Statins protect human aortic smooth muscle cells from inorganic phosphate-induced calcification by restoring Gas6-Axl survival pathway

Circulation Research

Volumn 98, Issue 8, 2006, Pages 1024-1031

  Son, Bo Kyung ^a   Kozaki, Koichi ^a,c   Iijima, Katsuya ^a   Eto, Masato ^a   Kojima, Taro ^a   Ota, Hidetaka ^a   Senda, Yuka ^a   Maemura, Koji ^a   Nakano, Toru ^b   Akishita, Masahiro ^a   Ouchi, Yasuyoshi ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b SHIONOGI AND CO LTD   (Japan)

^c KYORIN UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Apoptosis; Axl; Calcification; Gas6; Statins

Indexed keywords

ATORVASTATIN; COMPLEMENTARY DNA; DACTINOMYCIN; FLUINDOSTATIN; GROWTH ARREST SPECIFIC PROTEIN 6; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; MESSENGER RNA; PHOSPHATE; PRAVASTATIN; RECOMBINANT PROTEIN; SMALL INTERFERING RNA; TYROSINE KINASE RECEPTOR;

AORTA; APOPTOSIS; ARTERY CALCIFICATION; ARTICLE; CELL CULTURE; CONTROLLED STUDY; CORONARY ARTERY; DOSE RESPONSE; DRUG EFFECT; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VASCULAR SMOOTH MUSCLE;

AORTA; APOPTOSIS; CALCINOSIS; DNA PRIMERS; HEPTANOIC ACIDS; HUMANS; HYDROXYMETHYLGLUTARYL-COA REDUCTASE INHIBITORS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MUSCLE, SMOOTH, VASCULAR; ONCOGENE PROTEINS; PHOSPHATES; PYRROLES; RECEPTOR PROTEIN-TYROSINE KINASES; RNA, MESSENGER; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 33646799150     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.RES.0000218859.90970.8d     Document Type: Article

References (42)

