Oxidized phospholipids induce phenotypic switching of vascular smooth muscle cells in vivo and in vitro

Circulation Research

Volumn 101, Issue 8, 2007, Pages 792-801

  Pidkovka, Nataliya A ^a   Cherepanova, Olga A ^a   Yoshida, Tadashi ^a   Alexander, Matthew R ^a   Deaton, Rebecca A ^a   Thomas, James A ^a   Leitinger, Norbert ^a   Owens, Gary K ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Atherosclerosis; Oxidized phospholipids; Smooth muscle cell phenotypic switching

Indexed keywords

1 PALMITOYL 2 ARACHIDONOYL SN GLYCERO 3 PHOSPHORYLCHOLINE; 1 PALMITOYL 2 GLUTAROYL SN GLYCERO 3 PHOSPHOCHOLINE; 1 PALMYTOYL 2 (5 OXOVALEROYL)SN GLYCERO 3 PHOSPHOCHOLINE; ALPHA ACTIN; CYTOLYSIN; KRUPPEL LIKE FACTOR 4; MONOCYTE CHEMOTACTIC PROTEIN 1; MONOCYTE CHEMOTACTIC PROTEIN 3; MYOSIN HEAVY CHAIN; PHOSPHOLIPID DERIVATIVE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; KRUPPEL LIKE FACTOR; PHOSPHOLIPID;

ANALYTIC METHOD; ANIMAL CELL; ARTICLE; ATHEROSCLEROTIC CARDIOVASCULAR DISEASE; CELL DIFFERENTIATION; CONTROLLED STUDY; DISEASE COURSE; MARKER GENE; NONHUMAN; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; RAT; VASCULAR SMOOTH MUSCLE; ANIMAL; BIOSYNTHESIS; CELL CULTURE; COMPARATIVE STUDY; CYTOLOGY; GENETICS; METABOLISM; OXIDATION REDUCTION REACTION; PHYSIOLOGY; SMOOTH MUSCLE FIBER;

ANIMALS; CELLS, CULTURED; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; OXIDATION-REDUCTION; PHENOTYPE; PHOSPHOLIPIDS; RATS;

EID: 35448965633     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.107.152736     Document Type: Article

References (42)

