Does an acidic pH explain why low density lipoprotein is oxidised in atherosclerotic lesions?

Atherosclerosis

Volumn 129, Issue 2, 1997, Pages 149-157

  Leake, David S ^a  

^a UNIVERSITY OF READING   (United Kingdom)

Author keywords

acidic pH; atherosclerosis; caeruloplasmin; copper; iron; low density lipoprotein; oxidized low density lipoprotein; transferrin

Indexed keywords

CERULOPLASMIN; LOW DENSITY LIPOPROTEIN; TRANSFERRIN;

ANIMAL CELL; ATHEROGENESIS; ATHEROSCLEROSIS; INFLAMMATION; ISCHEMIA; LIPID METABOLISM; LIPID OXIDATION; MACROPHAGE; MOUSE; NONHUMAN; PH; PRIORITY JOURNAL; REVIEW;

EID: 0030956262     PISSN: 00219150     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0021-9150(96)06035-2     Document Type: Article

References (100)

1. Berliner, JA, Heinecke, JW. The role of oxidized lipoproteins in atherosclerosis. Free Radic Biol Med 1996;20:707-727.
2. Henriksen T, Mahoney EM, Steinberg D. Enhanced macrophage degradation of low density lipoprotein previously incubated with cultured endothelial cells - recognition by receptors for acetylated low density lipoproteins. Proc Natl Acad Sci USA 1981;78:6499-6503.
3. Henriksen T, Mahoney EM, Steinberg D. Enhanced macrophage degradation of biologically modified low density lipoprotein. Arteriosclerosis 1983;3:149-159.
4. Parthasarathy S, Printz DJ, Boyd D, Joy L, Steinberg D. Macrophage oxidation of low density lipoprotein generates a modified form recognized by the scavenger receptor. Arteriosclerosis 1986;6:505-510.
5. Leake DS, Rankin SM. The oxidative modification of low-density lipoproteins by macrophages. Biochem J 1990;270:741-748.
6. Lamb DJ, Wilkins GM, Leake DS. The oxidative modification of low density lipoprotein by human lymphocytes. Atherosclerosis 1992;92:187-192.
7. Heinecke JW, Rosen H, Chait A. Iron and copper promote modification of low density lipoprotein by human arterial smooth muscle cells in culture. J Clin Invest 1984;74:1890-1894.
8. Lamb DJ, Leake DS. Acidic pH enables caeruloplasmin to catalyse the modification of low-density lipoprotein. FEBS Lett 1994;338:122-126.
9. 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.
10. Parthasarathy S. Oxidation of low-density lipoprotein by thiol compounds leads to its recognition by the acetyl LDL receptor. Biochim Biophys Acta 1987;917:337-340.
11. Winyard PG, Tatzber F, Esterbauer H, Kus ML, Blake DR, Morris CJ. Presence of foam cells containing oxidised low density lipoprotein in the synovial membrane from patients with rheumatoid arthritis. Ann Rheum Dis 1993;52:677-680.
12. Magil AB, Frohlich JJ, Innis SM, Steinbrecher UP. Oxidized low-density lipoprotein in experimental focal glomerulosclerosis. Kidney Int 1993;43:1243-1250.
13. Dabbagh AJ, Frei B. Human suction blister interstitial fluid prevents metal ion-dependent oxidation of low density lipoprotein by macrophages and in cell-free systems. J Clin Invest 1995;96:1958-1966.
14. 2-macroglobulin. Atherosclerosis 1979;34:391-405.
15. Smith EB, Staples EM. Distribution of plasma proteins across the human aortic wall. Barrier functions of endothelium and internal elastic lamina. Atherosclerosis 1980;37:579-590.
16. Morgan J, Leake DS. Acidic pH increases the oxidation of LDL by macrophages. FEBS Lett 1993;333:275-279.
17. Morgan J, Leake DS. The oxidation of low density lipoprotein by iron or copper at acidic pH. J Lipid Res 1995;36:2504-2512.
