The oxidation hypothesis of atherogenesis: The role of oxidized phospholipids and HDL

Journal of Lipid Research

Volumn 45, Issue 6, 2004, Pages 993-1007

  Navab, Mohamad ^a   Ananthramaiah, G M ^b   Reddy, Srinivasa T ^a   Van Lenten, Brian J ^a   Ansell, Benjamin J ^a   Fonarow, Gregg C ^a   Vahabzadeh, Kambiz ^a   Hama, Susan ^a   Hough, Greg ^a   Kamranpour, Naeimeh ^a   Berliner, Judith A ^a   Lusis, Aldons J ^a   Fogelman, Alan M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b University of Alabama at Birmingham   (United States)

Author keywords

Apolipoprotein A I mimetic peptides; Arachidonic acid; High density lipoprotein; Reverse cholesterol transport

Indexed keywords

ALPHA TOCOPHEROL; APOLIPOPROTEIN A1; ARACHIDONIC ACID; HIGH DENSITY LIPOPROTEIN; LIPOXYGENASE; LOW DENSITY LIPOPROTEIN; MYELOPEROXIDASE; PHOSPHOLIPID; SYNTHETIC PEPTIDE;

ATHEROGENESIS; ATHEROSCLEROSIS; CHOLESTEROL TRANSPORT; DISEASE COURSE; DISEASE PREDISPOSITION; HUMAN; HYPOTHESIS; IMMUNE SYSTEM; LIPID METABOLISM; NONHUMAN; OXIDATION; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW;

ANIMALS; ARTERIOSCLEROSIS; HUMANS; INFLAMMATION; LIPOPROTEINS, HDL; LIPOPROTEINS, LDL; OXIDATION-REDUCTION; PHOSPHOLIPIDS;

EID: 2542460047     PISSN: 00222275     EISSN: None     Source Type: Journal    
DOI: 10.1194/jlr.R400001-JLR200     Document Type: Review

References (121)

1. Hessler, J. R., A. L. Robertson, and G. M. Chisolm. 1979. LDL-induced cytotoxicity and its inhibition by HDL in human vascular smooth muscle and endothelial cells in culture. Atherosclerosis. 32: 213-229.
2. Colles, S. M., J. M. Maxson, S. G. Carlson, and G. M. Chisolm. 2001. Oxidized LDL-induced injury and apoptosis in atherosclerosis. Potential roles for oxysterols. Trends Cardiovasc. Med. 11: 131-138.
3. Goldstein, J. L., Y. K. Ho, S. K. Basu, and M. S. Brown. 1979. Binding site on macrophages that mediates uptake and degradation of acetylated low density lipoprotein, producing massive cholesterol deposition. Proc. Natl. Acad. Sci. USA. 76: 333-337.
4. Fogelman, A. M., I. Shechter, J. Seager, M. Hokom, J. S. Child, and P. A. Edwards. 1980. Malondialdehyde alteration of low density lipoproteins leads to cholesteryl ester accumulation in human monocyte-macrophages. Proc. Natl. Acad. Sci. USA. 77: 2214-2218.
5. Henricksen, T., E. M. Mahoney, and D. Steinberg. 1981. Enhanced macrophage degradation of low density lipoprotein previously incubated with cultured endothelial cells: recognition by receptor for acetylated low density lipoproteins. Proc. Natl. Acad. Sci. USA. 78: 6499-6503.
6. Morel, D. W., P. E. DiCorleto, and G. M. Chisolm. 1984. Endothelial and smooth muscle cells alter low-density lipoprotein in vitro by free radical oxidation. Arteriosclerosis. 4: 357-364.
7. Steinbrecher, U., S. Parthasarathy, D. S. Leake, J. L. Witztum, and D. Steinberg. 1984. Modification of low density lipoprotein by endothelial cells involves lipid peroxidation and degradation of low density lipoprotein phospholipids. Proc. Natl. Acad. Sci. USA. 83: 3883-3887.
8. Heinecke, J. W., H. Rosen, and A. Chait. 1984. Iron and copper promote modification of LDL by human arterial smooth muscle cells. J. Clin. Invest. 74: 1890-1894.
9. Haberland, M. E., D. Fong, and L. Cheng. 1988. Malondialdehyde altered protein occurs in atheroma of WHHL rabbits. Science. 241: 215-218.
10. Palinski, W., M. E. Rosenfeld, S. Yla-Herttuala, G. C. Gurtner, S. S. Socher, S. W. Butler, S. Parthasarathy, T. E. Carew, D. Steinberg, and J. L. Witztum. 1989. LDL undergoes oxidative modification in vivo. Proc. Natl. Acad. Sci. USA. 86: 1372-1376.
11. Yla-Herttuala, S., W. Palinski, S. Rosenfeld, S. Parthasarathy, T. E. Carew, S. Butler, J. L. Witztum, and D. Steinberg. 1989. Evidence for the presence of oxidatively modified low density lipoprotein in atherosclerotic lesions of rabbit and man. J. Clin. Invest. 84: 1086-1095.
