Uptake of type IV hypertriglyceridemic VLDL by cultured macrophages is enhanced by interferon-γ

Journal of Lipid Research

Volumn 40, Issue 6, 1999, Pages 1017-1028

  Whitman, Stewart C ^a   Argmann, Carmen A ^a   Sawyez, Cynthia G ^a   Miller, David B ^a   Hegele, Robert A ^a   Huff, Murray W ^a  

^a ROBARTS RESEARCH INSTITUTE   (Canada)

Author keywords

ACAT; Atherosclerosis; Cytokine; J774A.1; Lipid deposition; Lipoprotein; Lipoprotein lipase

Indexed keywords

ALPHA 2 MACROGLOBULIN; APOLIPOPROTEIN; CHOLESTEROL; CHOLESTEROL ESTER; GAMMA INTERFERON; LIPOPROTEIN LIPASE; LOW DENSITY LIPOPROTEIN; SCAVENGER; TRIACYLGLYCEROL; VERY LOW DENSITY LIPOPROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; BINDING AFFINITY; ESTERIFICATION; HUMAN; HYPERTRIGLYCERIDEMIA; LIPID STORAGE; MACROPHAGE FUNCTION; MAJOR HISTOCOMPATIBILITY COMPLEX; MOUSE; NONHUMAN; PRIORITY JOURNAL; SMOOTH MUSCLE FIBER; T LYMPHOCYTE;

ALPHA-MACROGLOBULINS; ANIMALS; APOLIPOPROTEINS E; CELL LINE; CHOLESTEROL ESTERS; ESTERIFICATION; HUMANS; HYPERTRIGLYCERIDEMIA; INTERFERON TYPE II; LIPOPROTEIN LIPASE; LIPOPROTEINS, LDL; LIPOPROTEINS, VLDL; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OXIDATION-REDUCTION; TRIGLYCERIDES;

EID: 0032993208     PISSN: 00222275     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (73)

