Atherosclerosis
Volume 192, Issue 2 , Pages 266-274 , June 2007

Common variants of apolipoprotein A-IV differ in their ability to inhibit low density lipoprotein oxidation

  • Wai-Man R. Wong

      Affiliations

    • Centre for Cardiovascular Genetics, British Heart Foundation Laboratories, Royal Free and University College London Medical School, London WC1E 6JF, UK
    • These authors contributed equally.
  • ,
  • Andrew B. Gerry

      Affiliations

    • School of Animal and Microbial Sciences, The University of Reading, Whiteknights, P.O. Box 228, Reading RG6 6AJ, UK
    • These authors contributed equally.
  • ,
  • Wendy Putt

      Affiliations

    • Centre for Cardiovascular Genetics, British Heart Foundation Laboratories, Royal Free and University College London Medical School, London WC1E 6JF, UK
  • ,
  • Jane L. Roberts

      Affiliations

    • Centre for Cardiovascular Genetics, British Heart Foundation Laboratories, Royal Free and University College London Medical School, London WC1E 6JF, UK
  • ,
  • Richard B. Weinberg

      Affiliations

    • The Departments of Internal Medicine and Physiology & Pharmacology, Wake Forest University School of Medicine, Winston-Salem, NC 27157-1040, USA
  • ,
  • Steve E. Humphries

      Affiliations

    • Centre for Cardiovascular Genetics, British Heart Foundation Laboratories, Royal Free and University College London Medical School, London WC1E 6JF, UK
  • ,
  • David S. Leake

      Affiliations

    • School of Animal and Microbial Sciences, The University of Reading, Whiteknights, P.O. Box 228, Reading RG6 6AJ, UK
  • ,
  • Philippa J. Talmud

      Affiliations

    • Centre for Cardiovascular Genetics, British Heart Foundation Laboratories, Royal Free and University College London Medical School, London WC1E 6JF, UK
    • Corresponding Author InformationCorresponding author. Tel.: +44 20 7679 6968; fax: +44 20 7679 6212.

Received 19 December 2005 ,Revised 29 June 2006 ,Accepted 14 July 2006.