12. Witztum, J. L., and D. Steinberg. 1991. Role of oxidized low density lipoprotein in atherogenesis. J. Clin. Invest. 88: 1785-1792.
13. Parthasarathy, S. 1994. Modified Lipoproteins in the Pathogenesis of Atherosclerosis. R. G. Landes Co., Austin, TX. 91-119.
14. Parthasarathy, S. 1994. Mechanism(s) of cell-mediated oxidation of low density lipoprotein. In Free Radicals in the Environment, Medicine and Toxicology. H. Nohl, H. Esterbauer, and C. R. Evans, editors. Richelieu Press, London. 163-179.
15. Witztum, J. L. 1994. The oxidation hypothesis of atherosclerosis. Lancet. 344: 793-795.
16. Chisolm, G. M. 1991. Antioxidants and atherosclerosis: a current assessment. Clin. Cardiol. 14: 125-130.
17. Navab, M., F. Liao, G. P. Hough, L. A. Ross, B. J. Van Lenten, T. B. Rajavashisth, A. J. Lusis, H. Laks, D. C. Drinkwater, and A. M. Fogelman. 1991. Interaction of monocytes with coculture of human aortic wall cells involves interleukins 1 and 6 with marked increases in connexin43 message. J. Clin. Invest. 87: 1763-1772.
18. Navab, M., S. S. Imes, S. Y. Hama, G. P. Hough, L. A. Ross, R. W. Bork, A. J. Valente, J. A. Berliner, D. C. Drinkwater, H. Laks, and A. M. Fogelman. 1991. Monocyte transmigration induced by modification of low density lipoprotein in cocultures of human aortic wall cells is due to induction of monocyte chemotactic protein-1 synthesis and is abolished by high density lipoprotein. J. Clin. Invest. 88: 2039-2046.
19. Napoli, C., P. F. D'Armiento, F. P. Mancini, A. Postiglione, J. L. Witztum, G. Palumbo, and W. Palinski. 1997. Fatty streak formation occurs in human fetal aortas and is greatly enhanced by maternal hypercholesterolemia: intimal accumulation of low density lipoprotein and its oxidation precede monocyte recruitment into early atherosclerotic lesions. J. Clin. Invest. 100: 2680-2690.
20. Berliner, J. A., M. C. Territo, A. Sevanian, S. Ramin, J. A. Kim, B. Bamshad, M. Esterson, and A. M. Fogelman. 1990. Minimally modified low density lipoprotein stimulates monocyte endothelial interactions. J. Clin. Invest. 85: 1260-1266.
21. Cushing, S. D., J. A. Berliner, A. J. Valente, M. C. Territo, M. Navab, F. Parhami, R. Gerrity, C. J. Schwartz, and A. M. Fogelman. 1990. Minimally modified LDL induces monocyte chemotactic protein-1 in human endothelial and smooth muscle cells. Proc. Natl. Acad. Sci. USA. 87: 5134-5138.
22. Rajavashisth, T. B., A. Andalibi, M. C. Territo, J. A. Berliner, M. Navab, A. M. Fogelman, and A. J. Lusis. 1990. Induction of endothelial cell expression of granulocyte and macrophage colony-stimulating factors by modified low density lipoproteins. Nature. 344: 254-257.
23. Schwartz, D., L. Chaverri-Almada, J. A. Berliner, T. Kirchgessener, D. C. Quismorio, Z. T. Fang, P. Tekamp-Olson, A. J. Lusis, A. M. Fogelman, and M. C. Territo. 1994. The role of a GRO homologue in monocyte adhesion to endothelium. J. Clin. Invest. 94: 1968-1973.
24. Vora, D. K., Z. T. Fang, S. M. Liva, T. R. Tyner, F. Parhami, A. D. Watson, T. A. Drake, M. C. Territo, and J. A. Berliner. 1997. Induction of P-selectin by oxidized lipoproteins. Separate effects on synthesis and surface expression. Circ. Res. 80: 810-818.
25. Cushing, S. D., and A. M. Fogelman. 1992. Monocytes may amplify their recruitment into inflammatory lesions by inducing monocyte chemotactic protein. Arterioscler. Thromb. 12: 78-82.
26. Liao, F., J. A. Berliner, M. Mehrabian, M. Navab, L. L. Demer, A. J. Lusis, and A. M. Fogelman. 1991. Minimally modified low density lipoprotein is biologically active in vivo in mice. J. Clin. Invest. 87: 2253-2257.
27. Watson, A. D., N. Leitinger, M. Navab, K. F. Faull, S. Horkko, J. L. Witztum, W. Palinski, D. Schwenke, R. G. Salomon, W. Sha, G. Subbanagounder, A. M. Fogelman, and J. A. Berliner. 1997. 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. 272: 13597-13607.