1. Eggen DA. Relationship of calcified lesions to clinically significant atherosclerotic lesions. Ann N Y Acad Sci. 1968;149:752-767.
2. Wexler L, Brundage B, Crouse J, Detrano R, Fuster V, Maddahi J, Rumberger J, Stanford W, White R, Taubert K. Coronary artery calcification: pathophysiology, epidemiology, imaging methods, and clinical implications. A statement for health professionals from the American Heart Association Writing Group. Circulation. 1996;94:1175-1192.
3. Mullen MJ, Wright D, Donald AE, Thorne S, Thomson H, Deanfield JE. Atorvastatin but not L-arginine improves endothelial function in type-I diabetes mellitus: a double-blind study. J Am Coll Cardiol. 2000;36:410-416.
4. Bustos C, Hernandez-Presa MA. Ortego M, Tunon J, Ortega L, Perez F, Diaz C, Hernandez G, Egido J. HMG-CoA reductase inhibition by atorvastatin reduces neointimal inflammation in a rabbit model of atherosclerosis. J Am Coll Cardiol. 1998;32:2057-2064.
5. Axel DI, Riessen R, Runge H, Viebahn R, Karsch KR. Effects of cerivastatin on human arterial smooth muscle cell proliferation and migration in transfilter cocultures. J Cardiovasc Pharmacot. 2000;35:619-629.
6. Shavelle DM, Takasu J, Budoff MJ, Mao S, Zhao XQ, O'Brien KD. HMG CoA reductase inhibitor (statin) and aortic valve calcium. Lancet. 2002;359:1125-1126.
7. Novaro GM, Tiong IY, Pearce GL, Lauer MS, Sprecher DL, Griffin BP. Effect of hydroxymethylglutaryl coenzyme A reductase inhibitors on the progression of calcific aortic stenosis. Circulation. 2001;104:2205-2209.
8. Achenbach S, Ropers D, Pohle K, Leber A, Thilo C, Knez A, Menendez T, Maeffert R, Kusus M, Regenfus M, Bickel A, Haberl R, Steinbeck G, Moshage W, Daniel WG. Influence of lipid-lowering therapy on the progression of coronary artery calcification: a prospective evaluation. Circulation. 2002;106:1077-1082.
9. Callister TQ, Raggi P, Cooil B, Lippolis NJ, Russo DJ. Effect of HMG-CoA reductase inhibitors on coronary artery disease as assessed by electron-beam computed tomography. N Engl J Med. 1998;339:1972-1978.
10. Williams JK, Sukhova GK, Herrington DM, Libby P. Pravastatin has cholesterol-lowering independent effects on the artery wall of atherosclerotic monkeys. J Am Coll Cardiol. 1998;31:684-691.
11. Bea F, Blessing E, Bennett B, Levitz M, Wallace EP, Rosenfeld ME. Simvastatin promotes atherosclerotic plaque stability in apoE-deficient mice independently of lipid lowering. Arterioscler Thromb Vasc Biol. 2002;22:1832-1837.
12. Cowell SJ, Newby DE, Prescott RJ, Bloomfield P, Reid J, Northridge DB, Boon NA. A randomized trial of intensive lipid-lowering therapy in calcific aortic stenosis. N Engl J Med. 2005;352:2389-2397.
13. Wanner C, Krane V, Marz W, Olschewski M, Mann JF, Ruf G, Ritz E. Atorvastatin in patients with type 2 diabetes mellitus undergoing hemodialysis. N Engl J Med. 2005;353:238-248.
14. Goodman WG, London G, Amann K, Block GA, Giachelli C, Hruska KA, Ketteler M, Levin A, Massy Z, McCarron DA, Raggi P, Shanahan CM, Yorioka N; Vascular Calcification Work Group. Vascular calcification in chronic kidney disease. Am J Kidney Dis. 2004;43:572-579.
15. Giachelli CM, Jono S, Shioi A, Nishizawa Y, Mori K, Morii H. Vascular calcification and inorganic phosphate. Am J Kidney Dis. 2001;38:S34-S37.
16. Proudfoot D, Skepper JN, Hegyi L, Bennett MR, Shanahan CM, Weissberg PL. Apoptosis regulates human vascular calcification by apoptotic bodies. Circ Res. 2000;87:1055-1062.
17. Mansfield K, Rajpurohit R, Shapiro IM. Extracellular phosphate ions cause apoptosis of terminally differentiated epiphyseal chondrocytes. J Cell Physiol. 1999;179:276-286.
18. Collett G, Wood A, Alexander MY, Varnum BC, Boot-Handford RP, Ohanian V, Ohanian J, Fridell YW, Canfield AE. Receptor tyrosine kinase Axl modulates the osteogenic differentiation of pericytes. Circ Res. 2003;92:1123-1129.
19. Mark MR, Chen J, Hammonds RG, Sadick M, Godowsk PJ. Characterization of Gas6, a member of the superfamily of G domain-containing proteins, as a ligand for Rse and Axl. J Biol Chem. 1996;271:9785-9789.
20. Yanagita M, Arai H, Ishii K, Nakano T, Ohashi K, Mizuno K, Varnum B, Fukatsu A, Doi T, Kita T. Gas6 regulates mesangial cell proliferation through Axl in experimental glomerulonephritis. Am J Pathol. 2001;158:1423-1432.
21. Goruppi S, Ruaro E, Schneider C. Gas6, the ligand of Axl tyrosine kinase receptor, has mitogenic and survival activities for serum starved NIH3T3 fibroblasts. Oncogene. 1996;12:471-480.
