Statins up-regulate SmgGDS through β1-integrin/Akt1 pathway in endothelial cells

Cardiovascular Research

Volumn 109, Issue 1, 2016, Pages 151-161

  Minami, Tatsuro ^a,b   Satoh, Kimio ^a   Nogi, Masamichi ^a   Kudo, Shun ^a   Miyata, Satoshi ^a   Tanaka, Shin Ichi ^a,b   Shimokawa, Hiroaki ^a  

^a TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b ASAHI KASEI PHARMA CORPORATION   (Japan)

Author keywords

Akt; SmgGDS; Statins; VEGF; 1 integrin

Indexed keywords

AKT1 PROTEIN; ATORVASTATIN; BETA1 INTEGRIN; CAVEOLIN 1; GTP BINDING PROTEIN DISSOCIATION STIMULATOR; GUANINE NUCLEOTIDE BINDING PROTEIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; MESSENGER RNA; PRAVASTATIN; PROTEIN KINASE B; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR 2; AKT1 PROTEIN, MOUSE; CYTOSKELETON PROTEIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; KIFAP3 PROTEIN, MOUSE; RAP1GDS1 PROTEIN, HUMAN; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DRUG EFFECT; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; UPREGULATION; VASCULAR SMOOTH MUSCLE CELL; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; CELL CULTURE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ANTIGENS, CD29; ATORVASTATIN CALCIUM; CELLS, CULTURED; CYTOSKELETAL PROTEINS; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; HYDROXYMETHYLGLUTARYL-COA REDUCTASE INHIBITORS; MICE; MICE, INBRED C57BL; PHOSPHORYLATION; PRAVASTATIN; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 84959928084     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvv253     Document Type: Article

References (59)