28. Watson, A. D., G. Subbanagounder, D. S. Welsbie, K. F. Faull, M. Navab, M. E. Jung, A. M. Fogelman, and J. A. Berliner. 1999. Structural identification of a novel pro-inflammatory epoxyisoprostane phospholipid in mildly oxidized low density lipoprotein. J. Biol. Chem. 274: 24787-24798.
29. Subbanagounder, G., N. Leitinger, D. C. Schwenke, J. W. Wong, H. Lee, C. Rizza, A. D. Watson, K. F. Faull, A. M. Fogelman, and J. A. Berliner. 2000. Determinants of bioactivity of oxidized phospholipids-specific oxidized fatty acyl groups at the sn-2 position. Arterioscler. Thromb. Vasc. Biol. 20: 2248-2254.
30. Subbanagounder, G., J. W. Wong, H. Lee, K. F. Faull, E. Miller, J. L. Witztum, and J. A. Berliner. 2002. Epoxyisoprostane and epoxycyclopentenone phospholipids regulate monocyte chemotactic protein-1 and interleukin-8 synthesis. Formation of these oxidized phospholipids in response to interleukin-1beta. J. Biol. Chem. 277: 7271-7281.
31. Subbanagounder, G., Y. Deng, C. Borromeo, A. N. Dooley, J. A. Berliner, and R. G. Salomon. 2002. Hydroxy alkenal phospholipids regulate inflammatory functions of endothelial cells. Vascul. Pharmacol. 38: 201-209.
32. Poliakov, E., M-L. Brennan, J. MacPherson, R. Zhang, L. N. Weisha, R. G. Salomon, and S. L. Hazen. 2003. Isolevuglandins, a novel class of isoprostenoid derivatives, function as integrated sensors of oxidant stress and are generated by myeloperoxidase in vivo. FASEB J. 17: 2209-2220.
33. Marathe, G. K., S. M. Prescott, G. A. Zimmerman, and T. M. McIntyre. 2001. Oxidized LDL contains inflammatory PAF-like phospholipids. Trends Cardiovasc. Med. 11: 139-142.
34. Marathe, G. K., G. A. Zimmerman, S. M. Prescott, and T. M. McIntyre. 2002. Activation of vascular cells by PAF-like lipids in oxidized LDL. Vascul. Pharmacol. 38: 193-200.
35. Huber, J., A. Vales, G. Mitulovic, M. Blumer, R. Schmid, J. L. Witztum, B. R. Binder, and N. Leitinger. 2002. Oxidized membrane vesicles and blebs from apoptotic cells contain biologically active oxidized phospholipids that induce monocyte-endothelial interactions. Arterioscler. Thromb. Vasc. Biol. 22: 101-107.
36. Huber, J., A. Vales, G. Mitulovic, M. Blumer, R. Schmid, J. L. Witztum, B. R. Binder, and N. Leitinger. 2002. Oxidized membrane vesicles and blebs from apoptotic cells contain biologically active oxidized phospholipids that induce monocyte-endothelial interactions. Arterioscler. Thromb. Vasc. Biol. 22: 101-107.
37. Hörkkö, S., D. A. Bird, E. Miller, H. Itabe, L. Leitinger, G. Subbanagounder, J. A. Berliner, P. Friedman, E. A. Dennis, L. K. Curtiss, W. Palinski, and J. L. Witztum. 1999. Monoclonal autoantibodies specific for oxidized phospholipids or oxidized phospholipid-protein adducts inhibit macrophage uptake of oxidized low-density lipoproteins. J. Clin. Invest. 103: 117-128.
38. Bird, D. A., K. L. Gillotte, S. Horkko, P. Friedman, E. A. Dennis, J. L. Witztum, and D. Steinberg. 1999. Receptors for oxidized low-density lipoprotein on elicited mouse peritoneal macrophages can recognize both the modified lipid moieties and the modified protein moieties: implications with respect to macrophage recognition of apoptotic cells. Proc. Natl. Acad. Sci. USA. 96: 6347-6352.
39. Shaw, P. X., S. Horkko, M-K. Chang, L. K. Curtiss, W. Palinski, G. J. Silverman, and J. L. Witztum. 2000. Natural antibodies with the T15 idiotype may act in atherosclerosis, apoptotic clearance, and protective immunity. J. Clin. Invest. 105: 1731-1740.
40. Binder, C. J., S. Horkko, A. Dewan, M-K. Chang, E. P. Kieu, C. S. Goodyear, P. X. Shaw, W. Palinski, J. L. Witztum, and G. J. Silverman. 2003. Pneumococcal vaccination decreases atherosclerotic lesion formation: molecular mimicry between Streptococcus pneumoniae and oxidized LDL. Nat. Med. 9: 736-743.
41. Binder, C. J., M-K. Chang, P. X. Shaw, Y. I. Miller, K. Hartvigsen, A. Dewan, and J. L. Witztum. 2002. Innate and acquired immunity in atherogenesis. Nat. Med. 8: 1218-1226.
