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Journal of Lipid Research, Vol. 41, 1495-1508, September 2000
Copyright © 2000 by Lipid Research, Inc.

Original Article

Normal high density lipoprotein inhibits three steps in the formation of mildly oxidized low density lipoprotein: steps 2 and 3

Mohamad Navaba, Susan Y. Hamaa, G. M. Anantharamaiahb, Kholood Hassana, Greg P. Hougha, Andrew D. Watsona, Srinivasa T. Reddya, Alex Sevanianc, Gregg C. Fonarowa, and Alan M. Fogelmana
a Atherosclerosis Research Unit, Division of Cardiology, Department of Medicine, University of California, Los Angeles, Los Angeles, CA 90095
b Department of Medicine and the Atherosclerosis Research Unit, University of Alabama, Birmingham, AL 35294
c Psychiatry and Biobehavioral Sciences, Department of Molecular Pharmacology and Toxicology, School of Pharmacy, University of Southern California, Los Angeles, CA 90089

Correspondence to: Alan M. Fogelman

Treatment of human artery wall cells with apolipoprotein A-I (apoA-I), but not apoA-II, with an apoA-I peptide mimetic, or with high density lipoprotein (HDL), or paraoxonase, rendered the cells unable to oxidize low density lipoprotein (LDL). Human aortic wall cells were found to contain 12-lipoxygenase (12-LO) protein. Transfection of the cells with antisense to 12-LO (but not sense) eliminated the 12-LO protein and prevented LDL-induced monocyte chemotactic activity. Addition of 13(S)-hydroperoxyoctadecadienoic acid [13(S)-HPODE] and 15(S)-hydroperoxyeicosatetraenoic acid [15(S)-HPETE] dramatically enhanced the nonenzymatic oxidation of both 1-palmitoyl-2-arachidonoyl-sn-glycero-3-phosphocholine (PAPC) and cholesteryl linoleate. On a molar basis 13(S)-HPODE and 15(S)-HPETE were approximately two orders of magnitude greater in potency than hydrogen peroxide in causing the formation of biologically active oxidized phospholipids (m/z 594, 610, and 828) from PAPC. Purified paraoxonase inhibited the biologic activity of these oxidized phospholipids. HDL from 10 of 10 normolipidemic patients with coronary artery disease, who were neither diabetic nor receiving hypolipidemic medications, failed to inhibit LDL oxidation by artery wall cells and failed to inhibit the biologic activity of oxidized PAPC, whereas HDL from 10 of 10 age- and sex-matched control subjects did.

We conclude that a) mildly oxidized LDL is formed in three steps, one of which involves 12-LO and each of which can be inhibited by normal HDL, and b) HDL from at least some coronary artery disease patients with normal blood lipid levels is defective both in its ability to prevent LDL oxidation by artery wall cells and in its ability to inhibit the biologic activity of oxidized PAPC.—Navab, M., S. Y. Hama, G. M. Anantharamaiah, K. Hassan, G. P. Hough, A. D. Watson, S. T. Reddy, A. Sevanian, G. C. Fonarow, and A. M. Fogelman. Normal high density lipoprotein inhibits three steps in the formation of mildly oxidized low density lipoprotein: steps 2 and 3. J. Lipid Res. 2000. 41: 1495;–1508.

Supplementary key words: LDL, HDL, mildly oxidized LDL, MM-LDL, oxidized phospholipids, HPODE, HPETE, cholesteryl linoleate hydroperoxide, paraoxonase, atherosclerosis, antioxidant


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C.-y. Yang, J. Wang, A. N. Krutchinsky, B. T. Chait, J. D. Morrisett, and C. V. Smith
Selective oxidation in vitro by myeloperoxidase of the N-terminal amine in apolipoprotein B-100
J. Lipid Res., November 1, 2001; 42(11): 1891 - 1896.
[Abstract] [Full Text] [PDF]

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 FASEB J.Home page
A. MERTENS and P. HOLVOET
Oxidized LDL and HDL: antagonists in atherothrombosis
FASEB J, October 1, 2001; 15(12): 2073 - 2084.
[Abstract] [Full Text] [PDF]

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 CarcinogenesisHome page
B. C. Y. Wong, W. P. Wang, C. H. Cho, X. M. Fan, M. C. M. Lin, H. F. Kung, and S. K. Lam
12-Lipoxygenase inhibition induced apoptosis in human gastric cancer cells
Carcinogenesis, September 1, 2001; 22(9): 1349 - 1354.
[Abstract] [Full Text] [PDF]