18. Hessler JR, Morel DW, Lewis LJ, Chisolm GM. Lipoprotein oxidation and lipoprotein-induced cytotoxicity. Arteriosclerosis 1983;3:215-222.
19. Gutteridge JMC. A method for removal of trace iron contamination from biological buffers. FEBS Lett 1987;214:362-364.
20. Bedwell S, Dean RT, Jessup W. The action of defined oxygen-centred free radicals on human low-density lipoprotein. Biochem J 1989;262:707-712.
21. 2 free radicals produced by gamma radiolysis. Radiat Res 1992;132:228-236.
22. Gebicki JM, Bielski BHJ. Comparison of the capacities of the perhydroxyl and the superoxide radicals to initiate chain oxidation of linoleic acid. J Am Chem Soc 1981;103:7020-7022.
23. Halliwell B, Gutteridge JMC. Free Radicals in Biology and Medicine, 2nd edn. Oxford: Clarendon Press, 1989;73-74.
24. Hoff HF, O'Neil J. Structural and functional changes in LDL after modification with both 4-hydroxynonenal and malondialdehyde. J Lipid Res 1993;34:1209-1217.
25. Chang GJ, Woo P, Honda HM et al. Oxidation of LDL to a biologically active form by derivatives of nitric oxide and nitrite in the absence of superoxide:dependence on pH and oxygen. Arterioscler Thromb 1994;14:1808-1814.
26. Daughterty A, Dunn JL, Rateri DL, Heinecke JW. Myeloperoxidase, a catalyst for lipoprotein oxidation, is expressed in human atherosclerotic lesions. J Clin Invest 1994;94:437-444.
27. Savenkova MI, Mueller DM, Heinecke JW. Tyrosyl radical generated by myeloperoxidase is a physiological catalyst for the initiation of lipid peroxidation in low density lipoprotein. J Biol Chem 1994;269:20 394-20 400.
28. Heinecke JW, Li W, Mueller DM, Bohrer A, Turk J. Cholesterol chlorohydrin synthesis by the myeloperoxidase-hydrogen peroxide-chloride system: potential markers for lipoproteins oxidatively damaged by phagocytes. Biochemistry 1994;33:10 127-10 136.
29. Hazell LJ, Arnold L, Flowers D, Waeg G, Malle E, Stocker R. Presence of hypochlorite-modified proteins in human atherosclerotic lesions. J Clin Invest 1996;97:1535-1544.
30. Lentner C. In: Geigy Scientific Tables, Vol. 3. Basle: Ciba-Geigy, 1984;85-86, 145, 147.
31. Welch S. A comparison of the structure and properties of serum transferrin from 17 animal species. Comp Biochem Physiol 1990;97B:417-427.
32. Sipe DM, Murphy RF. Binding to cellular receptors results in increased iron release from transferrin at mildly acidic pH. J Biol Chem 1991;266:8002-8007.
33. El Hage Chahine J-M, Fain D. The mechanism of iron release from transferrin-slow-proton-transfer-induced loss of nitrolotriacetatoiron (III) complex in acidic media. Eur J Biochem 1994;223:581-587.
34. Lamb DJ, Leake DS. Iron released from transferrin at acidic pH can catalyse the oxidation of low density lipoprotein. FEBS Lett 1994;352:15-18.
35. 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;286:901-905.
36. Swain J, Gutteridge JMC. Prooxidant iron and copper, with ferroxidase and xanthine oxidase activities in human atherosclerotic material. FEBS Lett 1995;368:513-515.
37. Lamb DJ, Mitchinson MJ, Leake DS. Transition metal ions within human atherosclerotic lesions can catalyse the oxidation of low density lipoprotein by macrophages. FEBS Lett 1995;374:12-16.
38. Sempos CT, Looker AC, Gillum RF. Iron and heart disease: the epidemiologic data. Nutr Res 1996;54:73-84.