42. Miller, Y. I., M-K. Chang, C. J. Binder, P. X. Shaw, and J. L. Witztum. 2003. Oxidized low density lipoprotein and innate immune receptors. Curr. Opin. Lipidol. 14: 437-445.
43. Cyrus, T., J. L. Witztum, D. J. Rader, R. Tangirala, S. Fazio, M. F. Linton, and C. D. Funk. 1999. Disruption of the 12/15-lipoxygenase gene diminishes atherosclerosis in apo E-deficient mice. J. Clin. Invest. 103: 1597-1604.
44. Steinberg, D. 1999. At last, direct evidence that lipoxygenases play a role in atherogenesis. J. Clin. Invest. 103: 1487-1488.
45. Cyrus, T., D. Pratico, L. Zhao, J. L. Witztum, D. J. Rader, J. Rokach, G. A. FitzGerald, and C. D. Funk. 2001. Absence of 12/15-lipoxygenase expression decreases lipid peroxidation and atherogenesis in apolipoprotein E-deficient mice. Circulation. 103: 2277-2282.
46. George, J., A. Afek, A. Shaish, H. Levkovitz, N. Bloom, T. Cyrus, L. Zhao, C. D. Funk, E. Sigal, and D. Harats. 2001. 12/15-Lipoxygenase gene disruption attenuates atherogenesis in LDL receptor-deficient mice. Circulation. 104: 1646-1650.
47. Zhao, L., C. A. Cuff, E. Moss, U. Wille, T. Cyrus, E. A. Klein, D. Pratico, D. J. Rader, C. A. Hunter, E. Pure, and C. D. Funk. 2002. Selective interleukin-12 synthesis defect in 12/15-lipoxygenase deficient macrophages associated with reduced atherosclerosis in a mouse model of familial hypercholesterolemia. J. Biol. Chem. 277: 35350-35356.
48. Harats, D., A. Shaish, J. George, M. Mulkins, H. Kurihara, H. Levkovitz, and E. Sigal. 2000. Overexpression of 15-lipoxygenase in vascular endothelium accelerates early atherosclerosis in LDL receptor-deficient mice. Arterioscler. Thromb. Vasc. Biol. 20: 2100-2105.
49. Reilly, K. B., S. Srinivasan, M. E. Hatley, M. K. Patricia, J. Lannigan, D. T. Bolick, G. Vandenhoff, H. Pei, R. Natarajan, J. L. Nadler, and C. C. Hedrick. 2004. 12/15-Lipoxygenase activity mediates inflammatory monocyte/endothelial interactions and atherosclerosis in vivo. J. Biol. Chem. 279: 9440-9450.
50. Navab, M., S. Y. Hama, G. M. Anantharamaiah, K. Hassan, G. P. Hough, A. D. Watson, S. Reddy, G. C. Fonarow, and A. M. Fogelman. 2000. Normal high density lipoprotein inhibits three steps in the formation of mildly oxidized low density lipoprotein: steps 2 and 3. J. Lipid Res. 41: 1495-1508.
51. Brennan, M. L., M. M. Anderson, D. M. Shih, X. D. Qu, X. Wang, A. C. Mehta, L. L. Lim, W. Shi, S. L. Hazen, J. S. Jacob, J. R. Crowley, J. W. Heinecke, and A. J. Lusis. 2001. Increased atherosclerosis in myeloperoxidase-deficient mice. J. Clin. Invest. 107: 419-430.
52. Thukkani, A. K., J. McHowat, F-F. Hsu, M-L. Brennan, S. L. Hazen, and D. A. Ford. 2003. Identification of α-chloro fatty aldehydes and unsaturated lysophosphatidylcholine molecular species in human atherosclerotic lesions. Circulation. 108: 3128-3133.
53. Carr, A. C., M. R. McCall, and B. Frei. 2000. Oxidation of LDL by myeloperoxidase and reactive nitrogen species: reaction pathways and antioxidant protection. Arterioscler. Thromb. Vasc. Biol. 20: 1716-1723.
54. Zhang, R., M-L. Brennan, Z. Shen, J. C. MacPherson, D. Schmitt, C. E. Molena, and S. L. Hazen. 2002. Myeloperoxidase functions as a major enzymatic catalyst for initiation of lipid peroxidation at sites of inflammation. J. Biol. Chem. 277: 46116-46122.
55. Shishebhor, M. H., B. J. Aviles, M-L. Brennan, X. Fu, M. Goormastic, G. L. Pearce, N. Gokee, J. F. Keaney, Jr., M. S. Penn, D. L. Sprecher, J. A. Vita, and S. L. Hazen. 2003. Association of nitrotyrosine levels with cardiovascular disease and modulation by statin therapy. J. Am. Med. Assoc. 289: 1675-1680.
