Glycolaldehyde-modified low density lipoprotein leads macrophages to foam cells via the macrophage scavenger receptor

Journal of Biochemistry

Volumn 123, Issue 6, 1998, Pages 1208-1217

  Jinnouchi, Yoshiteru ^a   Sano, Hiroyuki ^a   Nagai, Ryoji ^a   Hakamata, Hideki ^a   Kodama, Tatsuhiko ^b   Suzuki, Hiroshi ^c   Yoshida, Masaki ^a   Ueda, Shoichi ^a   Horiuchi, Seikoh ^a  

^a KUMAMOTO UNIVERSITY   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c CHUGAI PHARMACEUTICAL CO LTD   (Japan)

Author keywords

Advanced glycation end products; Atherosclerosis; Foam cell formation; Maillard reaction; Modified low density lipoprotein

Indexed keywords

ACETYL LOW DENSITY LIPOPROTEIN; ALDEHYDE DERIVATIVE; ANTIBODY; CHOLESTEROL ESTER; LOW DENSITY LIPOPROTEIN; SCAVENGER RECEPTOR;

ANIMAL CELL; ARTICLE; ATHEROSCLEROSIS; CELL INTERACTION; CHO CELL; CONTROLLED STUDY; ENDOCYTOSIS; FLUORESCENCE; FOAM CELL; GLYCATION; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PERITONEUM MACROPHAGE; PHYSICAL CHEMISTRY; PROTEIN DEGRADATION; PROTEIN MODIFICATION;

EID: 0031777742     PISSN: 0021924X     EISSN: None     Source Type: Journal    
DOI: 10.1093/oxfordjournals.jbchem.a022062     Document Type: Article

References (72)