1. Owens GK, Kumar MS, Wamhoff BR. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol Rev. 2004;84:767-801.
2. Libby P, Theroux P. Pathophysiology of coronary artery disease. Circulation. 2005;111:3481-3488.
3. Tsimikas S, Aikawa M, Miller FJ Jr, Miller ER, Torzewski M, Lentz SR, Bergmark C, Heistad DD, Libby P, Witztum JL. Increased plasma oxidized phospholipid:apolipoprotein B-100 ratio with concomitant depletion of oxidized phospholipids from atherosclerotic lesions after dietary lipid-lowering: a potential biomarker of early atherosclerosis regression. Arterioscler Thromb Vasc Biol. 2007;27:175-181.
4. Berliner J, Leitinger N, Watson A, Huber J, Fogelman A, Navab M. Oxidized lipids in atherogenesis: formation, destruction and action. Thromb Haemost. 1997;78:195-199.
5. Berliner JA, Subbanagounder G, Leitinger N, Watson AD, Vora D. Evidence for a role of phospholipid oxidation products in atherogenesis. Trends Cardiovasc Med. 2001;11:142-147.
6. Liao F, Berliner JA, Mehrabian M, Navab M, Demer LL, Lusis AJ, Fogelman AM. Minimally modified low density lipoprotein is biologically active in vivo in mice. J Clin Invest. 1991;87:2253-2257.
7. Furnkranz A, Leitinger N. Regulation of inflammatory responses by oxidized phospholipids: structure-function relationships. Curr Pharm Des. 2004;10:915-921.
8. Furnkranz A, Schober A, Bochkov VN, Bashtrykov P, Kronke G, Kadl A, Binder BR, Weber C, Leitinger N. Oxidized phospholipids trigger atherogenic inflammation in murine arteries. Arterioscler Thromb Vasc Biol. 2005;25:633-638.
9. Watson AD, Navab M, Hama SY, Sevanian A, Prescott SM, Stafforini DM, McIntyre TM, Du BN, Fogelman AM, Berliner JA. Effect of platelet activating factor-acetylhydrolase on the formation and action of minimally oxidized low density lipoprotein. J Clin Invest. 1995;95:774-782.
10. Watson AD, Berliner JA, Hama SY, La Du BN, Faull KF, Fogelman AM, Navab M. Protective effect of high density lipoprotein associated paraoxonase. Inhibition of the biological activity of minimally oxidized low density lipoprotein. J Clin Invest. 1995;96:2882-2891.
11. Watson AD, Leitinger N, Navab M, Faull KF, Horkko S, Witztum JL, Palinski W, Schwenke D, Salomon RG, Sha W, Subbanagounder G, Fogelman AM, Berliner JA. Structural identification by mass spectrometry of oxidized phospholipids in minimally oxidized low density lipoprotein that induce monocyte/endothelial interactions and evidence for their presence in vivo. J Biol Chem. 1997;272:13597-13607.
12. Watson AD, Subbanagounder G, Welsbie DS, Faull KF, Navab M, Jung ME, Fogelman AM, Berliner JA. Structural identification of a novel pro-inflammatory epoxyisoprostane phospholipid in mildly oxidized low density lipoprotein. J Biol Chem. 1999;274:24787-24798.
13. Leitinger N, Watson AD, Hama SY, Ivandic B, Qiao JH, Huber J, Faull KF, Grass DS, Navab M, Fogelman AM, de Beer FC, Lusis AJ, Berliner JA. Role of group II secretory phospholipase A2 in atherosclerosis: 2. Potential involvement of biologically active oxidized phospholipids. Arterioscler Thromb Vasc Biol. 1999;19:1291-1298.
14. Berliner JA, Navab M, Fogelman AM, Frank JS, Demer LL, Edwards PA, Watson AD, Lusis AJ. Atherosclerosis: basic mechanisms. Oxidation, inflammation, and genetics. Circulation. 1995;91:2488-2496.
15. Yeh M, Leitinger N, de Martin R, Onai N, Matsushima K, Vora DK, Berliner JA, Reddy ST. Increased transcription of IL-8 in endothelial cells is differentially regulated by TNF-α and oxidized phospholipids. Arterioscler Thromb Vasc Biol. 2001;21:1585-1591.
16. Berliner JA, Watson AD. A role for oxidized phospholipids in atherosclerosis. N Engl J Med. 2005;353:9-11.
17. Fruhwirth GO, Moumtzi A, Loidl A, Ingolic E, Hermetter A. The oxidized phospholipids POVPC and PGPC inhibit growth and induce apoptosis in vascular smooth muscle cells. Biochim Biophys Acta. 1761(9):1060-1069, 2006; Sep.
18. Shimizu RT, Blank RS, Jervis R, Lawrenz-Smith SC, Owens GK. The smooth muscle alpha-actin gene promoter is differentially regulated in smooth muscle versus non-smooth muscle cells. J Biol Chem. 1995;270: 7631-7643.
19. Navab M, Ananthramaiah GM, Reddy ST, Van Lenten BJ, Ansell BJ, Fonarow GC, Vahabzadeh K, Hama S, Hough G, Kamranpour N, Berliner JA, Lusis AJ, Fogelman AM. The oxidation hypothesis of atherogenesis: the role of oxidized phospholipids and HDL. J Lipid Res. 2004;45:993-1007.
20. Isakson BE, Kronke G, Kadl A, Leitinger N, Duling BR. Oxidized phospholipids alter vascular connexin expression, phosphorylation, and heterocellular communication. Arterioscler Thromb Vasc Biol. 2006; 2216-2221.
21. Liu Y, Sinha S, McDonald OG, Shang Y, Hoofnagle MH, Owens GK. Kruppel-like factor 4 abrogates myocardin-induced activation of smooth muscle gene expression. J Biol Chem. 2005;280:9719-9727.