56. Brennan, M-L., M. S. Penn, F. Van Lente, V. Nambi, M. H. Shishehbor, R. J. Aviles, M. Goormastic, M. L. Pepoy, E. S. McErlean, E. J. Topol, S. E. Nissen, and S. L. Hazen. 2003. Prognostic value of myeloperoxidase in patients with chest pain. N. Engl. J. Med. 349: 1595-1604.
57. Brennan, M-L., and S. L. Hazen. 2003. Emerging role of myeloperoxidase and oxidant stress markers in cardiovascular risk assessment. Curr. Opin. Lipidol. 14: 353-359.
58. Gaut, J. P., J. Byun, H. D. Tran, W. M. Lauber, J. A. Carroll, R. S. Hotchkiss, A. Belaaouaj, and J. W. Heinecke. 2002. Myeloperoxidase produces nitrating oxidants in vivo. J. Clin. Invest. 109: 1311-1319.
59. Sorescu, D., K. Szocs, and K. K. Griendling. 2001. NAD(P)H oxidases and their relevance to atherosclerosis. Trends Cardiovasc. Med. 11: 124-131.
60. Cathcart, M. K. 2004. Regulation of superoxide anion production by NADPH oxidase in monocytes/macrophages. Contributions to atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 24: 23-28.
61. Heinecke, J. W. 2003. Oxidative stress: new approaches to diagnosis and prognosis in atherosclerosis. Am. J. Cardiol. 91: 12A-16A.
62. Parthasarathy, S., N. Khan-Merchant, M. Penumetcha, B. V. Khan, and N. Santanam. 2001. Did the antioxidant trials fail to validate the oxidation hypothesis? Curr. Atheroscler. Rep. 3: 392-398.
63. Heinecke, J. W. 1999. Is lipid peroxidation relevant to atherogenesis? J. Clin. Invest. 104: 135-136.
64. Witting, P., K. Pettersson, A-M. Ostlund-Lindqvist, C. Westerlund, M. Wagberg, and R. Stocker. 1999. Dissociation of atherogenesis from aortic accumulation of lipid hydro(pero)xides in Watanabe heritable hyperlipidemic rabbits. J. Clin. Invest. 104: 213-220.
65. Shen, J., E. Herderick, J. F. Cornhill, E. Zsigmond, H-S. Kim, H. Kuhn, N. V. Guevara, and L. Chan. 1996. Macrophage-mediated 15-lipoxygenase expression protects against atherosclerosis development. J. Clin. Invest. 98: 2201-2208.
66. Bocan, T. M., W. S. Rosebury, S. B. Mueller, S. Kuchera, K. Welch, A. Daugherty, and J. A. Cornicelli. 1998. Specific 15-lipoxygenase inhibitor limits the progression and monocyte-macrophage enrichment of hypercholesterolemia-induced atherosclerosis in the rabbit. Atherosclerosis. 136: 203-216.
67. Sendobry, S. M., J. A. Cornicelli, K. Welch, T. Bocan, B. Tait, B. K. Trivedi, N. Colbry, R. D. Dyer, S. J. Feinmark, and A. Daugherty. 1997. Attenuation of diet-induced atherosclerosis in rabbits with a highly selective 15-lipoxygenase inhibitor lacking significant antioxidant properties. Br. J. Pharmacol. 120: 1199-1206.
68. US Preventive Services Task Force. 2003. Routine vitamin supplementation to prevent cancer and cardiovascular disease: recommendations and rationale. Ann. Intern. Med. 139: 51-55.
69. Morris, C. D., and S. Carson. 2003. Routine vitamin supplementation to prevent cardiovascular disease: a summary of the evidence for the US Preventive Services Task Force. Ann. Intern. Med. 139: 56-70.
70. Vivekananthan, D. P., M. S. Penn, S. K. Sapp, A. Hsu, and E. J. Topol. 2003. Use of antioxidant vitamins for the prevention of cardiovascular disease: meta-analysis of randomised trials. Lancet. 361: 2017-2023.
71. Steinberg, D., and J. L. Witztum. 2002. Is the oxidative modification hypothesis relevant to human atherosclerosis? Do the antioxidant trials conducted to date refute the hypothesis? Circulation. 105: 2107-2111.
72. Heinecke, J. W. 2003. Clinical trials of vitamin E in coronary artery disease: is it time to reconsider the low-density lipoprotein oxidation hypothesis? Curr. Atheroscler. Rep. 5: 83-87.
73. Meagher, E. A., O. P. Barry, J. A. Lawson, J. Rokach, and G. A. FitzGerald. 2001. Effects of vitamin E on lipid peroxidation in healthy persons. J. Am. Med. Assoc. 285: 1178-1182.
74. Navab, M., S. Y. Hama, G. P. Hough, G. Subbanagounder, S. T. Reddy, and A. M. Fogelman. 2001. A cell-free assay for detecting HDL that is dysfunctional in preventing the formation of or inactivating oxidized phospholipids. J. Lipid Res. 42: 1308-1317.