1. Scandinavian Simvastatin Survival Study Group. Randomized trial of cholesterol lowering in 4444 patients with coronary heart disease: the Scandinavian Survival Study (4S). Lancet 1994; 344: 1383-1389
2. Levine GN, Keaney JF Jr, Vita JA. Cholesterol reduction in cardiovascular disease. Clinical benefits and possible mechanisms. N Engl J Med 1995; 332: 512-521
3. Davignon J. Beneficial cardiovascular pleiotropic effects of statins. Circulation 2004; 109: 39-43
4. Liao JK, Laufs U. Pleiotropic effects of statins. Annu Rev Pharmacol Toxicol 2005; 45: 89-118
5. Hall A. Rho GTPases and the actin cytoskeleton. Science 1998; 279: 509-514
6. Takemoto M, Liao JK. Pleiotropic effects of 3-hydroxy-3-methylglutaryl coenzyme A reductase inhibitors. Arterioscler Thromb Vasc Biol 2001; 21: 1712-1719
7. 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
8. Brown JH, Del Re DP, Sussman M.A. Rac and Rho hall of fame: a decade of hypertrophic signaling hits. Circ Res 2006; 98: 730-742
9. 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
10. Wassmann S, Laufs U, Bäumer AT, Müller K, Konkol C, Sauer H, Böhm M, Nickenig G. Inhibition of geranylgeranylation reduces angiotensin II-mediated free radical production in vascular smooth muscle cells: Involvement of AT1 receptor expression and Rac1 GTPase. Mol Pharmacol 2001; 59: 646-654
11. Delbosc S, Cristol JP, Descomps B, Mimran A, Jover B. Simvastatin prevents angiotensin II-induced cardiac alteration and oxidative stress. Hypertension 2002; 40: 142-147
12. Wassmann S, Laufs U, Müller K, Konkol C, Ahlbory K, Bäumer AT, Linz W, Böhm M, Nickenig G. Cellular antioxidant effects of atorvastatin in vitro and in vivo. Arterioscler Thromb Vasc Biol 2002; 22: 300-305
13. 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
14. 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 SmgGDS up-regulation with a resultant Rac1 degradation and reduced oxidative stress. Arterioscler Thromb Vasc Biol 2013; 33: 1591-1600
15. Carlson TR, Hu H, Braren R, Kim YH, Wang RA. Cell-autonomous requirement for b1 integrin in endothelial cell adhesion, migration, and survival during angiogenesis in mice. Development 2008; 135: 2193-2202
16. Zovein AC, Lugue A, Turio KA, Hofmann JJ, Yee KM, Becker MS, Fassler R, Mellman I, Lane TF, Iruela-Arispe ML. b1 integrin establishes endothelial polarity and arteriolar lumen formation via Par3-dependent mechanism. Dev Cell 2010; 18: 39-51
17. Shi L, Fisslthaler B, Zippel N, Frömel T, Elgheznawy A, Heide H, Popp R, Flemin I. MicroRNA-223 Antagonizes angiogenesis by targeting b1 integrin and preventing growth factor signaling in endothelial cells. Circ Res 2013; 113: 1320-1330
18. Devalliére J, Chatelais M, Fitau J, Gérard N, Hulin P, Velazquez L, Turner CE, Charreau B. LNK (SH2B3) is key regulator of integrin signaling in endothelial cells and targets a-parvin to control cell adhesion and migration. FASEB J 2012; 26: 2592-2606
19. Ménard C, Pupier S, Mornet D, Kitzmann M, Nargeot J, Lory P. Modulation of L-type calcium channel expression during retinoic acid-induced differentiation of H9C2 cardiac cells. J Biol Chem 1999; 274: 29063-29070
20. Canto C, Jiang LQ, Deshmukh AS, Mataki C, Coste A, Lagouge M, Zierath JR, Auwerx J. Interdependence of AMPK and SIRT1 for metabolic adaptation to fasting and exercise in skeletal muscle. Cell Metab 2010; 11: 213-219
21. Datta SR, Brunet A, Greenberg ME. Cellular survival: a play in three Akts. Genes Dev 1999; 13: 2905-2927
22. Scheid MP, Woodgett JR. PKB/AKT: Functional insights from genetic models. Nat Rev Mol Cell Biol 2001; 2: 760-768
23. Shiojima I, Walsh K. Role of Akt signaling in vascular homeostasis and angiogenesis. Circ Res 2002; 90: 1243-1250
24. Coffer PJ, Woodgett JR. Molecular cloning and characterisation of a novel putative protein-serine kinase related to the cAMP-dependent and protein kinase C families. Eur J Biochem 1991; 201: 475-481
