7-Ketocholesterol and cholesterol-5α,6α-epoxide induce smooth muscle cell migration and proliferation through the epidermal growth factor receptor/phosphoinositide 3-kinase/Akt signaling pathways

Toxicology Letters

Volumn 197, Issue 2, 2010, Pages 88-96

  Liao, Po Lin ^a   Cheng, Yu Wen ^b   Li, Ching Hao ^a   Wang, Yan Ting ^b   Kang, Jaw Jou ^a  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b TAIPEI MEDICAL UNIVERSITY   (Taiwan)

Author keywords

Atherosclerosis; Epidermal growth factor receptor; Oxysterols; Smooth muscle cell

Indexed keywords

7 OXOCHOLESTEROL; CERAMIDE; CHOLESTEROL 5ALPHA,6ALPHA OXIDE; EPIDERMAL GROWTH FACTOR RECEPTOR; GELATINASE A; GELATINASE B; MAMMALIAN TARGET OF RAPAMYCIN; OXYSTEROL; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SPHINGOMYELIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; ATHEROGENESIS; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVITY; GENE EXPRESSION; IMMUNOPRECIPITATION; MITOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; VASCULAR SMOOTH MUSCLE; WESTERN BLOTTING;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; AORTA; CELL MOVEMENT; CELL PROLIFERATION; CERAMIDES; CHOLESTEROL; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; KETOCHOLESTEROLS; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RECEPTOR, EPIDERMAL GROWTH FACTOR; RNA, MESSENGER; SIGNAL TRANSDUCTION; SPHINGOMYELINS;

EID: 77953959947     PISSN: 03784274     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.toxlet.2010.05.002     Document Type: Article

References (55)