75. Shih, D. M., L. Gu, Y-R. Xia, M. Navab, W-F. Li, S. Hama, L. W. Castellani, C. E. Furlong, L. G. Costa, A. M. Fogelman, and A. J. Lusis. 1998. Mice lacking serum paraoxonase are susceptible to organophosphate toxicity and atherosclerosis. Nature. 394: 284-287.
76. Shih, D. M., Y-R. Xia, X-P. Wang, E. Miller, L. W. Castellani, G. Subbanagounder, H. Cheroutre, K. Faull, J. A. Berliner, J. L. Witztum, and A. J. Lusis. 2000. Combined serum paraoxonase/apolipoprotein E knockout mice exhibit increased lipoprotein oxidation and atherosclerosis. J. Biol. Chem. 275: 17527-17535.
77. Tward, A., Y. R. Xia, X. P. Wang, Y. S. Shi, C. Park, L. W. Castellani, A. J. Lusis, and D. M. Shih. 2002. Decreased atherosclerotic lesion formation in human serum paraoxonase transgenic mice. Circulation. 106: 484-490.
78. Shih, D., S. T. Reddy, and A. J. Lusis. 2002. CHD and atherosclerosis: human epidemiological studies and transgenic mouse models. In Paraoxonase (PON1) in Health and Disease: Basic and Clinical Aspects. L. G. Costa and C. E. Furlong, editors. Kluwer Academic Publishers, Norwell, MA. 93-124.
79. Ishikawa, K., D. Sugawara, X. P. Wang, K. Suzuki, H. Itabe, Y. Maruyama, and A. J. Lusis. 2001. Heme oxygenase-1 inhibits atherosclerotic lesion formation in LDL-receptor knockout mice. Circ. Res. 88: 506-512.
80. Yet, S. F., M. D. Layne, X. Liu, Y. H. Chen, B. Ith, N. E. Sibinga, and M. A. Perrella. 2003. Absence of heme oxygenase-1 exacerbates atherosclerotic lesion formation and vascular remodeling. FASEB J. 17: 1759-1761.
81. Kaneda, H., M. Ohno, J. Taguchi, M. Togo, H. Hashimoto, K. Ogasawara, T. Aizawa, N. Ishizaka, and R. Nagai. 2002. Heme oxygenase-1 gene promoter polymorphism is associated with coronary artery disease in Japanese patients with coronary risk factors. Arterioscler. Thromb. Vasc. Biol. 22: 1680-1685.
82. Navab, M., S. Y. Hama, C. J. Cooke, G. M. Anantharamaiah, M. Chaddha, L. Jin, G. Subbanagounder, K. F. Faull, S. T. Reddy, N. E. Miller, and A. M. Fogelman. 2000. Normal high density lipoprotein inhibits three steps in the formation of mildly oxidized low density lipoprotein: step 1. J. Lipid Res. 41: 1481-1494.
83. Badimon, J. J., L. Badimon, and V. Fuster. 1990. Regression of atherosclerotic lesions by high density lipoprotein plasma fraction in the cholesterol-fed rabbit. J. Clin. Invest. 85: 1234-1241.
84. Plump, A. S., C. J. Scott, and J. L. Breslow. 1994. Human apolipoprotein A-I gene expression increases high density lipoprotein and suppresses atherosclerosis in the apolipoprotein E-deficient mouse. Proc. Natl. Acad. Sci. USA. 91: 9607-9611.
85. Milano mobilizes tissue cholesterol and rapidly reduces plaque lipid and macrophage content in apolipoprotein E-deficient mice: potential implications for acute plaque stabilization. Circulation. 103: 3047-3050.
86. Garber, D. W., G. Datta, M. Chaddha, M. N. Palgunachari, S. Y. Hama, M. Navab, A. M. Fogelman, J. P. Segrest, and G. M. Anatharamaiah. 2001. A new synthetic class A amphipathic peptide analogue protects mice from diet-induced atherosclerosis. J. Lipid Res. 42: 545-552.
87. Navab, M., G. M. Anantharamaiah, S. Hama, D. W. Garber, M. Chaddha, G. Hough, R. Lallone, and A. M. Fogelman. 2002. Oral administration of an Apo A-I mimetic peptide synthesized from D-amino acids dramatically reduces atherosclerosis in mice independent of plasma cholesterol. Circulation. 105: 290-292.
88. Van Lenten, B. J., A. C. Wagner, G. M. Anantharamaiah, D. W. Garber, M. C. Fishbein, L. Adhikary, D. P. Nayak, S. Hama, M. Navab, and A. M. Fogelman. 2002. Influenza infection promotes macrophage traffic into arteries of mice that is prevented by D-4F, an apolipoprotein A-I mimetic peptide. Circulation. 106: 1127-1132.
89. Ou, Z., J. Ou, A. Ackerman, K. T. Oldham, and K. A. Pritchard. 2003. L-4F, an apolipoprotein A-I mimetic, restores nitric oxide and superoxide anion balance in low-density lipoprotein-treated endothelial cells. Circulation. 107: 1520-1524.
