SmgGDS as a crucial mediator of the inhibitory effects of statins on cardiac hypertrophy and fibrosis: Novel mechanism of the pleiotropic effects of statins

Hypertension

Volumn 67, Issue 5, 2016, Pages 878-889

  Kudo, Shun ^a   Satoh, Kimio ^a   Nogi, Masamichi ^a   Suzuki, Kota ^a   Sunamura, Shinichiro ^a   Omura, Junichi ^a   Kikuchi, Nobuhiro ^a   Kurosawa, Ryo ^a   Satoh, Taijyu ^a   Minami, Tatsuro ^a   Ikeda, Shohei ^a   Miyata, Satoshi ^a   Shimokawa, Hiroaki ^a  

^a TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

angiotensin II; chemokines; oxidative stress; pravastatin; statin

Indexed keywords

ANGIOTENSIN II; ATORVASTATIN; BRAIN NATRIURETIC PEPTIDE; CHEMOKINE; GROWTH FACTOR; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PRAVASTATIN; RAC1 PROTEIN; RHO KINASE; CYTOSKELETON PROTEIN; KIFAP3 PROTEIN, MOUSE; REACTIVE OXYGEN METABOLITE; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; AORTA CONSTRICTION; ARTICLE; CARDIAC MUSCLE CELL; CONDITIONED MEDIUM; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME ACTIVITY; GENOTYPE; HEART FIBROBLAST; HEART MUSCLE FIBROSIS; HEART VENTRICLE HYPERTROPHY; HISTOPATHOLOGY; MALE; MOUSE; NONHUMAN; OSMOTIC PUMP; OXIDATIVE STRESS; PLEIOTROPY; PRIORITY JOURNAL; SYSTOLIC BLOOD PRESSURE; UPREGULATION; ANIMAL; CARDIOMEGALY; CELL CULTURE; CELL PROLIFERATION; DISEASE MODEL; DRUG EFFECTS; FIBROSIS; GENETICS; METABOLISM; PATHOLOGY; PROCEDURES; RANDOMIZATION; RAT; REAL TIME POLYMERASE CHAIN REACTION; ROLE PLAYING; SPECIES DIFFERENCE; WESTERN BLOTTING;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; BLOTTING, WESTERN; CARDIOMEGALY; CELL PROLIFERATION; CELLS, CULTURED; CHEMOKINES; CYTOSKELETAL PROTEINS; DISEASE MODELS, ANIMAL; FIBROSIS; HYDROXYMETHYLGLUTARYL-COA REDUCTASE INHIBITORS; MICE; MYOCYTES, CARDIAC; PRAVASTATIN; RANDOM ALLOCATION; RATS; REACTIVE OXYGEN SPECIES; REAL-TIME POLYMERASE CHAIN REACTION; ROLE; SPECIES SPECIFICITY;

EID: 84961231160     PISSN: 0194911X     EISSN: 15244563     Source Type: Journal    
DOI: 10.1161/HYPERTENSIONAHA.115.07089     Document Type: Article

References (56)