1. Ross, R. (1993) The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature 362, 801-809
2. Steinberg, D., Parthasarathy, S., Carew, T.E., Khoo, J.C., and Witztum, J. (1989) Beyond cholesterol: modifications of low-density lipoprotein that increase its atherogenicity. N. Engl. J. Med. 320, 915-924
3. Palinski, W., Rosenfeld, M.E., Ylä-Herttula, S., Gurtner, G.C., Soccher, S.S., Butler, S.W., Parthasarathy, S., Carew, T.E., and Steinberg, D. (1989) Low density lipoprotein undergoes oxidatively modification in vivo. Proc. Natl. Acad. Sci. USA 86, 1372-1376
4. Ylä-Herttula, S., Palinski, W., Rosenfeld, M.E., Parthasarathy, S., Carew, T.E., Butler, S.W., Witztum, J.L., and Steinberg, D. (1989) Evidence for the presence of oxidatively modified low density lipoprotein in atherosclerotic lesions of rabbit and man. J. Clin. Invest. 84, 1086-1095
5. Stamler, J., Vaccaro, O., Neaton, J.D., and the Multiple Risk Factors Intervention Trials Research Group (1993) Diabetes, other risk factors and 12-y cardiovascular mortality for men screened in the multiple risk factor intervention trial. Diabetes Care 15, 434-444
6. Witztum, J., Mahoney, E.M., Branks, M.J., Fisher, M., Elam, R., and Steinberg, D. (1982) Nonenzymatic glucosylation of low-density lipoprotein alters its biologic activity. Diabetes 31, 283-291
7. Kume, S., Takeya, M., Mori, T., Araki, N., Suzuki, H., Horiuchi, S., Kodama, T., Miyauchi, Y., and Takahashi, K. (1995) Immunohistochemical and ultrastructural detection of advanced glycation end products in atherosclerotic lesions of human aorta with a novel specific monoclonal antibody. Am. J. Pathol. 147, 654-667
8. Araki, N., Higashi, T., Mori, T., Shibayama, R., Kawabe, Y., Kodama, T., Takahashi, K., Shichiri, M., and Horiuchi, S. (1995) Macrophage scavenger receptor mediates the endocytic uptake and degradation of advanced glycation end products of the Maillard reaction. Eur. J. Biochem. 230, 408-415
9. Suzuki, H., Kurihara, Y., Takeya, M., Kamada, N., Kataoka, M., Jishage, K., Ueda, O., Sakaguchi, H., Higashi, T., Suzuki, T., Takashima, Y., Kawabe, Y., Cynshi, O., Wada, Y., Honda, M., Kurihara, H., Aburatani, H., Doi, T., Matsumoto, A., Azuma, S., Noda, T., Toyoda, Y., Itakura, H., Yazaki, Y., Horiuchi, S., Takahashi, K., Kruijt, J.K., van Berkel, T.J.C., Steinbrecher, U.P., Ishibashi, S., Maeda, N., Gordon, S., and Kodama, T. (1997) A role for macrophage scavenger receptors in atherosclerosis and susceptibility to infection. Nature 386, 292-296
10. Glomb, M.A. and Monnier, V.M. (1995) Mechanism of protein modification by glyoxal and glycolaldehyde, reactive intermediates of the Maillard reaction. J. Biol. Chem. 270, 10017-10026
11. Anderson, M.M., Hazen, S.L., Hsu, F.F., and Heinecke, J.W. (1997) Human neutrophils employ the myeloperoxidase-hydrogen peroxide-chloride system to convert hydroxy-amino acids into glycolaldehyde, 2-hydroxypropanal, and acrolein: A mechanism for the generation of highly reactive α-hydroxy and α,β-unsaturated aldehydes by phagocytes at sites of inflammation. J. Clin. Invest. 99, 424-432
12. Thornalley, P., Wolff, S., Crabbe, J., and Stern, A. (1984) The autoxidation of glyceraldehyde and other simple monosaccharides under physiological conditions catalysed by buffer ions. Biochim. Biophys. Acta 797, 276-287
13. Murakami, M., Horiuchi, S., Takata, K., and Morino, Y. (1987) Distinction in the mode of receptor-mediated endocytosis of high density lipoprotein and acetylated high density lipoprotein. J. Biochem. 101, 724-741
14. McFarlane, A.S. (1958) Efficient trace labeling of proteins with iodine. Nature 28, 53
15. Smith, P.K., Krohn, R.I., Hermanson, G.T., Mallia, A.K., Gartner, F.H., Provenzano, M.D., Fujimoto, E.K., Goeke, N.M., Olson, B.J., and Klenk, D.C. (1985) Measurement of protein using bicinchoninic acid. Anal. Biochem. 150, 76-85
16. ε-(Carboxymethyl)lysine protein adduct is a major immunological epitope in proteins modified with advanced glycation end products of the Maillard reaction. Biochemistry 35, 8075-8083