39. Salonen JT, Nyyssönen K, Korpela H, Tuomilehto J, Seppänen R, Salonen R. High stored iron levels are associated with excess risk of myocardial infarction in eastern Finnish men. Circulation 1992;86:803-811.
40. Magnusson MK, Sigfusson N, Sigvaldason H, Johannesson GM, Magnusson S, Thorgeirsson G. Low iron-binding capacity as a risk factor for myocardial infarction. Circulation 1994;89:102-108.
41. Regnström J, Tornvall P, Kallner A, Nilsson J, Hamsten A. Stored iron levels and myocardial infarction at young age. Atherosclerosis 1994;106:123-125.
42. Liao Y, Cooper RS, McGee DL. Iron status and coronary heart disease: negative findings from the NHAMES I epidemiologic follow-up study. Am J Epidemiol 1994;139:704-712.
43. Sempos CT, Looker AC, Gillum RF, Makuc DM. Body iron stores and the risk of coronary heart disease. N Engl J Med 1994;330:1119-1124.
44. Zhang Y, Cliff WJ, Schoefl GI, Higgins G. Immunohistochemical study of intimal microvessels in coronary atherosclerosis. Am J Pathol 1993;143:164-172.
45. Dee G, Rice-Evans C, Obeyesekera S, Meraji S, Jacobs M, Bruckdorfer KR. The modulation of ferryl myoglobin formation and its oxidative effects on low density lipoproteins by nitric oxide. FEBS Lett 1991;294:38-42.
46. Paganga G, Rice-Evans C, Rule R, Leake D. The interaction between ruptured erythrocytes and low-density lipoproteins. FEBS Lett 1992;303:154-158.
47. Musci G, Bonaccorsi di Patti MC, Calabrese L. The state of the copper sites in human ceruloplasmin. Arch Biochem Biophys 1993;306:111-118.
48. Winyard PG, Arundell LA, Blake DR. Lipoprotein oxidation and induction of ferroxidase activity in stored human extracellular fluids. Free Radic Res Comm 1988;5:227-235.
49. Webb J, Kirk KA, Niedermeier W, Griggs JH, Turner ME, James TN. Distribution of 9 trace metals in 17 anatomic sites of dog heart tissue and their classification using pattern recognition. Bioinorg Chem 1977;7:303-314.
50. Ehrenwald E, Chisolm GM, Fox PL. Intact human ceruloplasmin oxidatively modifies low density lipoprotein. J Clin Invest 1994;93:1493-1501.
51. Ehrenwald E, Fox PL. Role of endogenous ceruloplasmin in low density lipoprotein oxidation by human U937 monocytic cells. J Clin Invest 1996;97:884-890.
52. Abdalla DSP, Campa A, Monteiro HP. Low density lipoprotein oxidation by stimulated neutrophils and ferritin. Atherosclerosis 1992;97:149-159.
53. Swain JA, Darley-Usmar V, Gutteridge JMC. Peroxynitrite releases copper from caeruloplasmin: implications for atherosclerosis. FEBS Lett 1994;342:49-52.
54. Salonen JT, Salonen R, Seppänen K, Kartola M, Suntioinen S, Korpela H. Interactions of serum copper, selenium, and low density lipoprotein cholesterol in atherogenesis. Br Med J 1991;302:756-760.
55. Kok FJ, von Duijn CM, Hofman A et al. Serum copper and zinc and the risk of death from cancer and cardiovascular disease. Am J Epidemiol 1988;128:352-359.
56. Reunanen A, Knekt P, Aaran R-K. Serum ceruloplasmin level and the risk of myocardial infarction and stroke. Am J Epidemiol 1992;136:1082-1090.
57. Punsar S, Erämatsä O, Karvonen MJ, Ryhänen A, Hilska P, Vornamo H. Coronary heart disease and drinking water: a search in two Finnish male cohorts for epidemiologic evidence of a water factor. J Chronic Dis 1975;28:259-287.
58. Mabrouk AF, Dugan LR Jr. A kinetic study of the autoxidation of methyl linoleate and linoleic acid emulsions in the presence of sodium chloride. J Am Oil Chem Soc 1960;37:486-490.