90. Ou, J., Z. Ou, D. W. Jones, S. Holzhaure, O. A. Hatoum, A. W. Ackerman, D. W. Weihrauch, D. D. Gutterman, K. Guice, K. T. Oldham, C. A. Hillery, and K. A. Pritichard. 2003. L-4F, an apolipoprotein A-I mimetic, dramatically improves vasodilation in hypercholesterolemia and sickle cell disease. Circulation. 107: 2337-2341.
91. Nissen, S. E., T. Tsunoda, E. M. Tuzcu, P. Schoenhagen, C. J. Cooper, M. Yasin, G. M. Eaton, M. A. Lauer, W. S. Sheldon, C. L. Grines, S. Halpern, T. Crowe, J. C. Blankenship, and R. Kerensky. 2003. Effect of recombinant apoA-I Milano on coronary atherosclerosis in patients with acute coronary syndromes. A randomized controlled trial. J. Am. Med. Assoc. 290: 2292-2300.
92. Rader, D. J. 2003. High-density lipoproteins as an emerging therapeutic target for atherosclerosis. J. Am. Med. Assoc. 290: 2322-2324.
93. Bisoendial, R. J., G. K. Hovingh, J. H. M. Levels, P. G. Lerch, I. Andresen, M. R. Hayden, J. J. P. Kastelein, and E. S. G. Stroes. 2003. Restoration of endothelial function by increasing high-density lipoprotein in subjects with isolated low high-density lipoprotein. Circulation. 107: 2944-2948.
94. Zhang, Y. Z., I. Zanotti, M. P. Reilly, J. M. Glick, G. H. Rothblat, and D. J. Rader. 2003. Overexpression of apolipoprotein A-I promotes reverse transport of cholesterol from macrophages to feces in vivo. Circulation. 108: 661-663.
95. Remaley, A. T., F. Thomas, J. A. Stonik, S. J. Demosky, S. E. Bark, E. B. Neufeld, A. V. Bocharov, T. G. Vishnyakova, A. P. Patterson, T. L. Eggerman, S. Santamarina-Fojo, and H. B. Brewer. 2003. Synthetic amphipathic helical peptides promote lipid efflux from cells by an ABCA1-dependent and an ABCA1-independent pathway. J. Lipid Res. 44: 828-836.
96. Martinez, L. O., B. Agerholm-Larsen, N. Wang, W. Chen, and A. R. Tall. 2003. Phosphorylation of a pest sequence in ABCA1 promotes calpain degradation and is reversed by apoA-I. J. Biol. Chem. 278: 37368-37374.
97. - is a lipid hydroperoxide-enriched circulating lipoprotein. J. Lipid Res. 38: 419-428.
98. Bowry, V. W., K. K. Stanley, and R. Stocker. 1992. High density lipoprotein is the major carrier of lipid hydroperoxides in human blood plasma from fasting donors. Proc. Natl. Acad. Sci. USA. 89: 10316-10320.
99. Downs, J. R., M. Clearfield, S. Weis, E. Whitney, D. R. Shapiro, P. A. Beere, A. Langendorfer, E. A. Stein, W. Kruyer, and A. M. Gotto, Jr. 1998. Primary prevention of acute coronary events with lovastatin in men and women with average cholesterol levels. J. Am. Med. Assoc. 279: 1615-1622.
100. Ansell, B. J., M. Navab, S. Hama, N. Kamranpour, G. Fonarow, G. Hough, S. Rahmani, R. Mottahedeh, R. Dave, S. T. Reddy, and A. M. Fogelman. 2003. The inflammatory/anti-inflammatory properties of HDL distinguish patients from controls better than HDL-cholesterol levels and are favorably impacted by simvastatin treatment. Circulation. 108: 2751-2756.
101. Gordon, T., W. P. Castelli, M. C. Hjortland, W. B. Kannel, and T. R. Dawber. 1977. High density lipoprotein as a protective factor against coronary heart disease. Am. J. Med. 62: 707-714.
102. Castelli, W. P., R. J. Garrison, P. W. Wilson, R. D. Abbott, S. Kalousdian, and W. B. Kannel. 1986. Incidence of coronary heart disease and lipoprotein cholesterol levels. The Framingham Study. J. Am. Med. Assoc. 256: 2835-2838.
103. Ridker, P. M. 2002. On evolutionary biology, inflammation, infection, and the causes of atherosclerosis. Circulation. 105: 2-4.
104. Van Lenten, B. J., S. Y. Hama, F. C. deBeer, D. M. Stafforini, T. M. McIntyre, S. M. Prescott, B. N. La Du, A. M. Fogelman, and M. Navab. 1995. Anti-inflammatory HDL becomes pro-inflammatory during the acute phase response. J. Clin. Invest. 96: 2758-2767.