22. McDonald OG, Wamhoff BR, Hoofnagle MH, Owens GK. Control of SRF binding to CArG box chromatin regulates smooth muscle gene expression in vivo. J Clin Invest. 2006;116:36-48.
23. Katz JP. The zinc-finger transcription factor Klf4 is required for terminal differentiation of goblet cells in the colon. Development. 2002;129: 2619-2628.
24. Kronke G, Bochkov VN, Huber J, Gruber F, Bluml S, Furnkranz A, Kadl A, Binder BR, Leitinger N. Oxidized phospholipids induce expression of human heme oxygenase-1 involving activation of cAMP-responsive element-binding protein. J Biol Chem. 2003;278:51006-51014.
25. Leitinger N, Watson AD, Faull KF, Fogelman AM, Berliner JA. Monocyte binding to endothelial cells induced by oxidized phospholipids present in minimally oxidized low density lipoprotein is inhibited by a platelet activating factor receptor antagonist. Adv Exp Med Biol. 1997; 433:379-382.
26. Leitinger N, Tyner TR, Oslund L, Rizza C, Subbanagounder G, Lee H, Shih PT, Mackman N, Tigyi G, Territo MC, Berliner JA, Vora DK. Structurally similar oxidized phospholipids differentially regulate endothelial binding of monocytes and neutrophils. Proc Natl Acad Sci U S A. 1999;96:12010-12015.
27. Bochkov VN, Philippova M, Oskolkova O, Kadl A, Furnkranz A, Karabeg E, Afonyushkin T, Gruber F, Breuss J, Minchenko A, Mechtcheriakova D, Hohensinner P, Rychli K, Wojta J, Resink T, Erne P, Binder BR, Leitinger N. Oxidized phospholipids stimulate angiogenesis via autocrine mechanisms, implicating a novel role for lipid oxidation in the evolution of atherosclerotic lesions. Circ Res. 2006;99:900-908.
28. Adam PJ, Regan CP, Hautmann MB, Owens GK. Positive- and negative-acting Kruppel-like transcription factors bind a transforming growth factor beta control element required for expression of the smooth muscle cell differentiation marker SM22alpha in vivo. J Biol Chem. 2000;275: 37798-37806.
29. Liu Y, Sinha S, Owens G. A transforming growth factor-beta control element required for SM alpha-actin expression in vivo also partially mediates GKLF-dependent transcriptional repression. J Biol Chem. 2003; 278:48004-48011.
30. Regan CP, Adam PJ, Madsen CS, Owens GK. Molecular mechanisms of decreased smooth muscle differentiation marker expression after vascular injury. J Clin Invest. 2000;106:1139-1147.
31. Wamhoff BR, Hoofnagle MH, Burns A, Sinha S, McDonald OG, Owens GK. A G/C element mediates repression of the SM22alpha promoter within phenotypically modulated smooth muscle cells in experimental atherosclerosis. Circ Res. 2004;95:981-988.
32. Shields JM, Christy RJ, Yang VW. Identification and characterization of a gene encoding a gut-enriched Kruppel-like factor expressed during growth arrest. J Biol Chem. 1996;271:20009-20017.
33. Madsen CS, Regan CP, Owens GK. Interaction of CArG elements and a GC-rich repressor element in transcriptional regulation of the smooth muscle myosin heavy chain gene in vascular smooth muscle cells. J Biol Chem. 1997;272:29842-29851.
34. Madsen CS, Hershey JC, Hautmann MB, White SL, Owens GK. Expression of the smooth muscle myosin heavy chain gene is regulated by a negative-acting GC-rich element located between two positive-acting serum response factor-binding elements. J Biol Chem. 1997;272:6332-6340.
35. Creemers EE, Sutherland LB, McAnally J, Richardson JA, Olson EN. Myocardin is a direct transcriptional target of Mef2, Tead and Foxo proteins during cardiovascular development. Development. 2006;133: 4245-4256.
36. Kawai-Kowase K, Owens GK. Multiple repressor pathways contribute to phenotypic switching of vascular smooth muscle cells. Am J Physiol Cell Physiol. 2007;292:C59-C69.
37. Yoshida T, Sinha S, Dandre F, Wamhoff BR, Hoofnagle MH, Kremer BE, Wang DZ, Olson EN, Owens GK. Myocardin is a key regulator of CArG-dependent transcription of multiple smooth muscle marker genes. Circ Res. 2003;92:856-864.
38. Yoshida T, Owens GK. Molecular determinants of vascular smooth muscle cell diversity. Circ Res. 2005;96:280-291.
39. Yoshida T, Gan Q, Shang Y, Owens GK. Platelet-derived growth factor-BB represses smooth muscle cell marker genes via changes in binding of MKL factors and histone deacetylases to their promoters. Am J Physiol Cell Physiol. 2007;292:C886-C895.
40. Chen J, Kitchen CM, Streb JW, Miano JM. Myocardin: a component of a molecular switch for smooth muscle differentiation. J Mol Cell Cardiol. 2002;34:1345-1356.
41. Wang Z, Wang DZ, Hockemeyer D, McAnally J, Nordheim A, Olson EN. Myocardin and ternary complex factors compete for SRF to control smooth muscle gene expression. Nature. 2004;428:185-189.
42. Milne GL, Seal JR, Havrilla CM, Wijtmans M, Porter NA. Identification and analysis of products formed from phospholipids in the free radical oxidation of human low density lipoproteins. J Lipid Res. 2005;46: 307-319.