25. Altomare DA, Guo K, Cheng JQ, Sonoda G, Walsh K, Testa JR. Cloning, chromosomal localization and expression analysis of the mouse Akt2 oncogene. Oncogene 1995; 11: 1055-1060
26. Altomare DA, Lyons GE, Mitsuuchi Y, Cheng JQ, Testa JR. Akt2 mRNA is highly expressed in embryonic brown fat and the Akt2 kinase is activated in insulin. Oncogene 1998; 16: 2407-2411
27. Brodbeck D, Cron P, Hemmings BA. A human protein kinase Bg with regulatory phosphorylation site in the activation loop and in the C-terminal hydrophobic domain. J Biol Chem 1999; 274: 9133-9136
28. Van Vliet AK, Van Thiel GC, Huisman RH, Moshage H, Yap SH, Cohen LH. Different effects of 3-hydroxy-3-methylglutaryl-coenzyme A reductase inhibitors on sterol synthesis in various human cell types. Biochim Biophys Acta 1995; 1254: 105-111
29. Gerber HP, McMurtrey A, Kowalski J, Yan M, Keyt BA, Dixit V, Ferrara N. Vascular endothelial growth factor regulates endothelial cell survival through the phosphatidylinositol 3'-kinase/Akt signal transduction pathway: Requirement for Flk-1/KDR activation. J Biol Chem 1998; 273: 30336-30343
30. Gonzalez E, Nagiel A, Lin AJ, Golan DE, Michel T. Small interfering RNA mediated down-regulation of caveolin-1 differentially modulates signaling pathways in endothelial cells. J Biol Chem 2004; 279: 40659-40669
31. Yao R, Cooper GM. Requirement for phosphatidylinositol-3 kinase in the prevention of apoptosis by nerve growth factor. Science 1995; 267: 2003-2006
32. Franke TF, Yang SI, Chan TO, Datta K, Kazlauskas A, Morrison DK, Kaplan DR, Tsichilis PN. The protein kinase encoded by the Akt proto-oncogene is a target of the PDGF-activated phosphatidylinositol-3 kinase. Cell 1995; 81: 727-736
33. Wang Q, Somwar R, Bilan PJ, Liu Z, Jin J, Woodgett JR, Klip A. Protein kinase B/Akt participates in GLUT4 translocation by insulin in L6 myoblast. Mol Cell Biol 1999; 19: 4008-4018
34. Cross DA, Alessi DR, Cohen P, Andjelkovich M, Hemmings BA. Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 1995; 378: 785-789
35. Mayo LD, Donner DB. A phosphatidylinositol 3-kinase/Akt pathway promotes translocation of Mdm2 from the cytoplasm to the nucleus. Proc Natl Acad Sci USA 2001; 98: 11598-11603
36. Rössig L, Badorff C, Holzmann Y, Zeiher AM, Dimmeler S. Glycogen synthase kinase-3 couples Akt-dependent signaling to the regulation of p21Cip1 degradation. J Biol Chem 2002; 277: 9684-9689
37. Shah OJ, Anthony JC, Kimball SR, Jefferson LS. 4E-BP1 and S6K1: translational integration sites for nutritional and hormonal information in muscle. Am J Physiol 2000; 279: E715-E729
38. Pullen N, Dennis PB, Andjelkovic M, Dufner A, Kozma SC, Hemmings BA, Thomas G. Phosphorylation and activation of p70s6k by PDK1. Science 1998; 279: 707-710
39. Alon T, Hemo I, Itin A, Pèer J, Stone J, Keshet E. Vascular endothelial growth factor acts as a survival factor for newly formed retinal vessels and has implications for retinopathy of prematurity. Nat Med 1995; 1: 1024-1028
40. Fujio Y, Walsh K. Akt mediates cytoprotection of endothelial cells by vascular endothelial growth factor in an anchorage-dependent manner. J Biol Chem 1999; 274: 16349-16354
41. Rothberg KG, Heuser JE, Donzell WC, Ying YS, Glenney JR, Anderson RG. Caveolin, a protein component of caveolae membrane coats. Cell 1992; 68: 673-682
42. Sedding DG, Hermsen J, Seay U, Eickelberg O, Kummer W, Schwencke C, Strasser H, Tillmanns H, Braun-Dullaeus RC. Caveolin-1 facilitates mechanosensitive protein kinase B (Akt) signaling in vitro and in vivo. Circ Res 2005; 96: 635-642
43. Parmar KM, Nambudiri V, Dai G, Larman HB, Gimbrone MA Jr, García-Cardeña G. Statins exert endothelial atheroprotective effects via the KLF2 transcription factor. J Biol Chem 2005; 280: 26714-26719