1. Jonasson, L., J. Holm, O. Skalli, G. Bondjers, and G. K. Hansson. 1986. Regional accumulations of T cells, macrophages, and smooth muscle cells in the human atherosclerotic plaque. Arteriosclerosis. 6: 131-138.
2. Emeson, E. E., and A. L. J. Robertson. 1988. T lymphocytes in aortic and coronary intimas. Their potential role in atherogenesis. Am. J. Pathol. 130: 369-376.
3. Hansson, G. K., L. Jonasson, B. Lojsthed, S. Stemme, O. Kocher, and G. Gabbiani. 1988. Localization of T lymphocytes and macrophages in fibrous and complicated human atherosclerotic plaques. Atherosclerosis. 72: 135-141.
4. Hansson, G. K., J. Holm, and L. Jonasson. 1989. Detection of activated T lymphocytes in human atherosclerotic plaques. Am. J. Pathol. 135: 169-175.
5. Vilcek, J., P. W. Gray, E. Rinderknecht, and C. G. Sevastopoulos. 1985. Interferon-γ: a lymphokine for all seasons. Lymphokines. 11: 1-32.
6. Schreiber, R. D., and A. Celada. 1985. Molecular characterization of interferon-γ as a macrophage activating factor. Lymphokines. 11: 87-118.
7. Geng, Y., J. Holm, S. Nygren, M. Bruzelius, S. Stemme, and G. K. Hansson. 1995. Expression of the macrophage scavenger receptor in atheroma. Relationship to immune activation and the T-cell cytokine interferon-γ. Arterioscler. Thromb. Vasc. Biol. 15: 1995-2002.
8. Hansson, G. K. 1997. Cell-mediated immunity in atherosclerosis. Curr. Opin. Lipidol. 8: 301-311.
9. Fyfe, A. I., J-H. Qiao, and A. J. Lusis. 1994. Immune-deficient mice develop typical atherosclerotic fatty streaks when fed an atherogenic diet. J. Clin. Invest. 94: 2516-2520.
10. Daugherty, A., E. Pure, D. Delfel-Butteiger, S. Shen, J. Leferovich, S. E. Roselaar, and D. J. Rader. 1997. The effects of total lymphocyte deficiency on the extent of atherosclerosis in apolipoprotein E-/-mice. J. Clin. Invest. 100: 1575-1580.
11. Li, H., M. W. Freeman, and P. Libby. 1995. Regulation of smooth muscle cell scavenger receptor expression in vivo by atherogenic diets and in vitro by cytokines. J. Clin. Invest. 95: 122-133.
12. Gong, Q., and R. E. Pitas. 1995. Synergistic effects of growth factors on the regulation of smooth muscle cell scavenger receptor activity. J. Biol. Chem. 270: 21672-21678.
13. Gupta, S., A. M. Poblo, X. Jiang, N. Wang, A. R. Tall, and C. Schindler. 1997. IFN-γ potentiates atherosclerosis in apoE knock-out mice. J. Clin. Invest. 99: 2752-2761.
14. LaMarre, J., B. B. Wolf, E. L. W. Kittler, P. J. Quesenberry, and S. L. Gonias. 1993. Regulation of macrophage α-2-macroglobulin receptor/low density lipoprotein receptor-related protein by lipopolysaccharide and interferon-γ. J. Clin. Invest. 91: 1219-1224.
15. Fong, L. G., T. A. Fong, and A. D. Cooper. 1990. Inhibition of mouse macrophage degradation of acetyl-low density lipoprotein by Interferon-γ. J. Biol. Chem. 265: 11751-11760.
16. Querfeld, U., J. M. Ong, J. Prehn, J. Carty, B. Saffari, S. C. Jordan, and P. A. Kern. 1990. Effects of cytokines on the production of lipoprotein lipase in cultured human macrophages. J. Lipid Res. 31: 1379-1386.
17. Hansson, G. K., M. Hellstraand, L. Rymo, L. Rubbia, and G. Gabbiani. 1989. Interferon-γ inhibits smooth muscle cell proliferation and expression of differentiation-specific α-smooth muscle actin in arterial smooth muscle cells. J. Exp. Med. 170: 1595-1608.
18. Libby, P. 1995. Molecular basis of the acute coronary syndrome. Circulation. 91: 2844-2850.
19. Geng, Y., and G. K. Hansson. 1992. Interferon-γ inhibits scavenger receptor expression and foam cell formation in human monocyte-derived macrophages. J. Clin. Invest. 89: 1322-1330.
20. Brunzell, J. D., H. G. Schrott, A. G. Motulsky, and E. L. Bierman. 1976. Myocardial infarction in the familial forms of hypertriglyceridemia. Metabolism. 25: 313-320.
21. Grundy, S. M., H. Y. I. Mok, L. Zech, D. Steinberg, and M. Berman. 1979. Transport of very low density lipoprotein triglycerides in varying degrees of obesity and hypertriglyceridemia. J. Clin. Invest. 63: 1274-1283.