17. Habeeb, A.F.S.A. (1966) Determination of free amino groups in proteins by trinitrobenzenesulfonic acid. Anal. Biochem. 14, 328-336
18. Miyazaki, A., Sakai, M., Suginohara, Y., Hakamata, H., Sakamoto, Y., Morikawa, W., and Horiuchi, S. (1994) Acetylated low density lipoprotein reduces its ligand activity for the scavenger receptor after interaction with reconstituted high density lipoprotein. J. Biol. Chem. 269, 5264-5269
19. Araki, N., Ueno, N., Chacrabarti, B., Morino, Y., and Horiuchi, S. (1992) Immunochemical evidence for the presence of advanced glycation end products in human lens proteins and its positive correlation with aging. J. Biol. Chem. 267, 10211-10214
20. Fong, Y., Edelstein, D., Wang, E.A., and Brownlee, M. (1993) Inhibition of matrix-induced bone differentiation by advanced glycation end-products in rats. Diabetologia 36, 802-807
21. Acharya, A.S. and Manning, J.M. (1983) Reaction of glycolaldehyde with proteins: latent crosslinking potential of α-hydroxyaldehydes. Proc. Natl. Acad. Sci. USA 80, 3590-3594
22. Horiuchi, S., Araki, N., and Morino, Y. (1991) Immunochemical approach to characterize advanced glycation end products of the Maillard reaction: evidence for the presence of a common structure. J. Biol. Chem. 226, 7329-7332
23. Hakamata, H., Miyazaki, A., Sakai, M., Suginohara, Y., Sakamoto, Y., and Horiuchi, S. (1994) Species difference in cholesteryl ester cycle and HDL-induced cholesterol efflux from macrophage foam cells. Arterioscler. Thromb. 14, 1860-1865
24. Freeman, M., Ekkel, Y., Rohrer, L., Penman, M., Freeman, N.J., Chisolm, G.M., and Krieger, M. (1991) Expression of type I and II bovine scavenger receptors in Chinese hamster ovary cells: lipid droplet accumulation and nonreciprocal cross competition by acetylated and oxidized low density lipoprotein. Proc. Natl. Acad. Sci. USA 88, 4931-4935
25. Higashi, T., Sano, H., Saishoji, T., Ikeda, K., Jinnouchi, Y., Kanzaki, T., Morisaki, N., Rauvala, H., Shichiri, M., and Horiuchi, S. (1997) The receptor for advanced glycation end products mediates the chemotaxis of rabbit smooth muscle cells. Diabetes 46, 463-472
26. Suginohara, Y., Miyazaki, A., Hakamata, H., Sakamoto, Y., Ohta, T., Matsuda, I., and Horiuchi, S. (1996) The heparin-bound fraction of human lipoprotein-deficient serum inhibits endocytic uptake of oxidized low density lipoprotein by macrophages. Atherosclerosis 120, 167-179
27. Miyazaki, A., Rahim, A.T.M.A., Araki, S., Morino, Y., and Horiuchi, S. (1991) Chemical cross-linking alters high density lipoprotein to be recognized by a scavenger receptor in rat peritoneal macrophages. Biochim. Biophys. Acta 1082, 143-151
28. Maillard, L.C. (1912) Action des acides amines sur les sucres: formation des melanoidines par voie methodique. C.R. Acad. Sci. III 154, 66-68
29. Finot, P.A. (1982) Modification of proteins. Am. Chem. Soc. 198, 66-68
30. Sell, D.R. and Monnier, V.M. (1989) Structure elucidation of a senescence crosslink from human extracellular matrix: implication of pentoses in the aging process. J. Clin. Invest. 85, 380-384
31. Ienaga, K., Nakamura, K., Hochi, T., Nakazawa, Y., Fukunaga, Y., Kakita, H., and Nakano, K. (1995) Crosslines, fluorophores in the AGE-related cross-linked proteins. Contrib. Nephrol. 112, 42-51
32. Hayase, F., Konishi, Y., and Kato, H. (1995) Identification of the modified structure of arginine residues in proteins with 3-deoxyglucosone, a Maillard reaction intermediate. Biosci. Biotechnol. Biochem. 58, 1953-1955
33. Niwa, T., Katsuzaki, T., Miyazaki, S., Miyazaki, T., Ishizaki, Y., Hayase, F., Tatemichi, N., and Takei, Y. (1997) Immunohistochemical detection of imidazolone, a novel advanced glycation end product, in kidneys and aortas of diabetic patients. J. Clin. Invest. 99, 1272-1280
34. ε-carboxymethyllysine as a degradation products of fructose-lysine in glycated protein. J. Biol. Chem. 261, 4889-4894
35. Hayase, F., Nagaraj, R.H., Miyata, S., Njoroge, F.G., and Monnier, V.M. (1989) Aging of proteins: immunological detection of a glucose-derived pyrrole formed during Maillard reaction in vivo. J. Biol. Chem. 263, 3758-3764