References 

  1. Steinberg D, Parthasarathy S, Carew TE, Khoo JC, Witztum JL. Beyond cholesterol. Modifications of low-density lipoprotein that increase its atherogenicity. N Engl J Med. 1989;320:915–924
  2. Parthasarathy S, Fong LG, Otero D, Steinberg D. Recognition of solubilized apoproteins from delipidated, oxidized low density lipoprotein (LDL) by the acetyl-LDL receptor. Proc Natl Acad Sci USA. 1987;84:537–540
  3. Quinn MT, Parthasarathy S, Steinberg D. Lysophosphatidylcholine: a chemotactic factor for human monocytes and its potential role in atherogenesis. Proc Natl Acad Sci USA. 1988;85:2805–2809
  4. Frostegard J, Haegerstrand A, Gidlund M, Nilsson J. Biologically modified LDL increases the adhesive properties of endothelial cells. Atherosclerosis. 1991;90:119–126
  5. Mallat Z, Tedgui A. Apoptosis in the vasculature: mechanisms and functional importance. Br J Pharmacol. 2000;130:947–962
  6. MRC/BHF, Heart Protection Study of antioxidant vitamin supplementation in 20,536 high-risk individuals: a randomised placebo-controlled, trial. Lancet. 2002;360:23–33
  7. Stampfer MJ, Hennekens CH, Manson JE, et al. Vitamin E consumption and the risk of coronary disease in women. N Engl J Med. 1993;328:1444–1449
  8. Carew TE, Schwenke DC, Steinberg D. Antiatherogenic effect of probucol unrelated to its hypocholesterolemic effect: evidence that antioxidants in vivo can selectively inhibit low density lipoprotein degradation in macrophage-rich fatty streaks and slow the progression of atherosclerosis in the Watanabe heritable hyperlipidemic rabbit. Proc Natl Acad Sci USA. 1987;84:7725–7729
  9. Utermann G, Beisiegel U. Apolipoprotein A-IV: a protein occurring in human mesenteric lymph chylomicrons and free in plasma. Eur J Biochem. 1979;99:333–343
  10. Hayashi H, Nutting DJ, Fujimoto K, et al. Transport of lipid and apolipoproteins A-I and A-IV in intestinal lymph of the rat. J Lipid Res. 1990;31:1613–1625
  11. Green PH, Glickman RM, Saudek CD, Blum CB, Tall AR. Human intestinal lipoproteins. Studies in chyluric subjects. J Clin Invest. 1979;64:233–242
  12. Ezeh B, Haiman M, Alber HF, et al. Plasma distribution of apoA-IV in patients with coronary artery disease and healthy controls. J Lipid Res. 2003;44:1523–1529
  13. Steinmetz A, Utermann G. Activation of lecithin cholesterol acyltransferase by human apolipoprotein A-IV. J Biol Chem. 1985;2258–2264
  14. Chen CH, Albers JJ. Activation of lecithin cholesteryl acyltransferase by human apolipoproteins E-2, E-3, and A-IV. Biochim Biophys Acta. 1985;836:279–285
  15. Main LA, Ohnishi T, Yokoyama S. Activation of human plasma cholesteryl ester transfer protein by human apolipoprotein A-IV. Biochim Biophys Acta. 1996;1300:17–24
  16. Goldberg IJ, Scheraldi CA, Yacoub LK, Saxena U, Bisgaier CL. Lipoprotein ApoC-II activation of lipoprotein lipase. Modulation by apolipoprotein A-IV. J Biol Chem. 1990;265:4266–4272
  17. Steinmetz A, Barbaras R, Ghalim N, et al. Human apolipoprotein A-IV binds to apolipoprotein A-I/A-II receptor sites and promotes cholesterol efflux from adipose cells. J Biol Chem. 1990;265:7859–7863
  18. Dvorin E, Gorder NL, Benson DM, Gotto AM. Apolipoprotein A-IV: a determinant for binding and uptake of high density lipoproteins by rat hepatocytes. J Biol Chem. 1986;261:15714–15720
  19. Duverger N, Tremp G, Caillaud JM, et al. Protection against atherogenesis in mice mediated by human apolipoprotein A-IV. Science. 1996;273:966–968
  20. Kronenberg F, Stuhlinger M, Trenkwalder E, et al. Low apolipoprotein A-IV plasma concentrations in men with coronary artery disease. J Am Coll Cardiol. 2000;36:751–757
  21. Warner MM, Guo J, Zhao Y. The relationship between plasma apolipoprotein A-IV levels and coronary heart disease. Chin Med J (Engl). 2001;114:275–279
  22. Ostos MA, Conconi M, Vergnes L, et al. Antioxidative and antiatherosclerotic effects of human apolipoprotein A-IV in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol. 2001;21:1023–1028