105. Gabay, C., and I. Kushner. 1999. Acute-phase proteins and other systemic responses to inflammation. N. Engl. J. Med. 340: 448-454.
106. Navab, M., S. Hama-Levy, B. J. Van Lenten, G. C. Fonarow, C. J. Cardinez, L. W. Castellani, M-L. Brennan, A. J. Lusis, and A. M. Fogelman. 1997. Mildly oxidized LDL induces an increased apolipoprotein J/paraoxonase ratio. J. Clin. Invest. 99: 2005-2019.
107. Navab, M., J. A. Berliner, G. Subbanagounder, S. Hama, A. J. Lusis, L. W. Castellani, S. Reddy, D. Shih, W. Shi, A. D. Watson, B. J. Van Lenten, D. Vora, and A. M. Fogelman. 2001. HDL and the inflammatory response induced by LDL-derived oxidized phospholipids. Arterioscler. Thromb. Vasc. Biol. 21: 481-488.
108. Watson, A. D., M. Navab, S. Y. Hama, A. Sevanian, S. M. Prescott, D. M. Stafforini, T. M. McIntyre, B. N. La Du, A. M. Fogelman, and J. A. Berliner. 1995. Effect of platelet activating factor-acetyl-hydrolase on the formation and action of minimally oxidized-low density lipoprotein. J. Clin. Invest. 95: 774-782.
109. Forte, T. M., G. Subbanagounder, J. A. Berliner, P. J. Blanche, A. O. Clermont, Z. Jia, M. N. Oda, R. M. Krauss, and J. K. Bielicki. 2002. Altered activities of anti-atherogenic enzymes LCAT, paraoxonase, and platelet-activating factor acetylhydrolase in atherosclerosis-susceptible mice. J. Lipid Res. 43: 477-485.
110. 2001. Executive Summary of the Third Report of the National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III). J. Am. Med. Assoc. 285: 2486-2497.
111. Macdonald, D. L., T. L. Terry, L. B. Agellon, P. N. Nation, and G. A. Francis. 2003. Administration of tyrosyl radical-oxidized HDL inhibits the development of atherosclerosis in apolipoprotein E-deficient mice. Arterioscler. Thromb. Vasc. Biol. 23: 1583-1588.
112. Bergt, C., J. F. Oram, and J. W. Heinecke. 2003. Oxidized HDL: the paradox-idation of lipoproteins. Arterioscler. Thromb. Vasc. Biol. 23: 1488-1490.
113. Wang, W. Q., D. L. Merriam, A. S. Moses, and G. A. Francis. 1998. Enhanced cholesterol efflux by tyrosyl radical-oxidized high density lipoprotein is mediated by apolipoprotein AI-AII heterodimers. J. Biol. Chem. 273: 17391-17398.
114. Christison, J., A. Karjalainen, J. Brauman, F. Bygrave, and R. Stocker. 1996. Rapid reduction and removal of HDL- but not LDL-associated cholesteryl ester hydroperoxides by rat liver perfused in situ. Biochem. J. 314: 739-742.
115. Khovidhunkit, W., J. K. Shigenaga, A. H. Moser, K. R. Feingold, and C. Grunfeld. 2001. Cholesterol efflux by acute-phase high density lipoprotein: role of lecithin:cholesterol acyltransferase. J. Lipid Res. 42: 967-975.
116. Pussinen, P. J., M. Jauhiainen, T. Vilkuna-Rautiainen, J. Sundvall, M. Vesanen, K. Mattila, T. Palosuo, G. Alfthan, and S. Asikainen. 2004. Periodontitis decreases the antiatherogenic potency of high density lipoprotein. J. Lipid Res. 45: 139-147.
117. Reddy, S. T., S. Hama, C. Ng, V. Grijalva, M. Navab, and A. M. Fogelman. 2002. ATP-binding cassette transporter 1 (ABCA1) participates in LDL oxidation by artery wall cells. Arterioscler. Thromb. Vasc. Biol. 22: 1877-1883.
118. Churchill, W. S. 1949. The Second World War. Their Finest Hour. Houghton Mifflin Company, Boston. p. 550.
119. Auerbach, B. J., J. S. Kiely, and J. A. Cornicelli. 1992. A spectrophotometric microtiter-based assay for the detection of hydroperoxy derivatives of linoleic acid. Anal. Biochem. 201: 375-380.
120. Van Lenten, B. J., A. C. Wagner, D. P. Nayak, S. Hama, M. Navab, and A. M. Fogelman. 2001. High-density lipoprotein loses its antiinflammatory properties during acute influenza A infection. Circulation. 103: 2283-2288.
121. Whitelegge, J. P., J. le Coutre, J. C. Lee, C. K. Engel, G. G. Prive, K. F. Faull, and H. R. Kaback. 1999. Toward the bilayer proteome, electrospray ionization-mass spectrometry of large, intact transmembrane proteins. Proc. Natl. Acad. Sci. USA. 96: 10695-10698.