1. Addis P.B. Occurrence of lipid oxidation products in foods. Food Chem. Toxicol. 1986, 24:1021-1030.
2. Addis P.B., Emanuel H.A., Bergmann S.D., Zavoral J.H. Capillary GC quantification of cholesterol oxidation products in plasma lipoproteins of fasted humans. Free Radical Biol. Med. 1989, 7:179-182.
3. Allen L.B., Capps B.E., Miller E.C., Clemmons D.R., Maile L.A. Glucose-oxidized low-density lipoproteins enhance insulin-like growth factor I-stimulated smooth muscle cell proliferation by inhibiting integrin-associated protein cleavage. Endocrinology 2009, 150:1321-1329.
4. Auge N., Garcia V., Maupas-Schwalm F., Levade T., Salvayre R., Negre-Salvayre A. Oxidized LDL-induced smooth muscle cell proliferation involves the EGF receptor/PI-3 kinase/Akt and the sphingolipid signaling pathways. Arterioscler. Thromb. Vasc. Biol. 2002, 22:1990-1995.
5. Auge N., Maupas-Schwalm F., Elbaz M., Thiers J.C., Waysbort A., Itohara S., Krell H.W., Salvayre R., Negre-Salvayre A. Role for matrix metalloproteinase-2 in oxidized low-density lipoprotein-induced activation of the sphingomyelin/ceramide pathway and smooth muscle cell proliferation. Circulation 2004, 110:571-578.
6. Bachem M.G., Wendelin D., Schneiderhan W., Haug C., Zorn U., Gross H.J., Schmid-Kotsas A., Grunert A. Depending on their concentration oxidized low density lipoproteins stimulate extracellular matrix synthesis or induce apoptosis in human coronary artery smooth muscle cells. Clin. Chem. Lab. Med. 1999, 37:319-326.
7. Bendeck M.P., Zempo N., Clowes A.W., Galardy R.E., Reidy M.A. Smooth muscle cell migration and matrix metalloproteinase expression after arterial injury in the rat. Circ. Res. 1994, 75:539-545.
8. Berk B.C. Redox signals that regulate the vascular response to injury. Thromb. Haemost. 1999, 82:810-817.
9. Brown A.J., Jessup W. Oxysterols and atherosclerosis. Atherosclerosis 1999, 142:1-28.
10. Buckley C., Bund S.J., McTaggart F., Bruckdorfer K.R., Oldham A., Jacobs M. Oxidized low-density lipoproteins inhibit endothelium-dependent relaxations in isolated large and small rabbit coronary arteries. J. Auton. Pharmacol. 1996, 16:261-267.
11. Carmichael J., DeGraff W.G., Gazdar A.F., Minna J.D., Mitchell J.B. Evaluation of a tetrazolium-based semiautomated colorimetric assay: assessment of radiosensitivity. Cancer Res. 1987, 47:943-946.
12. Chen C.N., Li Y.S., Yeh Y.T., Lee P.L., Usami S., Chien S., Chiu J.J. Synergistic roles of platelet-derived growth factor-BB and interleukin-1beta in phenotypic modulation of human aortic smooth muscle cells. Proc. Natl. Acad. Sci. USA 2006, 103:2665-2670.
13. Cherepanova O.A., Pidkovka N.A., Sarmento O.F., Yoshida T., Gan Q., Adiguzel E., Bendeck M.P., Berliner J., Leitinger N., Owens G.K. Oxidized phospholipids induce type VIII collagen expression and vascular smooth muscle cell migration. Circ. Res. 2009, 104:609-618.
14. Chisolm G.M., Chai Y. Regulation of cell growth by oxidized LDL. Free Radical Biol. Med. 2000, 28:1697-1707.
15. Clare K., Hardwick S.J., Carpenter K.L., Weeratunge N., Mitchinson M.J. Toxicity of oxysterols to human monocyte-macrophages. Atherosclerosis 1995, 118:67-75.
16. Clarke M.C., Figg N., Maguire J.J., Davenport A.P., Goddard M., Littlewood T.D., Bennett M.R. Apoptosis of vascular smooth muscle cells induces features of plaque vulnerability in atherosclerosis. Nat. Med. 2006, 12:1075-1080.
17. Edwards P.A., Ericsson J. Signaling molecules derived from the cholesterol biosynthetic pathway: mechanisms of action and possible roles in human disease. Curr. Opin. Lipidol. 1998, 9:433-440.
18. Estrada C.R., Adam R.M., Eaton S.H., Bagli D.J., Freeman M.R. Inhibition of EGFR signaling abrogates smooth muscle proliferation resulting from sustained distension of the urinary bladder. Lab. Invest. 2006, 86:1293-1302.
19. Galis Z.S., Khatri J.J. Matrix metalloproteinases in vascular remodeling and atherogenesis: the good, the bad, and the ugly. Circ. Res. 2002, 90:251-262.
20. Guardiola F., Codony R., Addis P.B., Rafecas M., Boatella J. Biological effects of oxysterols: current status. Food Chem. Toxicol. 1996, 34:193-211.
21. Hubbard R.W., Ono Y., Sanchez A. Atherogenic effect of oxidized products of cholesterol. Prog. Food Nutr. Sci. 1989, 13:17-44.
22. Hughes H., Mathews B., Lenz M.L., Guyton J.R. Cytotoxicity of oxidized LDL to porcine aortic smooth muscle cells is associated with the oxysterols 7-ketocholesterol and 7-hydroxycholesterol. Arterioscler. Thromb. 1994, 14:1177-1185.
23. Ikeda U., Shimada K. Matrix metalloproteinases and coronary artery diseases. Clin. Cardiol. 2003, 26:55-59.
24. Imai H., Werthessen N.T., Subramanyam V., LeQuesne P.W., Soloway A.H., Kanisawa M. Angiotoxicity of oxygenated sterols and possible precursors. Science 1980, 207:651-653.
25. Ioannou Y.A. Multidrug permeases and subcellular cholesterol transport. Nat. Rev. Mol. Cell Biol. 2001, 2:657-668.
26. Kavurma M.M., Khachigian L.M. ERK, JNK, and p38 MAP kinases differentially regulate proliferation and migration of phenotypically distinct smooth muscle cell subtypes. J. Cell Biochem. 2003, 89:289-300.
27. Kodali R., Hajjou M., Berman A.B., Bansal M.B., Zhang S., Pan J.J., Schecter A.D. Chemokines induce matrix metalloproteinase-2 through activation of epidermal growth factor receptor in arterial smooth muscle cells. Cardiovasc. Res. 2006, 69:706-715.