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 Arterioscler. Thromb. Vasc. Bio.Home page
R. Natarajan, M. A. Reddy, K. U. Malik, S. Fatima, and B. V. Khan
Signaling Mechanisms of Nuclear Factor-{kappa}B-Mediated Activation of Inflammatory Genes by 13-Hydroperoxyoctadecadienoic Acid in Cultured Vascular Smooth Muscle Cells
Arterioscler. Thromb. Vasc. Biol., September 1, 2001; 21(9): 1408 - 1413.
[Abstract] [Full Text] [PDF]

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 Arterioscler. Thromb. Vasc. Bio.Home page
B. Mackness, G. K. Davies, W. Turkie, E. Lee, D. H. Roberts, E. Hill, C. Roberts, P. N. Durrington, and M. I. Mackness
Paraoxonase Status in Coronary Heart Disease: Are Activity and Concentration More Important Than Genotype?
Arterioscler. Thromb. Vasc. Biol., September 1, 2001; 21(9): 1451 - 1457.
[Abstract] [Full Text] [PDF]

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 J. Lipid Res.Home page
M. Navab, S. Y. Hama, G. P. Hough, G. Subbanagounder, S. T. Reddy, and A. M. Fogelman
A cell-free assay for detecting HDL that is dysfunctional in preventing the formation of or inactivating oxidized phospholipids
J. Lipid Res., August 1, 2001; 42(8): 1308 - 1317.
[Abstract] [Full Text] [PDF]

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 J. Lipid Res.Home page
G. Datta, M. Chaddha, S. Hama, M. Navab, A. M. Fogelman, D. W. Garber, V. K. Mishra, R. M. Epand, R. F. Epand, S. Lund-Katz, et al.
Effects of increasing hydrophobicity on the physical-chemical and biological properties of a class A amphipathic helical peptide
J. Lipid Res., July 1, 2001; 42(7): 1096 - 1104.
[Abstract] [Full Text] [PDF]

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 CirculationHome page
B. J. Van Lenten, A. C. Wagner, D. P. Nayak, S. Hama, M. Navab, and A. M. Fogelman
High-Density Lipoprotein Loses Its Anti-Inflammatory Properties During Acute Influenza A Infection
Circulation, May 8, 2001; 103(18): 2283 - 2288.
[Abstract] [Full Text] [PDF]

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 J. Lipid Res.Home page
D. W. Garber, G. Datta, M. Chaddha, M. N. Palgunachari, S. Y. Hama, M. Navab, A. M. Fogelman, J. P. Segrest, and G. M. Anantharamaiah
A new synthetic class A amphipathic peptide analogue protects mice from diet-induced atherosclerosis
J. Lipid Res., April 1, 2001; 42(4): 545 - 552.
[Abstract] [Full Text]

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 Arterioscler. Thromb. Vasc. Bio.Home page
M. Navab, J. A. Berliner, G. Subbanagounder, S. Hama, A. J. Lusis, L. W. Castellani, S. Reddy, D. Shih, W. Shi, A. D. Watson, et al.
HDL and the Inflammatory Response Induced by LDL-Derived Oxidized Phospholipids
Arterioscler. Thromb. Vasc. Biol., April 1, 2001; 21(4): 481 - 488.
[Abstract] [Full Text] [PDF]

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 J. Lipid Res.Home page
M. Navab, S. Y. Hama, C. J. Cooke, G. M. Anantharamaiah, M. Chaddha, L. Jin, G. Subbanagounder, K. F. Faull, S. T. Reddy, N. E. Miller, et al.
Normal high density lipoprotein inhibits three steps in the formation of mildly oxidized low density lipoprotein: step 1
J. Lipid Res., September 1, 2000; 41(9): 1481 - 1494.
[Abstract] [Full Text]

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 J. Biol. Chem.Home page
C. C. Curtain, F. Ali, I. Volitakis, R. A. Cherny, R. S. Norton, K. Beyreuther, C. J. Barrow, C. L. Masters, A. I. Bush, and K. J. Barnham
Alzheimer's Disease Amyloid-beta Binds Copper and Zinc to Generate an Allosterically Ordered Membrane-penetrating Structure Containing Superoxide Dismutase-like Subunits
J. Biol. Chem., June 1, 2001; 276(23): 20466 - 20473.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
C. J. Ng, D. J. Wadleigh, A. Gangopadhyay, S. Hama, V. R. Grijalva, M. Navab, A. M. Fogelman, and S. T. Reddy
Paraoxonase-2 Is a Ubiquitously Expressed Protein with Antioxidant Properties and Is Capable of Preventing Cell-mediated Oxidative Modification of Low Density Lipoprotein
J. Biol. Chem., November 21, 2001; 276(48): 44444 - 44449.
[Abstract] [Full Text] [PDF]


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