22. Teng, B., A. D. Sniderman, A. K. Soutar, and G. R. Thompson. 1986. Metabolic basis of hyperapobetalipoproteinemia. Turnover of apolipoprotein B in low density lipoprotein and its precursors and subfractions compared with normal and familial hypercholesterolemia. J. Clin. Invest. 77: 663-672.
23. Sane, T., and E. A. Nikkila. 1988. Very low density lipoprotein triglyceride metabolism in relatives of hypertriglyceridemic probands. Arteriosclerosis. 8: 217-226.
24. Breslow, J. L., and M. Dammerman. 1995. Genetic basis of lipoprotein disorders. Circulation. 91: 505-512.
25. Huff, M. W., A. J. Evans, C. G. Sawyez, B. M. Wolfe, and P. J. Nestel. 1991. Cholesterol accumulation in J774 macrophages induced by triglyceride-rich lipoproteins: a comparison of VLDL from subjects with Types III, IV and V hyperlipoproteinemia. Arterioscler. Thromb. 11: 221-233.
26. Evans, A. J., C. G. Sawyez, B. M. Wolfe, P. W. Connelly, G. F. Maguire, and M. W. Huff. 1993. Evidence that cholesteryl ester and triglyceride accumulation in J774 macrophages induced by very low density subfractions occurs by different mechanisms. J. Lipid Res. 34: 703-717.
27. Gianturco, S. H., W. A. Bradley, A. M. Gotto, J. D. Morrisett, and D. L. Peavy. 1982. Hypertriglyceridemic very low density lipoproteins induce triglyceride synthesis in mouse peritoneal macrophages. J. Clin. Invest. 70: 168-178.
28. Lindqvist, P., A. Ostlund-Lindqvist, J. L. Witztum, D. Steinberg, and J. A. Little. 1983. The role of lipoprotein lipase in the metabolism of triglyceride-rich lipoproteins by macrophages. J. Biol. Chem. 258: 9086-9092.
29. Sacks, F. M., and J. L. Breslow. 1987. Very low density lipoproteins stimulate cholesterol ester formation in U937 macrophages: heterogeneity and biologic variation among normal humans. Arteriosclerosis. 7: 35-46.
30. Bates, S. R., B. A. Coughlin, T. Mazzone, J. Borensztajn, and G. S. Getz. 1987. Apoprotein E mediates the interaction of β-VLDL with macrophages. J. Lipid Res. 28: 787-797.
31. Ishibashi, S., N. Yamada, H. Shimano, N. Mori, H. Mokuno, T. Gotohda, M. Kawakami, T. Murase, and F. Takaku. 1990. Apolipoprotein E and lipoprotein lipase secreted from human monocyte-derived macrophages modulate very low density lipoprotein uptake. J. Biol. Chem. 265: 3040-3047.
32. Granot, E., and S. Eisenberg. 1990. ApoE-3-specific metabolism of human plasma very low density lipoproteins in cultured J-774 macrophages. J. Lipid Res. 31: 2133-2139.
33. Barbir, M., D. Wile, I. Trayner, V. R. Aber, and G. R. Thompson. 1988. High prevalence of hypertriglyceridemia and apolipoprotein abnormalities in coronary artery disease. Br. Heart J. 60: 397-403.
34. Carlson, L. A., and L. E. Bottiger. 1985. Risk factors for heart disease in men and women. Results of the 19-year follow-up of the Stockholm Prospective Study. Acta Med. Scand. 218: 207-211.
35. Castelli, W. P. 1986. The triglyceride issue: a view from Framingham. Am. Heart J. 112: 432-437.
36. Huff, M. W., W. C. Breckenridge, W. L. Strong, and B. M. Wolfe. 1988. Metabolism of apolipoproteins C-II, C-IIIl and B in hypertriglyceridemic men. Changes after heparin-induced lipolysis. Arteriosclerosis. 8: 471-479.
37. Shepherd, J., and C. J. Packard. 1987. Metabolic heterogeneity in very low density lipoproteins. Am. Heart J. 113: 503-508.
38. Reardon, M. F., N. H. Fidge, and P. J. Nestel. 1978. Catabolism of very low density lipoprotein apoprotein B in man. J. Clin. Invest. 61: 850-860.
39. Packard, C. J., A. Munro, R. Lorimer, A. M. Gotto, and J. Shepherd. 1984. Metabolism of apolipoprotein B in large triglyceride-rich very low density lipoproteins of normal and hypertriglyceridemic subjects. J. Clin. Invest. 74: 2178-2192.
40. Havel, R. J., and R. L. Hamilton. 1988. Hepatocytic lipoprotein receptors and intracellular lipoprotein catabolism. Hepatology. 8: 1689-1704.
41. Rapp, J. H., A. Lespine, R. L. Hamilton, N. Colyvas, A. H. Chaumeton, J. Tweedie-Hardman, L. Kotite, S. T. Kunitake, R. J. Havel, and J. P. Kane. 1994. Triglyceride-rich lipoproteins isolated by selected-affinity anti-apolipoprotein B immunosorption from human atherosclerotic plaques. Arterioscler. Thromb. 14: 1767-1774.