1. Shepherd J, Cobbe SM, Ford I, Isles CG, Lorimer AR, MacFarlane PW, McKillop JH, Packard CJ, Prevention of coronary heart disease with pravastatin in men with hypercholesterolemia. West of Scotland Coronary Prevention Study Group. N Engl J Med 1995 333 1301 1307. doi: 10.1056/NEJM199511163332001
2. Ridker PM, Danielson E, Fonseca FA, Genest J, Gotto AM Jr, Kastelein JJ, Koenig W, Libby P, Lorenzatti AJ, MacFadyen JG, Nordestgaard BG, Shepherd J, Willerson JT, Glynn RJ, JUPITER Study Group Rosuvastatin to prevent vascular events in men and women with elevated C-reactive protein. N Engl J Med 2008 359 2195 2207. doi: 10.1056/NEJMoa0807646
3. Liao JK, Laufs U, Pleiotropic effects of statins. Annu Rev Pharmacol Toxicol 2005 45 89 118. doi: 10.1146/annurev.pharmtox.45.120403.095748
4. Takemoto M, Node K, Nakagami H, Liao Y, Grimm M, Takemoto Y, Kitakaze M, Liao JK, Statins as antioxidant therapy for preventing cardiac myocyte hypertrophy. J Clin Invest 2001 108 1429 1437. doi: 10.1172/JCI13350
5. Sparrow CP, Burton CA, Hernandez M, Mundt S, Hassing H, Patel S, Rosa R, Hermanowski-Vosatka A, Wang PR, Zhang D, Peterson L, Detmers PA, Chao YS, Wright SD, Simvastatin has anti-inflammatory and antiatherosclerotic activities independent of plasma cholesterol lowering. Arterioscler Thromb Vasc Biol 2001 21 115 121
6. Yagi S, Aihara K, Ikeda Y, Sumitomo Y, Yoshida S, Ise T, Iwase T, Ishikawa K, Azuma H, Akaike M, Matsumoto T, Pitavastatin, an HMG-CoA reductase inhibitor, exerts eNOS-independent protective actions against angiotensin II induced cardiovascular remodeling and renal insufficiency. Circ Res 2008 102 68 76. doi: 10.1161/CIRCRESAHA.107.163493
7. Kameda Y, Hasegawa H, Kubota A, Tadokoro H, Kobayashi Y, Komuro I, Takano H, Effects of pitavastatin on pressure overload-induced heart failure in mice. Circ J 2012 76 1159 1168
8. Rikitake Y, Liao JK, Rho GTPases, statins, and nitric oxide. Circ Res 2005 97 1232 1235. doi: 10.1161/01.RES.0000196564.18314.23
9. Van Aelst L, D'Souza-Schorey C, Rho GTPases and signaling networks. Genes Dev 1997 11 2295 2322
10. Rashid M, Tawara S, Fukumoto Y, Seto M, Yano K, Shimokawa H, Importance of Rac1 signaling pathway inhibition in the pleiotropic effects of HMG-CoA reductase inhibitors. Circ J 2009 73 361 370
11. Tanaka S, Fukumoto Y, Nochioka K, Minami T, Kudo S, Shiba N, Takai Y, Williams CL, Liao JK, Shimokawa H, Statins exert the pleiotropic effects through small GTP-binding protein dissociation stimulator upregulation with a resultant Rac1 degradation. Arterioscler Thromb Vasc Biol 2013 33 1591 1600. doi: 10.1161/ATVBAHA.112.300922
12. Isomura M, Kaibuchi K, Yamamoto T, Kawamura S, Katayama M, Takai Y, Partial purification and characterization of GDP dissociation stimulator (GDS) for the rho proteins from bovine brain cytosol. Biochem Biophys Res Commun 1990 169 652 659
13. Yamamoto T, Kaibuchi K, Mizuno T, Hiroyoshi M, Shirataki H, Takai Y, Purification and characterization from bovine brain cytosol of proteins that regulate the GDP/GTP exchange reaction of smg p21s, ras p21-like GTP-binding proteins. J Biol Chem 1990 265 16626 16634
14. Yaku H, Sasaki T, Takai Y, The Dbl oncogene product as a GDP/GTP exchange protein for the Rho family: its properties in comparison with those of Smg GDS. Biochem Biophys Res Commun 1994 198 811 817. doi: 10.1006/bbrc.1994.1116