22. Nakano T, Ishimoto Y, Kishino J, Umeda M, Inoue K, Nagata K, Ohashi K, Mizuno K, Arita H. Cell adhesion to phosphatidylserine mediated by a product of growth arrest-specific gene 6. J Biol Chem. 1997;272:29411-29414.
23. Fridell YW, Villa J Jr, Attar EC, Liu ET. Gas6 induces Axl-mediated chemotaxis of vascular smooth muscle cells. J Biol Chem. 1998;273:7123-7126.
24. Ming Cao W, Murao K, Imachi H, Sato M, Nakano T, Kodama T, Sasaguri Y, Wong NC, Takahara J, Ishida T. Phosphatidylinositol 3-OH kinase-Akt/protein kinase B pathway mediates Gas6 induction of scavenger receptor a in immortalized human vascular smooth muscle cell line. Arterioscler Thromb Vasc Biol. 2001;21:1592-1597.
25. Jono S, McKee MD, Murry CE, Shioi A, Nishizawa Y, Mori K, Morii H, Giachelli CM. Phosphate regulation of vascular smooth muscle cell calcification. Circ Res. 2000;87:e10-e17.
26. Bergdahl A, Persson E, Hellstrand P, Sward K. Lovastatin induces relaxation and inhibits L-type Ca(2+) current in the rat basilar artery. Pharmacol Toxicol. 2003;93:128-134.
27. Mansfield K, Pucci B, Adams CS, Shapiro IM. Induction of apoptosis in skeletal tissues: phosphate-mediated chick chondrocyte apoptosis is calcium dependent. Calcif Tissue Int. 2003;73:161-172.
28. Weitz-Schmidt G, Welzenbach K, Brinkmann V, Kamata T, Kallen J, Bruns C, Cottens S, Takada Y, Hommel U. Statins selectively inhibit leukocyte function antigen-1 by binding to a novel regulatory integrin site. Nat Med. 2001;7:687-692.
29. Wagner AH, Gebauer M, Guldenzoph B, Hecker M. 3-Hydroxy-3-methylglutaryl coenzyme A reductase-independent inhibition of CD40 expression by atorvastatin in human endothelial cells. Arterioscler Thromb Vasc Biol. 2002;22:1784-1789.
30. Weis M, Heeschen C, Glassford AJ, Cooke JP. Statins have biphasic effects on angiogenesis. Circulation. 2002;105:739-745.
31. Bergmann MW, Rechner C, Freund C, Baurand A, El Jamali A, Dietz R. Statins inhibit reoxygenation-induced cardiomyocyte apoptosis: role for glycogen synthase kinase 3β and transcription factor β-catenin. J Mol Cell Cardiol. 2004;37:681-690.
32. Tanaka K, Honda M, Takabatake T. Anti-apoptotic effect of atorvastatin, a 3-hydroxy-3-methylglutaryl coenzyme a reductase inhibitor, on cardiac myocytes through protein kinase C activation. Clin Exp Pharm Phy. 2004;31:360-364.
33. Kureishi Y, Luo Z, Shiojima I, Bialik A, Fulton D, Lefer DJ, Sessa WC, Walsh K. The HMG-CoA reductase inhibitor simvastatin activates the protein kinase Akt and promotes angiogenesis in normocholesterolemic animals. Nature Med. 2000;6:1004-1010.
34. Miyashita Y, Ozaki H, Koide N, Otsuka M, Oyama T, Itoh Y, Mastuzaka T, Shirai K. Oxysterol-induced apoptosis of vascular smooth muscle cells is reduced by HMG-CoA reductase inhibitor, pravastatin. J Atheroscler Thromb. 2002;9:65-71.
35. Guijarro C, Blanco-Colio LM, Ortego M, Alonso C, Ortiz A, Plaza JJ, Diaz C, Hernandez G, Egido J. 3-Hydroxy-3 methylglutaryl coenzyme A reductase and isoprenylation inhibitors induce apoptosis of vascular smooth muscle cells in culture. Circ Res. 1998;83:490-500.
36. Newton CJ, Ran G, Xie YX, Bilko D, Burgoyne CH, Adams I, Abidia A, McCollum PT, Atkin SL. Statin-induced apoptosis of vascular endothelial cells is blocked by dexamethasone. J Endocrinol. 2002;174:7-16.
37. Ogata Y, Takahashi M, Takeuchi K, Ueno S, Mano H, Ookawara S, Kobayashi E, Ikeda U, Shimada K. Fluvastatin induces apoptosis in rat neonatal cardiac myocytes: a possible mechanism of statin-attenuated cardiac hypertrophy. J Cardiovasc Pharmacol. 2002;40:907-915.
38. Ishimoto Y, Ohashi K, Mizuno K, Nakano T. Promotion of the uptake of PS liposomes and apoptotic cells by a product of growth arrest-specific gene, gas6. J Biochem (Tokyo). 2000;127:411-417.
39. Cotmore JM, Nichols G Jr, Wuthier RE. Phospholipid-calcium phosphate complex: enhanced calcium migration in the presence of phosphate. Science. 1971;172:1339-1341.
40. Skrtic D, Eanes ED. Membrane mediated precipitation of calcium phosphate in model liposomes with matrix vesicle-like lipid composition. Bone Miner. 1992;16:109-119.
41. Walter DH, Zeiher AM, Dimmeler S. Effects of statins on endothelium and their contribution to neovascularization by mobilization of endothelial progenitor cells. Coron Artery Dis. 2004;15:235-242.
42. Menschikowski M, Hagelgans A, Heyne B, Hempel U, Neumeister V, Goez P, Jaross W, Siegert G. Statins potentiate the IFN-gamma-induced upregulation of group IIA phospholipase A2 in human aortic smooth muscle cells and HepG2 hepatoma cells. Biochim Biophys Acta. 2005;1733:157-171.