36. Henriksen, T., Mahoney, E.M., and Steinberg, D. (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
37. Steinbrecher, U.P. and Lougheed, M. (1992) Scavenger receptor-independent stimulation of cholesterol esterification in macrophages by low density lipoprotein extracted from human aortic intima. Arterioscler. Thromb. 12, 608-625
38. Monnier, V.M., Kohn, R.R., and Cerami, A. (1984) Accelerated age-related browning of human collagen in diabetes mellitus. Proc. Natl. Acad. Sci. USA 81, 583-587
39. Vlassara, H., Brownlee, M., and Cerami, A. (1984) Accumulation of diabetic rat peritoneal nerve myelin by macrophages increases with the presence of advanced glycosylation end products. J. Exp. Med. 160, 197-207
40. Yamada, K., Nakano, H., Nakayama, M., Nozaki, O., Miura, Y., Suzuki, S., Tuchida, H., Miura, N., Araki, N., and Horiuchi, S. (1994) Immunohistochemical study of human advanced glycosylation end products (AGE) in chronic renal failure. Clin. Nephrol. 42, 354-361
41. Makino, H., Shikata, K., Hironaka, K., Kushiro, M., Yamasaki, Y., Sugimoto, H., Ohta, Z., Araki, N., and Horiuchi, S. (1995) Ultrastructure of nonenzymatically glycated mesangial matrix in diabetic nephropathy. Kidney Int. 48, 517-526
42. Brownlee, M. (1993) Glycation and diabetic complications. Diabetes 43, 836-841
43. Meng, J., Sakata, N., Takebayashi, S., Asano, T., Futata, T., Araki, N., and Horiuchi, S. (1996) Advanced glycation end products of the Maillard reaction in aortic pepsin-insoluble and pepsin-soluble collagen from diabetic rats. Diabetes 45, 1037-1043
44. Horiuchi, S. (1996) Advanced glycation end products (AGE)-modified proteins and their potential relevance to atherosclerosis. Trends Cardiovasc. Med. 6, 163-168
45. 2-Microglobulin modified with advanced glycation end products is a major component of hemodialysis-associated amyloidosis. J. Clin. Invest. 92, 1243-1252
46. 2-microglobulin modified with advanced glycation end products in the pathogenesis of hemodialysis-associated amyloidosis. J. Clin. Invest. 93, 521-528
47. Vitek, M.P., Bhattacharya, K., Glendening, J.M., Stopa, E., Vlassara, H., Bucala, R., Manogue, K., and Cerami, A. (1994) Advanced glycation end products contribute to amyloidosis in Alzheimer disease. Proc. Natl. Acad. Sci. USA 91, 4766-4770
48. Smith, M.A., Taneda, S., Richey, P.L., Miyata, S., Yan, S.D., Stern, D., Sayre, L.M., Monnier, V.M., and Perry, G. (1994) Advanced Maillard reaction end products are associated with Alzheimer disease pathology. Proc. Natl. Acad. Sci. USA 91, 5710-5714
49. Yan, S.D., Chen, X., Schmidt, A.M., Brett, J., Godman, G., Zou, Y.S., Scott, C.W., Caputo, C., Frappier, T., Smith, M.A., Perry, G., Yen, S.H., and Stern, D. (1994) Glycated tau protein in Alzheimer disease: a mechanism for induction of oxidant stress. Proc. Natl. Acad. Sci. USA 91, 7787-7791
50. Kimura, T., Takamatsu, J., Ikeda, K., Kondo, A., Miyakawa, T., and Horiuchi, S. (1996) Accumulation of advanced glycation end products of the Maillard reaction with age in human hippocampal neurons. Neurosci. Lett. 208, 53-56
51. ε-(carboxymethyl)lysine, one of the glycoxidation products' of the Maillard reaction. J. Invest. Dermatol. 108, 797-802
52. Hayashi, T., Mase, S., and Namiki, M. (1985) Formation of the N,N′-dialkylpyrazine cation radical from glyoxal dialkylimine produced on reaction of a sugar with an amine or amino acid. Agric. Biol. Chem. 49, 3131-3137
53. Robinson, T.W., Zhou, H., and Kim, K.J. (1996) Generation of glycolaldehyde from guinea pig airway epithelial monolayers exposed to nitrogen dioxide and its effects on sodium pump activity. Environ. Health Perspect. 104, 852-856
54. Schmidt, A.M., Vianna, M., Gerlach, M., Brett, J., Ryan, J., Kao, J., Esposito, C., Hegarty, H., Hurley, W., Clauss, M., Wang, F., Pan, Y.E., Tsang, T.C., and Stern, D. (1992) Isolation and characterization of two binding proteins for advanced glycosylation end products from bovine lung which are present on the endothelial cell surface. J. Biol. Chem. 267, 14987-14997