59. Wills ED. Mechanisms of lipid peroxide formation in tissues. Role of metals and haematin proteins in the catalysis of the oxidation of unsaturated fatty acids. Biochim Biophys Acta 1965;98:238-251.
60. Wills ED. Mechansisms of lipid peroxide formation in animal tissues. Biochem J 1966;99:667-676.
61. Dianzani MU, Ugazio G. Lipid peroxidation. In: Slater TF (ed). Biochemical Mechanisms of Liver Injury. London: Academic Press, 1978;669-707.
62. Funahashi T, Floyd RA, Carney JM. Age effect on brain pH during ischemia/reperfusion and pH influence on peroxidation. Neurobiol Aging 1994;15:161-167.
63. Bralet J, Bouvier C, Schreiber L, Boquillon M. Effect of acidosis on lipid peroxidation in brain slices. Brain Res 1991;539:175-177.
64. Zimmerman JJ, Lewandoski JR. In vitro phosphatidylcholine peroxidation mediated by activated human neutrophils. Circ Shock 1991;34:231-239.
65. Misík V, Svajdlenka E, Filípek J, Gergel D, Ondrias K. Inhibition of lipid peroxidation of lecithin liposomes kept in a pH-stat system near neutral pH. Free Radic Res Commun 1991;15:159-165.
66. Corliss GA, Dugan LR Jr. Phospholipid oxidation in emulsions. Lipids 1970;5:846-853.
67. Munro JM, van der Walt JD, Munro CS, Chalmers JAC, Cox EL. An immunohistochemical analysis of human aortic fatty steaks. Hum Pathol 1987;18:375-380.
68. Salomon RN, Underwood R, Doyle MV, Wang A, Libby P. Increased apolipoprotein E and c-fms gene experssion without elevated interleukin 1 or 6 mRNA levels indicates selective activation of macrophage functions in advanced human atheroma. Proc Natl Acad Sci USA 1992;89:2814-2818.
69. Takahashi R. Untersuchungen über die chemischen eigenschaften des pneumokokkenempyem-eiters. V. Mitteilung. Uber die Wasserstoffionenkonzentration des pneumokokkenempyemeiters. Orient J Dis Infants 1932;11:22.
70. Menkin V. Studies on inflammation. X. The cytological picture of an inflammatory exudate in relation or its hydrogen ion concentration. Am J Pathol 1934;10:193-210.
71. Kelley WH, Scadron EN, Shinners BM. Hydrogen ion concentration in exudates of pneumococcus infection. Exp Med 1938;67:659-665.
72. Farr M, Garvey K, Bold AM, Kendall MJ, Bacon PA. Significance of the hydrogen ion concentration in synovial fluid in rheumatoid arthritis. Clin Exp Rheumatol 1985;3:99-104.
73. Newsholme P, Gordon S, Newsholme EA. Rates of utilization and fates of glucose, glutamine, pyruvate, fatty acids and ketone bodies by mouse macrophages. Biochem J 1987;242:631-636.
74. Roos D, Loos JA. Changes in the carbohydrate metabolism of mitogenically stimulated human peripheral lymphocytes. II Relative importance of glycolysis and oxidative phosphorylation on phytohaemagglutinin stimulation. Exp Cell Res 1973;77:127-135.
75. Loike JD, Kaback E, Silverstein SC, Steinberg TH. Lactate transport in macrophages. J Immunol 1993;150:1951-1958.
76. Kraig RP, Chesler M. Astrocytic acidosis in hyperglycemia and complete ischemia. J Cereb Blood Flow Metab 1990;10:104-114.
77. Griffiths JR. Are cancer cells acidic? Br J Cancer 1991;64:425-427.
78. Jähde E, Rajewsky MF. Tumor-selective modifcation of cellular microenvironment in vivo: effect of glucose infusion on the pH in normal and malignant rat tissues. Cancer Res 1982;42:1505-1512.
79. Silver IA, Murrills RJ, Etherington DJ. Microelectrode studies on the acid microenvironment beneath adherent macrophages and osteoclasts. Exp Cell Res 1988;175:266-276.