  23. Ferretti G, Bacchetti T, Bicchiega V, Curatola G. Effect of human Apo AIV against lipid peroxidation of very low density lipoproteins. Chem Phys Lipids. 2002;114:45–54
  24. Recalde D, Ostos MA, Badell E, et al. Human apolipoprotein A-IV reduces secretion of proinflammatory cytokines and atherosclerotic effects of a chronic infection mimicked by lipopolysaccharide. Arterioscler Thromb Vasc Biol. 2004;24:756–761
  25. Vowinkel T, Mori M, Krieglstein CF, et al. Apolipoprotein A-IV inhibits experimental colitis. J Clin Invest. 2004;114:260–269
  26. Boerwinkle E, Visvikis S, Chan L. Two polymorphisms for amino acid substitutions in the APOA4 gene. Nucl Acids Res. 1990;18:4966
  27. Tenkanen H, Koskinen P, Metso J, et al. A novel polymorphism of apolipoprotein A-IV is the result of an asparagine to serine substitution at residue 127. Biochim Biophys Acta. 1992;1138:27–33
  28. Wong WR, Hawe E, Li LK, et al. Apolipoprotein AIV gene variant S347 is associated with increased risk of coronary heart disease and lower plasma apolipoprotein AIV levels. Circ Res. 2003;92:969–975
  29. Wong WR, Stephens JW, Acharya J, et al. The APOA4 T347S variant is associated with reduced plasma TAOS in subjects with diabetes mellitus and cardiovascular disease. J Lipid Res. 2004;45:1565–1571
  30. Wilkins GM, Leake DS. The effect of inhibitors of free radical generating-enzymes on low-density lipoprotein oxidation by macrophages. Biochim Biophys Acta. 1994;1211:69–78
  31. Siow RC, Richards JP, Pedley KC, Leake DS, Mann GE. Vitamin C protects human vascular smooth muscle cells against apoptosis induced by moderately oxidized LDL containing high levels of lipid hydroperoxides. Arterioscler Thromb Vasc Biol. 1999;19:2387–2394
  32. Esterbauer H, Striegl G, Puhl H, Rotheneder M. Continuous monitoring of in vitro oxidation of human low density lipoprotein. Free Radic Res Commun. 1989;6:67–75
  33. el Saadani M, Esterbauer H, el Sayed M, et al. A spectrophotometric assay for lipid peroxides in serum lipoproteins using a commercially available reagent. J Lipid Res. 1989;30:627–630
  34. Ziouzenkova O, Sevanian A, Abuja PM, Ramos P, Esterbauer H. Copper can promote oxidation of LDL by markedly different mechanisms. Free Radic Biol Med. 1998;24:607–623
  35. Bowry VW, Ingold KU, Stocker R. Vitamin E in human low-density lipoprotein. When and how this antioxidant becomes a pro-oxidant. Biochem J. 1992;288(Pt 2):341–344
  36. Weinberg RB, Spector MS. Lipoprotein affinity of human apolipoprotein A-IV during cholesterol esterification. Biochem Biophys Res Commun. 1986;135:756–763
  37. Kuzuya M, Yamada K, Hayashi T, et al. Role of lipoprotein–copper complex in copper catalyzed-peroxidation of low-density lipoprotein. Biochim Biophys Acta. 1992;1123:334–341
  38. Retsky KL, Chen K, Zeind J, Frei B. Inhibition of copper-induced LDL oxidation by vitamin C is associated with decreased copper-binding to LDL and 2-oxo-histidine formation. Free Radic Biol Med. 1999;26:90–98
  39. Roland A, Patterson RA, Leake DS. Measurement of copper-binding sites on low density lipoprotein. Arterioscler Thromb Vasc Biol. 2001;21:594–602
  40. Ramos P, Gieseg SP, Schuster B, Esterbauer H. Effect of temperature and phase transition on oxidation resistance of low density lipoprotein. J Lipid Res. 1995;36:2113–2128
  41. Garnier J, Osguthorpe DJ, Robson B. Analysis of the accuracy and implications of simple methods for predicting the secondary structure of globular proteins. J Mol Biol. 1978;120:97–120
  42. Lohse P, Kindt MR, Rader DJ, Brewer HB. Three genetic variants of human plasma apolipoprotein A-IV. ApoA-IV- 1(Thr347⋯Ser), apoA-IV-0(Lys167⋯Glu,Gln360⋯His), and apoA-IV-3(Glu165⋯Lys). J Biol Chem. 1991;266:13513–13518
  43. Zaiou M, Visvikis S, Gueguen R, Parra HJ, Fruchart JC, Siest G. DNA polymorphisms of human apolipoprotein A-IV gene: frequency and effects on lipid, lipoprotein and apolipoprotein levels in a French population. Clin Genet. 1994;46:248–254