55. Neeper, M., Schmidt, A.M., Brett, J., Yan, S.D., Wang, F., Pan, Y.E., Elliston, K., Stern, D., and Shaw, A. (1992) Cloning and expression of a cell surface receptor for advanced glycosylation end products of proteins. J. Biol. Chem. 267, 14998-15004
56. Vlassara, H., Li, Y.M., Imani, F., Wojciechowicz, D., Yang, Z., Liu, F.T., and Cerami, A. (1995) Identification of galectin-3 as a high-affinity binding protein for advanced glycation end products (AGE): a new member of AGE-receptor complex. Mol. Med. 1, 634-646
57. Krieger, M. and Herz, J. (1994) Structures and functions of multiligand lipoprotein receptor: macrophage scavenger receptors and LDL receptor-related protein (LRP). Annu. Rev. Biochem. 63, 601-637
58. Westwood, M.E., Argirov, O.K., and Thornalley, P.J. (1997) Methylglyoxal-modified arginine residues a signal for receptor-mediated endocytosis and degradation of proteins by monocytic THP-1 cells. Biochim. Biophys. Acta 1356, 84-94
59. Cohen, M.P., Lautenslager, G., and Shea, E. (1993) Glycated LDL concentrations in non-diabetic and diabetic subjects measured with monoclonal antibodies reactive with glycated apolipoprotein B epitopes. Eur. J. Clin. Chem. Clin. Biochem. 31, 707-713
60. Steinbrecher, U.P. and Witztum, J.L. (1984) Glycosylation of low-density lipoproteins to an extent comparable to that seen in diabetes slows their catabolism. Diabetes 33, 130-134
61. Lyons, T.J., Li, E., Wells-Knecht, M.C., and Jokl, R. (1994) Toxicity of mildly modified low-density lipoproteins to cultured retinal capillary endothelial cells and pericytes. Diabetes 43, 1090-1095
62. Bucala, R. (1997) Lipoprotein modification by advanced glycosylation endproducts (AGEs): role in atherosclerosis. Trends Cardiovasc. Med. 7, 39-47
63. Bucala, R., Makita, Z., Vega, G., Grundy, S., Koschinsky, T., Cerami, A., and Vlassara, H. (1994) Modification of low density lipoprotein by advanced glycation end products contributes to dyslipidemia of diabetes and renal insufficiency. Proc. Natl. Acad. Sci. USA 91, 9441-9445
64. Takata, K., Horiuchi, S., Araki, N., Shiga, M., Saitoh, M., and Morino, Y. (1988) Endocytic uptake of nonenzymatically glycosylated proteins is mediated by a scavenger receptor for aldehyde-modified proteins. J. Biol. Chem. 263, 14819-14825
65. Smedsrød, B., Melkko, J., Araki, N., Sano, H., and Horiuchi, S. (1997) Advanced glycation end products are eliminated by scavenger-receptor-mediated endocytosis in hepatic sinusoidal Kupffer and endothelial cells. Biochem. J. 322, 567-573
66. Haberland, M.E., Olch, C., and Folgelman, A.M. (1984) Role of lysines in mediating interaction of modified low density lipoproteins with the scavenger receptor of human monocyte macrophages. J. Biol. Chem. 259, 11305-11311
67. Haberland, M.E., Fogelman, A.M., and Edwards, P.A. (1982) Specificity of receptor-mediated recognition of malondialdehyde-modified low density lipoproteins. Proc. Natl. Acad. Sci. USA 79, 1712-1716
68. Bucala, R., Mitchell, R., Arnold, K., Innerarity, T., Vlassara, H., and Cerami, A. (1995) Identification of the major site of apolipoprotein B modification by advanced glycosylation end products blocking uptake by the low density lipoprotein receptor. J. Biol. Chem. 270, 10828-10832
69. Steinberg, D. (1997) Oxidative modification of LDL of and atherogenesis. Circulation 95, 1062-1071
70. Haberland, M.E., Fong, D., and Cheng, L. (1988) Malondialdehyde-altered protein occurs in atheroma of Watanabe heritable hyperlipidemic rabbits. Science 241, 215-218
71. Rosenfeld, M.E. and Ross, R. (1990) Macrophage and smooth muscle cell proliferation in atherosclerotic lesion of WHHL and comparably hypercholesterolemic fat-fed rabbit. Arteriosclerosis 10, 87-92
72. Nakamura, Y., Horii, Y., Nishino, T., Shiiki, H., Sakaguchi, Y., Kagoshima, T., Dohi, K., Makita, Z., Vlassara, H., and Bucala, R. (1993) Immunohistochemical localization of advanced glycosylation endproducts in coronary atheroma and cardiac tissue in diabetes mellitus. Am. J. Pathol. 143, 1649-1656