80. +-ATPase. Biochem J 1992;281:245-250.
81. +-ATPases in murine peritoneal macrophages. FEBS Lett 1994;350:82-86.
82. +-ATPase. Am J Physiol 1994;266:L681-L688.
83. Maroudas A, Weinberg PD, Parker KH, Winlove CP. The distribution and diffusivities of small ions in chondroitin sulphate, hyaluronate and some proteoglycan solutions. Biophys Chem 1988;32:257-270.
84. Iverius P-H. The interaction between human plasma lipoproteins and connective tissue glycosaminoglycans. J Biol Chem 1972;247:2607-2613.
85. Hermann M, Gmeiner B. Altered susceptibility to in vitro oxidation of LDL in LDL complexes and LDL aggregates. Arterioscler Thromb 1992;12:1503-1506.
86. Hurt-Camejo E, Camejo G, Rosengren B et al. Effect of arterial proteoglycans and glycosaminoglycans on low density lipoprotein oxidation and its uptake by human macrophages and arterial smooth muscle cells. Arterioscler Thromb 1992;12:569-583.
87. Steinbrecher UP, Lougheed M. Scavenger receptor-independent stimulation of cholesterol esterification in macrophages by low density lipoprotein extracted from human aortic intima. Arterioscler Thromb 1992;12:608-625.
88. Khoo JC, Miller E, McLoughlin P, Steinberg D. Enhanced macrophage uptake of low density lipoprotein after self-aggregation. Arteriosclerosis 1988;8:348-358.
89. Kawabe Y, Cynshi O, Takashima Y, Suzuki T, Ohba Y, Kodama T. Oxidation-induced aggregation of rabbit low-density lipoprotein by azo initiator. Arch Biochem Biophys 1994;310:489-496.
90. Arnold K, Zschornig O. Aggregation of human plasma low density lipoproteins by means of poly(ethylene glycol). Biomed Biochim Acta 1988;47:949-954.
91. Morgan J, Hart D, Leake DS. Aggregation and increased macrophage uptake of LDLs modified by cellular acidic proteases. Atherosclerosis 1994;109:38-39 (Abstract).
92. Leake DS, Rankin SM, Collard J. Macrophage proteases can modifiy low density lipoproteins to increase their uptake by macrophages. FEBS Lett 1990;269:209-212.
93. Leoni P, Dean RT. Mechanisms of lysosomal enzyme secretion by human monocytes. Biochim Biophys Acta 1983;762:378-389.
94. Eagle H. The effect of environmental pH on the growth of normal and malignant cells. J Cell Physiol 1973;82:1-8.
95. Mitchinson MJ, Hothersall DC, Brooks PN, de Burbure CY. The distribution of ceroid in human atherosclerosis. J Pathol 1985;145:177-183.
96. Rosenfeld ME, Palinski W, Ylä-Herttuala S, Butler S, Witztum JL. Distribution of oxidation specific lipid-protein adducts and apolipoprotein B in atherosclerotic lesions of varying severity from WHHL rabbits. Arteriosclerosis 1990;10:336-349.
97. Ball RY, Carpenter KLH, Mitchinson MJ. What is the significance of ceroid in human atherosclerosis? Arch Pathol 1987;111:1134-1140.
98. Ohkuma S, Poole B. Fluorescence probe measurement of intralysosomal pH in living cells and perturbation of pH by various agents. Proc Nat Acad Sci USA 1978;75:3327-3331.
99. Shio H, Farquhar MG, de Duve C. Lysosomes of the arterial wall. IV. Cytochemical localization of acid phosphatase and catalase in smooth muscle cells and foam cells from rabbit atheromatous aorta. Am J Pathol 1974;76:1-17.
100. Zdolsek JM, Svennson I. Effect of reactive oxygen species on lysosomal membrane integrity. A study on a lysosomal fraction. Virchows Arch B Cell Pathol 1993;64:401-406.