  44. Hixson JE, Powers PK. Restriction isotyping of human apolipoprotein A-IV: rapid typing of known isoforms and detection of a new isoform that deletes a conserved repeat. J Lipid Res. 1991;32:1529–1535
  45. von Eckardstein A, Funke H, Schulte M, Erren M, Schulte H, Assmann G. Nonsynonymous polymorphic sites in the apolipoprotein (apo) A-IV gene are associated with changes in the concentration of apo B- and apo A-I-containing lipoproteins in a normal population. AJHG. 1992;50:1115–1128
  46. Weinberg RB, Jordan MK, Steinmetz A. Distinctive structure and function of human apolipoprotein variant apoA-IV-2. J Biol Chem. 1990;265:18372–18378
  47. Tenkanen H, Enholm C. Molecular basis for apoA-IV polymorphisms. Ann Med. 1992;24:47–52
  48. Kalant N, McCormick S, Parniak MA. Effects of copper and histidine on oxidative modification of low density lipoprotein and its subsequent binding to collagen. Arterioscler Thromb. 1991;11:1322–1329
  49. Patterson RA, Leake DS. Human serum, cysteine and histidine inhibit the oxidation of low density lipoprotein less at acidic pH. FEBS Lett. 1998;434:317–321
  50. Mackness B, Hunt R, Durrington PN, Mackness MI. Increased immunolocalization of paraoxonase, clusterin, and apolipoprotein A-I in the human artery wall with the progression of atherosclerosis. Arterioscler Thromb Vasc Biol. 1997;17:1233–1238
  51. Anber V, Griffin BA, McConnell M, Packard CJ, Shepherd J. Influence of plasma lipid and LDL-subfraction profile on the interaction between low density lipoprotein with human arterial wall proteoglycans. Atherosclerosis. 1996;124:261–271
  52. Esterbauer H, Gebicki J, Puhl H, Jurgens G. The role of lipid peroxidation and antioxidants in oxidative modification of LDL. Free Radic Biol Med. 1992;13:341–390
  53. Swain J, Gutteridge JM. Prooxidant iron and copper, with ferroxidase and xanthine oxidase activities in human atherosclerotic material. FEBS Lett. 1995;368:513–515
  54. Lamb DJ, Leake DS. Acidic pH enables caeruloplasmin to catalyse the modification of low-density lipoprotein. FEBS Lett. 1994;338:122–126
  55. Leake DS, Rankin SM. The oxidative modification of low-density lipoproteins by macrophages. Biochem J. 1990;270:741–748
  56. Kritharides L, Jessup W, Dean RT. Macrophages require both iron and copper to oxidize low-density lipoprotein in Hanks’ balanced salt solution. Arch Biochem Biophys. 1995;323:127–136
  57. Steinbrecher UP, Parthasarathy S, Leake DS, Witztum JL, Steinberg D. Modification of low density lipoprotein by endothelial cells involves lipid peroxidation and degradation of low density lipoprotein phospholipids. Proc Natl Acad Sci USA. 1984;81:3883–3887
  58. Heinecke JW. Oxidized amino acids: culprits in human atherosclerosis and indicators of oxidative stress. Free Radic Biol Med. 2002;32:1090–1101
  59. Stadler N, Lindner RA, Davies MJ. Direct detection and quantification of transition metal ions in human atherosclerotic plaques: evidence for the presence of elevated levels of iron and copper. Arterioscler Thromb Vasc Biol. 2004;24:949–954
  60. Smith C, Mitchinson MJ, Aruoma OI, Halliwell B. Stimulation of lipid peroxidation and hydroxyl-radical generation by the contents of human atherosclerotic lesions. Biochem J. 1992;286(Pt 3):901–905
  61. Fu S, Davies MJ, Stocker R, Dean RT. Evidence for roles of radicals in protein oxidation in advanced human atherosclerotic plaque. Biochem J. 1998;333(Pt 3):519–525
  62. Pietzsch J, Bergmann R. Measurement of 5-hydroxy-2-aminovaleric acid as a specific marker of metal catalysed oxidation of proline and arginine residues of low density lipoprotein apolipoprotein B-100 in human atherosclerotic lesions. J Clin Pathol. 2003;56:622–623

PII: S0021-9150(06)00414-X

doi: 10.1016/j.atherosclerosis.2006.07.017

Atherosclerosis
Volume 192, Issue 2 , Pages 266-274 , June 2007