28. Li C.H., Tzeng S.L., Cheng Y.W., Kang J.J. Chloramphenicol-induced mitochondrial stress increases p21 expression and prevents cell apoptosis through a p21-dependent pathway. J. Biol. Chem. 2005, 280:26193-26199.
29. Liebmann C. Regulation of MAP kinase activity by peptide receptor signalling pathway: paradigms of multiplicity. Cel. Signal. 2001, 13:777-785.
30. Lordan S., Mackrill J.J., O'Brien N.M. Involvement of Fas signalling in 7beta-hydroxycholesterol-and cholesterol-5beta,6beta-epoxide-induced apoptosis. Int. J. Toxicol. 2008, 27:279-285.
31. Lusis A.J. Atherosclerosis. Nature 2000, 407:233-241.
32. Martinet W., Schrijvers D.M., Timmermans J.P., Bult H. Interactions between cell death induced by statins and 7-ketocholesterol in rabbit aorta smooth muscle cells. Brit. J. Pharmacol. 2008, 154:1236-1246.
33. Muslin A.J. MAPK signalling in cardiovascular health and disease: molecular mechanisms and therapeutic targets. Clin. Sci. (Lond) 2008, 115:203-218.
34. Nagayama K., Matsumoto T. Contribution of actin filaments and microtubules to quasi-in situ tensile properties and internal force balance of cultured smooth muscle cells on a substrate. Am. J. Physiol. Cell Physiol. 2008, 295:C1569-1578.
35. Netzel-Arnett S., Mallya S.K., Nagase H., Birkedal-Hansen H., Van Wart H.E. Continuously recording fluorescent assays optimized for five human matrix metalloproteinases. Anal. Biochem. 1991, 195:86-92.
36. Parks W.C., Wilson C.L., Lopez-Boado Y.S. Matrix metalloproteinases as modulators of inflammation and innate immunity. Nat. Rev. Immunol. 2004, 4:617-629.
37. Peng S.K., Tham P., Taylor C.B., Mikkelson B. Cytotoxicity of oxidation derivatives of cholesterol on cultured aortic smooth muscle cells and their effect on cholesterol biosynthesis. Am. J. Clin. Nutr. 1979, 32:1033-1042.
38. Pettus B.J., Chalfant C.E., Hannun Y.A. Ceramide in apoptosis: an overview and current perspectives. Biochim. Biophys. Acta 2002, 1585:114-125.
39. Ramasamy S., Boissonneault G.A., Hennig B. Oxysterol-induced endothelial cell dysfunction in culture. J. Am. Coll. Nutr. 1992, 11:532-538.
40. Renault M.A., Jalvy S., Belloc I., Pasquet S., Sena S., Olive M., Desgranges C., Gadeau A.P. AP-1 is involved in UTP-induced osteopontin expression in arterial smooth muscle cells. Circ. Res. 2003, 93:674-681.
41. Schroepfer G.J. Oxysterols: modulators of cholesterol metabolism and other processes. Physiol. Rev. 2000, 80:361-554.
42. Seye C.I., Knaapen M.W., Daret D., Desgranges C., Herman A.G., Kockx M.M., Bult H. 7-Ketocholesterol induces reversible cytochrome c release in smooth muscle cells in absence of mitochondrial swelling. Cardiovasc. Res. 2004, 64:144-153.
43. Spiegel S., Milstien S. Sphingosine-1-phosphate: an enigmatic signalling lipid. Nat. Rev. Mol. Cell Biol. 2003, 4:397-407.
44. Tsai C.S., Loh S.H., Liu J.C., Lin J.W., Chen Y.L., Chen C.H., Cheng T.H. Urotensin II-induced endothelin-1 expression and cell proliferation via epidermal growth factor receptor transactivation in rat aortic smooth muscle cells. Atherosclerosis 2009, 206:86-94.
45. Tuomainen T.P., Diczfalusy U., Kaikkonen J., Nyyssonen K., Salonen J.T. Serum ferritin concentration is associated with plasma levels of cholesterol oxidation products in man. Free Radical Biol. Med. 2003, 35:922-928.
46. Ushio-Fukai M. Vascular signaling through G protein-coupled receptors: new concepts. Curr. Opin. Nephrol. Hypertens. 2009, 18:153-159.
47. van de Bovenkamp P., Kosmeijer-Schuil T.G., Katan M.B. Quantification of oxysterols in Dutch foods: egg products and mixed diets. Lipids 1988, 23:1079-1085.
48. Vaya J., Aviram M., Mahmood S., Hayek T., Grenadir E., Hoffman A., Milo S. Selective distribution of oxysterols in atherosclerotic lesions and human plasma lipoproteins. Free Radical Res. 2001, 34:485-497.
49. Visse R., Nagase H. Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry. Circ. Res. 2003, 92:827-839.
50. Voisin L., Foisy S., Giasson E., Lambert C., Moreau P., Meloche S. EGF receptor transactivation is obligatory for protein synthesis stimulation by G protein-coupled receptors. Am. J. Physiol. Cell Physiol. 2002, 283:C446-455.
51. Wang D.Q., Afdhal N.H. Good cholesterol, bad cholesterol: role of oxysterols in biliary tract diseases. Gastroenterology 2001, 121:216-218.
52. Wang D., Paria B.C., Zhang Q., Karpurapu M., Li Q., Gerthoffer W.T., Nakaoka Y., Rao G.N. A role for Gab1/SHP2 in thrombin activation of PAK1: gene transfer of kinase-dead PAK1 inhibits injury-induced restenosis. Circ. Res. 2009, 104:1066-1075.
53. Witztum J.L., Steinberg D. The oxidative modification hypothesis of atherosclerosis: does it hold for humans?. Trends Cardiovasc. Med. 2001, 11:93-102.
54. Yoon J.H., Canbay A.E., Werneburg N.W., Lee S.P., Gores G.J. Oxysterols induce cyclooxygenase-2 expression in cholangiocytes: implications for biliary tract carcinogenesis. Hepatology 2004, 39:732-738.
55. Zhang H., Chalothorn D., Jackson L.F., Lee D.C., Faber J.E. Transactivation of epidermal growth factor receptor mediates catecholamine-induced growth of vascular smooth muscle. Circ. Res. 2004, 95:989-997.