15. Vikis HG, Stewart S, Guan KL, SmgGDS displays differential binding and exchange activity towards different Ras isoforms. Oncogene 2002 21 2425 2432. doi: 10.1038/sj.onc.1205306
16. Lanning CC, Ruiz-Velasco R, Williams CL, Novel mechanism of the co-regulation of nuclear transport of SmgGDS and Rac1. J Biol Chem 2003 278 12495 12506. doi: 10.1074/jbc.M211286200
17. Williams CL, The polybasic region of Ras and Rho family small GTPases: a regulator of protein interactions and membrane association and a site of nuclear localization signal sequences. Cell Signal 2003 15 1071 1080
18. Satoh M, Ogita H, Takeshita K, Mukai Y, Kwiatkowski DJ, Liao JK, Requirement of Rac1 in the development of cardiac hypertrophy. Proc Natl Acad Sci U S A 2006 103 7432 7437. doi: 10.1073/pnas.0510444103
19. Takakura A, Miyoshi J, Ishizaki H, Tanaka M, Togawa A, Nishizawa Y, Yoshida H, Nishikawa Si, Takai Y, Involvement of a small GTP-binding protein (G protein) regulator, small G protein GDP dissociation stimulator, in antiapoptotic cell survival signaling. Mol Biol Cell 2000 11 1875 1886
20. Ikeda S, Satoh K, Kikuchi N, Miyata S, Suzuki K, Omura J, Shimizu T, Kobayashi K, Kobayashi K, Fukumoto Y, Sakata Y, Shimokawa H, Crucial role of rho-kinase in pressure overload-induced right ventricular hypertrophy and dysfunction in mice. Arterioscler Thromb Vasc Biol 2014 34 1260 1271. doi: 10.1161/ATVBAHA.114.303320
21. Godo S, Sawada A, Saito H, Ikeda S, Enkhjargal B, Suzuki K, Tanaka S, Shimokawa H, Disruption of Physiological Balance Between Nitric Oxide and Endothelium-Dependent Hyperpolarization Impairs Cardiovascular Homeostasis in Mice. Arterioscler Thromb Vasc Biol 2016 36 97 107. doi: 10.1161/ATVBAHA.115.306499
22. Fukui S, Fukumoto Y, Suzuki J, Saji K, Nawata J, Shinozaki T, Kagaya Y, Watanabe J, Shimokawa H, Diabetes mellitus accelerates left ventricular diastolic dysfunction through activation of the renin-Angiotensin system in hypertensive rats. Hypertens Res 2009 32 472 480. doi: 10.1038/hr.2009.43
23. Tew GW, Lorimer EL, Berg TJ, Zhi H, Li R, Williams CL, SmgGDS regulates cell proliferation, migration, and NF-kappaB transcriptional activity in non-small cell lung carcinoma. J Biol Chem 2008 283 963 976. doi: 10.1074/jbc.M707526200
24. Satoh K, Nigro P, Zeidan A, Soe NN, Jaffré F, Oikawa M, O'Dell MR, Cui Z, Menon P, Lu Y, Mohan A, Yan C, Blaxall BC, Berk BC, Cyclophilin A promotes cardiac hypertrophy in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 2011 31 1116 1123. doi: 10.1161/ATVBAHA.110.214601
25. Satoh K, Matoba T, Suzuki J, O'Dell MR, Nigro P, Cui Z, Mohan A, Pan S, Li L, Jin ZG, Yan C, Abe J, Berk BC, Cyclophilin A mediates vascular remodeling by promoting inflammation and vascular smooth muscle cell proliferation. Circulation 2008 117 3088 3098. doi: 10.1161/CIRCULATIONAHA.107.756106
26. Funayama A, Shishido T, Netsu S, Narumi T, Kadowaki S, Takahashi H, Miyamoto T, Watanabe T, Woo CH, Abe J, Kuwahara K, Nakao K, Takeishi Y, Kubota I, Cardiac nuclear high mobility group box 1 prevents the development of cardiac hypertrophy and heart failure. Cardiovasc Res 2013 99 657 664. doi: 10.1093/cvr/cvt128
27. Lanning CC, Daddona JL, Ruiz-Velasco R, Shafer SH, Williams CL, The Rac1 C-Terminal polybasic region regulates the nuclear localization and protein degradation of Rac1. J Biol Chem 2004 279 44197 44210. doi: 10.1074/jbc.M404977200
28. Hordijk PL, Regulation of NADPH oxidases: the role of Rac proteins. Circ Res 2006 98 453 462. doi: 10.1161/01.RES.0000204727.46710.5e
