apoptosis in tissue sections. Cell Tissue Res. 2000;301:19-31.
33. Armstrong RC, Aja TJ, Hoang KD, Gaur S, Bai X, Alnemri ES, Litwack G, Karanewsky DS, Fritz LC, Tomaselli KJ. Activation of the CED3/ ICE-related protease CPP32 in cerebellar granule neurons undergoing apoptosis but not necrosis. J Neurosci. 1997;17:553-562.
34. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72:248-254.
35. 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.
36. Hattori T, Shimokawa H, Higashi M, Hiroki J, Mukai Y, Tsutsui H, Kaibuchi K, Takeshita A. Long-term inhibition of Rho-kinase suppresses left ventricular remodeling after myocardial infarction in mice. Circulation. 2004;109:2234-2239.
37. Shimokawa H. Rho-kinase as a novel therapeutic target in treatment of cardiovascular diseases. J Cardiovasc Pharmacol. 2002;39:319-327.
38. Manning MW, Cassis LA, Daugherty A. Differential effects of doxycycline, a broad-spectrum matrix metalloproteinase inhibitor, on angiotensin II-induced atherosclerosis and abdominal aortic aneurysms. Arterioscler Thromb Vasc Biol. 2003;23:483-488.
39. Chen J, Kuhlencordt PJ, Astern J, Gyurko R, Huang PL. Hypertension does not account for the accelerated atherosclerosis and development of aneurysms in male apolipoprotein e/endothelial nitric oxide synthase double knockout mice. Circulation. 2001;104:2391-2394.
40. Rattan S, Puri RN, Fan YP. Involvement of Rho and Rho-associated kinase in sphincteric smooth muscle contraction by angiotensin II. Exp Biol Med (Maywood). 2003;228:972-981.
41. 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.
42. Zheng Y, Guan H, Li Y, Liu C, Liu B, Sheng Q, Miao S. Microarray in screening for differentially expressed genes of cellular cycle and apoptosis in abdominal aortic aneurysms [in Chinese]. Zhonghua Wai Ke Za Zhi. 2002;40:817-819.
43. 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. Arteriosder Thromb Vasc Biol. 2000;20:2351-2358.
44. Ikegaki I, Hattori T, Yamaguchi T, Sasaki Y, Satoh SI, Asano T, Shimokawa H. Involvement of Rho-kinase in vascular remodeling caused by long-term inhibition of nitric oxide synthesis in rats. Eur J Pharmacol. 2001;427:69-75.
45. Pinderski LJ, Fischbein MP, Subbanagounder G, Fishbein MC, Kubo N, Cheroutre H, Curtiss LK, Berliner JA, Boisvert WA. Overexpression of interleukin-10 by activated T lymphocytes inhibits atherosclerosis in LDL receptor-deficient mice by altering lymphocyte and macrophage phenotypes. Circ Res. 2002;90:1064-1071.
46. Daugherty A, Rateri DL. T Lymphocytes in atherosclerosis: the yin-yang of Th1 and Th2 influence on lesion formation. Circ Res. 2002;90:1039-1040.
47. Mallat Z, Gojova A, Sauzeau V, Brun V, Silvestre J-S, Esposito B, Merval R, Groux H, Loirand G, Tedgui A. Rho-associated protein kinase contributes to early atherosclerotic lesion formation in mice. Circ Res. 2003;93:884-888.
48. Tharaux PL, Bukoski RC, Rocha PN, Crowley SD, Ruiz P, Nataraj C, Howell DN, Kaibuchi K, Spurney RF, Coffman TM. Rho kinase promotes alloimmune responses by regulating the proliferation and structure of T cells. J Immunol. 2003;171:96-105.
49. Saraff K, Babamusta F, Cassis LA, Daugherty A. Aortic dissection precedes formation of aneurysms and atherosclerosis in angiotensin II-infused, apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol. 2003;23:1621-1626.
50. Negoro N, Hoshiga M, Seto M, Kohbayashi E, Ii M, Fukui R, Shibata N, Nakakoji T, Nishiguchi F, Sasaki Y, Ishihara T, Ohsawa N. The kinase inhibitor fasudil (HA-1077) reduces intimal hyperplasia through inhibiting migration and enhancing cell loss of vascular smooth muscle cells. Biochem Biophys Res Commun. 1999;262:211-215.
51. Abe K, Shimokawa H, Morikawa K, Uwatoku T, Oi K, Matsumoto Y, Hattori T, Nakashima Y, Kaibuchi K, Sueishi K, Takeshita A. Long-term treatment with a Rho-kinase inhibitor improves monocrotaline-induced fatal pulmonary hypertension in rats. Circ Res. 2004;94:385-393.