44. Sen-Banerjee S, Mir S, Lin Z, Hamik A, Atkins GB, Das H, Banerjee P, Kumar A, Jain MK. Kruppel-like factor 2 as a novel mediator of statin effects in endothelial cells. Circulation 2005; 112: 720-726
45. Ali F, Hamdulay SS, Kinderlerer AR, Boyle JJ, Lidington EA, Yamaguchi T, Soares MP, Haskard DO, Randi AM, Mason JC. Statin-mediated cytoprotection of human vascular endothelial cells: a role for Kruppel-like factor 2-dependent induction of heme oxygenase-1. J Thromb Haemost 2007; 5: 2537-2546
46. Tuomisto TT, Lumivuori H, Kansanen E, Häkkinen SK, Turunen MP, Van Thienen JV, Horrevoets AJ, Levonen AL, Ylä-Herttuala S. Simvastatin has an anti-inflammatory effect on macrophages via upregulation of an atheroprotective transcription factor, Kruppel-like factor 2. Cardiovasc Res 2008; 78: 175-184
47. Rhee WJ, Ni CW, Zheng Z, Chang K, Jo H, Bao G. HuR regulates the expression of stress-sensitive genes and mediates inflammatory response in human umbilical vein endothelial cells. Proc Natl Acad Sci USA 2010; 107: 6858-6863
48. Murata T, Kinoshita K, Hori M, Kuwahara M, Tsubone H, Karaki H, Ozaki H. Statin protects endothelial nitric oxide synthase activity in hypoxia-induced pulmonary hypertension. Arterioscler Thromb Vasc Biol 2005; 25: 2335-2342
49. Shimokawa H, Satoh K. 2015 ATVB Plenary Lecture: translational research on rhokinase in cardiovascular medicine. Arterioscler Thromb Vasc Biol 2015; 35: 1756-1769
50. Bhullar IS, Li YS, Miao H, Zandi E, Kim M, Shyy JY, Chien S. Fluid shear stress activation of IkappaB kinase is integrin-dependent. J Biol Chem 1998; 273: 30544-30549
51. Wang Y, Miao H, Li S, Chen KD, Li YS, Yuan S, Shyy JY, Chien S. Interplay between integrins and FLK-1 in shear stress-induced signaling. Am J Physiol 2002; 283: C1540-C1547
52. Nishida T, Shimokawa H, Oi K, Tatewaki H, Uwatoku T, Abe K, Matsumoto Y, Kajihara N, Eto M, Matsuda T, Yasui H, Takeshita A, Sunagawa K. Extracorporeal cardiac shock wave therapy markedly ameliorates ischemia-induced myocardial dysfunction in pigs in vivo. Circulation 2004; 110: 3055-3061
53. Uwatoku T, Ito K, Abe K, Oi K, Hizume T, Sunagawa K, Shimokawa H. Extracorporeal cardiac shock wave therapy improves left ventricular remodeling after acute myocardial infarction in pigs. Coron Artery Dis 2007; 18: 397-404
54. Fukumoto Y, Ito A, Uwatoku T, Matoba T, Kishi T, Tanaka H, Takeshita A, Sunagawa K, Shimokawa H. Extracorporeal cardiac shock wave therapy ameliorates myocardial ischemia in patients with severe coronary artery disease. Coron Artery Dis 2006; 17: 63-70
55. Kikuchi Y, Ito K, Ito Y, Shiroto T, Tsuburaya R, Aizawa K, Hao K, Fukumoto Y, Takahashi J, Takeda M, Nakayama M, Yasuda S, Kuriyama S, Tsuji I, Shimokawa H. Double-blind and placebo-controlled study of the effectiveness and safety of extracorporeal cardiac shock wave therapy for severe angina pectoris. Circ J 2010; 74: 589-591
56. Hanawa K, Ito K, Aizawa K, Shindo T, Nishimiya K, Hasebe Y, Tuburaya R, Hasegawa H, Yasuda S, Kanai H, Shimokawa H. Low-intensity pulsed ultrasound induces angiogenesis and ameliorates left ventricular dysfunction in a porcine model of chronic myocardial ischemia. PLoS One 2014; 9: e104863
57. Tang CH, Lu DY, Tan TW, Fu WM, Yang RS. Ultrasound induces hypoxia-inducible factor-1 activation and inducible nitric-oxide synthase expression through the integrin/integrin-linked kinase/Akt/mammalian target of rapamycin pathway in osteoblasts. J Biol Chem 2007; 282: 25406-25415
58. Watabe H, Furuhama T, Tani-Ishii N, Mikuni-Takagaki Y. Mechanotransduction activates a3b1 integrin and PI3K/Akt signaling pathways in mandibular osteoblasts. Exp Cell Res 2011; 317: 2642-2649
59. Whitney NP, Lamb AC, Louw TM, Subramanian A. Integrin-mediated mechanotransduction pathway of low-intensity continuous ultrasound in human chondrocytes. Ultrasound Med Biol 2012; 38: 1734-1743