29. Peng T, Lu X, Feng Q, Pivotal role of gp91phox-containing NADH oxidase in lipopolysaccharide-induced tumor necrosis factor-Alpha expression and myocardial depression. Circulation 2005 111 1637 1644. doi: 10.1161/01.CIR.0000160366.50210.E9
30. Frost JA, Steen H, Shapiro P, Lewis T, Ahn N, Shaw PE, Cobb MH, Cross-cascade activation of ERKs and ternary complex factors by Rho family proteins. EMBO J 1997 16 6426 6438. doi: 10.1093/emboj/16.21.6426
31. Liu PY, Liao JK, A method for measuring Rho kinase activity in tissues and cells. Methods Enzymol 2008 439 181 189. doi: 10.1016/S0076-6879(07)00414-4
32. Nihei T, Takahashi J, Tsuburaya R, Ito Y, Shiroto T, Hao K, Takagi Y, Matsumoto Y, Nakayama M, Miyata S, Sakata Y, Ito K, Shimokawa H, Circadian variation of Rho-kinase activity in circulating leukocytes of patients with vasospastic angina. Circ J 2014 78 1183 1190
33. Harada M, Itoh H, Nakagawa O, Ogawa Y, Miyamoto Y, Kuwahara K, Ogawa E, Igaki T, Yamashita J, Masuda I, Yoshimasa T, Tanaka I, Saito Y, Nakao K, Significance of ventricular myocytes and nonmyocytes interaction during cardiocyte hypertrophy: evidence for endothelin-1 as a paracrine hypertrophic factor from cardiac nonmyocytes. Circulation 1997 96 3737 3744
34. Valente AJ, Yoshida T, Gardner JD, Somanna N, Delafontaine P, Chandrasekar B, Interleukin-17A stimulates cardiac fibroblast proliferation and migration via negative regulation of the dual-specificity phosphatase MKP-1/DUSP-1. Cell Signal 2012 24 560 568. doi: 10.1016/j.cellsig.2011.10.010
35. Shang F, Wang J, Liu X, Li J, Zheng Q, Xue Y, Zhao L, Involvement of reactive oxygen species and JNK in increased expression of MCP-1 and infiltration of inflammatory cells in pressure-overloaded rat hearts. Mol Med Rep 2012 5 1491 1496. doi: 10.3892/mmr.2012.852
36. LaFramboise WA, Scalise D, Stoodley P, Graner SR, Guthrie RD, Magovern JA, Becich MJ, Cardiac fibroblasts influence cardiomyocyte phenotype in vitro. Am J Physiol Cell Physiol 2007 292 C1799 C1808. doi: 10.1152/ajpcell.00166.2006
37. Sano M, Fukuda K, Sato T, Kawaguchi H, Suematsu M, Matsuda S, Koyasu S, Matsui H, Yamauchi-Takihara K, Harada M, Saito Y, Ogawa S, ERK and p38 MAPK, but not NF-kappaB, are critically involved in reactive oxygen species-mediated induction of IL-6 by angiotensin II in cardiac fibroblasts. Circ Res 2001 89 661 669
38. Maack C, Kartes T, Kilter H, Schäfers HJ, Nickenig G, Böhm M, Laufs U, Oxygen free radical release in human failing myocardium is associated with increased activity of rac1-GTPase and represents a target for statin treatment. Circulation 2003 108 1567 1574. doi: 10.1161/01.CIR.0000091084.46500.BB
39. 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. doi: 10.1152/ajpheart.00327.2011
40. Shimizu T, Fukumoto Y, Tanaka S, Satoh K, Ikeda S, Shimokawa H, Crucial role of ROCK2 in vascular smooth muscle cells for hypoxia-induced pulmonary hypertension in mice. Arterioscler Thromb Vasc Biol 2013 33 2780 2791. doi: 10.1161/ATVBAHA.113.301357
41. Elias-Al-Mamun M, Satoh K, Tanaka S, Shimizu T, Nergui S, Miyata S, Fukumoto Y, Shimokawa H, Combination therapy with fasudil and sildenafil ameliorates monocrotaline-induced pulmonary hypertension and survival in rats. Circ J 2014 78 967 976
42. Hamel B, Monaghan-Benson E, Rojas RJ, Temple BR, Marston DJ, Burridge K, Sondek J, SmgGDS is a guanine nucleotide exchange factor that specifically activates RhoA and RhoC. J Biol Chem 2011 286 12141 12148. doi: 10.1074/jbc.M110.191122
43. Hauser AD, Bergom C, Schuld NJ, Chen X, Lorimer EL, Huang J, Mackinnon AC, Williams CL, The SmgGDS splice variant SmgGDS-558 is a key promoter of tumor growth and RhoA signaling in breast cancer. Mol Cancer Res 2014 12 130 142. doi: 10.1158/1541-7786.MCR-13-0362
44. 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. doi: 10.1016/j.tips.2010.12.006
45. Jin L, Ying Z, Webb RC, Activation of Rho/Rho kinase signaling pathway by reactive oxygen species in rat aorta. Am J Physiol Heart Circ Physiol 2004 287 H1495 H1500. doi: 10.1152/ajpheart.01006.2003
46. Jin L, Ying Z, Hilgers RH, Yin J, Zhao X, Imig JD, Webb RC, Increased RhoA/Rho-kinase signaling mediates spontaneous tone in aorta from angiotensin II-induced hypertensive rats. J Pharmacol Exp Ther 2006 318 288 295. doi: 10.1124/jpet.105.100735
47. Bailey SR, Mitra S, Flavahan S, Flavahan NA, Reactive oxygen species from smooth muscle mitochondria initiate cold-induced constriction of cutaneous arteries. Am J Physiol Heart Circ Physiol 2005 289 H243 H250. doi: 10.1152/ajpheart.01305.2004
48. Frost JA, Xu S, Hutchison MR, Marcus S, Cobb MH, Actions of Rho family small G proteins and p21-Activated protein kinases on mitogen-Activated protein kinase family members. Mol Cell Biol 1996 16 3707 3713
49. Clerk A, Pham FH, Fuller SJ, Sahai E, Aktories K, Marais R, Marshall C, Sugden PH, Regulation of mitogen-Activated protein kinases in cardiac myocytes through the small G protein Rac1. Mol Cell Biol 2001 21 1173 1184. doi: 10.1128/MCB.21.4.1173-1184.2001
50. de Jong JW, Schoemaker RG, de Jonge R, Bernocchi P, Keijzer E, Harrison R, Sharma HS, Ceconi C, Enhanced expression and activity of xanthine oxidoreductase in the failing heart. J Mol Cell Cardiol 2000 32 2083 2089. doi: 10.1006/jmcc.2000.1240
51. Kannan S, Muthusamy VR, Whitehead KJ, Wang L, Gomes AV, Litwin SE, Kensler TW, Abel ED, Hoidal JR, Rajasekaran NS, Nrf2 deficiency prevents reductive stress-induced hypertrophic cardiomyopathy. Cardiovasc Res 2013 100 63 73. doi: 10.1093/cvr/cvt150
52. Wang G, Hamid T, Keith RJ, Cardioprotective and antiapoptotic effects of heme oxygenase-1 in the failing heart. Circulation 2010 121 1912 1925. doi: 10.1161/CIRCULATIONAHA.109.905471
53. Sano M, Fukuda K, Kodama H, Pan J, Saito M, Matsuzaki J, Takahashi T, Makino S, Kato T, Ogawa S, Interleukin-6 family of cytokines mediate angiotensin II-induced cardiac hypertrophy in rodent cardiomyocytes. J Biol Chem 2000 275 29717 29723. doi: 10.1074/jbc.M003128200
54. Liu Y, Zhu H, Su Z, Sun C, Yin J, Yuan H, Sandoghchian S, Jiao Z, Wang S, Xu H, IL-17 contributes to cardiac fibrosis following experimental autoimmune myocarditis by a PKCβ/Erk1/2/NF-κB-dependent signaling pathway. Int Immunol 2012 24 605 612. doi: 10.1093/intimm/dxs056
55. The Lipid Study Group Prevention of cardiovascular events and death with pravastatin in patients with coronary heart disease and a broad range of initial cholesterol levels. The long-Term intervention with pravastatin in ischaemic disease (LIPID) study group. N Engl J Med 1998 339 1349 1357
56. Fichtlscherer S, Schmidt-Lucke C, Bojunga S, Rössig L, Heeschen C, Dimmeler S, Zeiher AM, Differential effects of short-Term lipid lowering with ezetimibe and statins on endothelial function in patients with CAD: clinical evidence for 'pleiotropic' functions of statin therapy. Eur Heart J 2006 27 1182 1190. doi: 10.1093/eurheartj/ehi881