42. Schaefer, E. J., and R. I. Levy. 1985. Pathogenesis and management of lipoprotein disorders. N. Engl. J. Med. 312: 1300-1310.
43. Hixson, J. E., and D. T. Vernier. 1990. Restriction isotyping of human apolipoprotein E by gene amplification and cleavage with HhaI. J. Lipid Res. 31: 545-548.
44. Evans, A. J., M. W. Huff, and B. M. Wolfe. 1989. Accumulation of an apo E-poor subfraction of very low density lipoprotein in hypertriglyceridemic men. J. Lipid Res. 30: 1691-1701.
45. Bouthilleir, D. C. F., C. F. Sing, and J. Davignon. 1983. Apolipoprotein E phenotyping with a single gel method: application to the study of informative matings. J. Lipid Res. 24: 1060-1069.
46. Piedrahita, J. A., S. H. Zhang, J. R. Hagaman, P. M. Oliver, and N. Maeda. 1992. Generation of mice earning a mutant apolipoprotein E gene inactivated by gene targeting in embryonic stem cells. Proc. Natl. Acad. Sci. USA. 89: 4471-4475.
47. Evans, A. J., C. G. Sawyez, B. M. Wolfe, and M. W. Huff. 1992. Lipolysis is a prerequisite for lipid accumulation in HepG2 cells induced by large hypertriglyceridemic very low density lipoproteins. J. Biol. Chem. 267: 10743-10751.
48. Markwell, M. A. K., S. M. Haas, L. L. Bieber, and N. E. Tolbert. 1978. A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples. Anal. Biochem. 87: 206-210.
49. Whitman, S. C., D. B. Miller, B. M. Wolfe, R. A. Hegele, and M. W. Huff. 1997. Uptake of type III hypertriglyceridemic VLDL by macrophages is enhanced by oxidation, especially following remnant formation. Arterioscler. Thromb. Vasc. Biol. 17: 1707-1715.
50. Whitman, S. C., C. G. Sawyez, D. B. Miller, B. M. Wolfe, and M. W. Huff. 1998. Oxidized type IV hypertriglyceridemic VLDL-remnants cause greater macrophage cholesteryl ester accumulation than oxidized LDL. J. Lipid Res. 39: 1008-1020.
51. Steinbrecher, U. P., J. L. Witztum, S. Parthasarathy, and D. Steinberg. 1987. Decrease in reactive amino groups during oxidation or endothelial cell modification of LDL. Arteriosclerosis. 7: 135-143.
52. Kleinveld, H. A., H. L. M. Hak-Lemmers, A. F. H. Stalenhoef, and P. N. M. Demacker. 1992. Improved measurement of low density lipoprotein susceptibility to copper-induced oxidation: application of a short procedure for isolating low density lipoprotein. Clin. Chem. 38: 2066-2072.
53. Koo, C., T. L. Innerarity, and R. W. Mahley. 1985. Obligatory role of cholesterol and apolipoprotein E in the formation of large cholesterol-enriched and receptor-active high density lipoproteins. J. Biol. Chem. 260: 11934-11943.
54. Werb, Z., and J. R. Chin. 1983. Onset of apoprotein E secretion during differentiation of mouse bone marrow-derived mononuclear phagocytes. J. Biol. Chem. 97: 1113-1118.
55. Carr, T. P., C. J. Andresen, and L. L. Rudel. 1993. Enzymatic determination of triglyceride, free cholesterol, and total cholesterol in tissue lipid extracts, Clin. Biochem. 26: 39-42.
56. Blache, D., D. Bouthillier, and J. Davignon. 1983. Simple, reproducible procedure for selective measurement of lipoprotein lipase and hepatic lipase. Clin. Chem. 29: 154-158.
57. Hussaini, I. M., J. LaMarre, J. J. Lysiak, L. R. Karns, S. R. Vanden-Berg, and S. L. Gonias. 1996. Transcriptional regulation of LDL receptor-related protein by IFN-γ and the antagonistic activity of TGF-β1 in the RAW 264.7 macrophage-like cell line. J. Leukocyte Biol. 59: 733-739.
58. Goldstein, J. L., S. K. Basu, and M. S. Brown. 1983. Receptor-mediated endocytosis of low-density lipoprotein in cultured cells. Methods Enzymol. 98: 241-260.
59. Takahashi, S., K. Oida, M. Ookubo, J. Suzuki, M. Kohno, T. Murase, T. Yamamoto, and T. Nakai. 1996. Very low density lipoprotein receptor binds apolipoprotein E2/2 as well as apolipoprotein E3/3. FEBS Lett. 386: 197-200.
60. Takahashi, S., J. Suzuki, M. Kohno, K. Oida, T. Tamai, S. Miyabo, T. Yamamoto, and T. Nakai. 1995. Enhancement of the binding of triglyceride-rich lipoproteins to the very low density lipoprotein receptor by apolipoprotein E and lipoprotein lipase. J. Biol. Chem. 270: 15747-15754.
61. Steinberg, D. 1997. Low density lipoprotein oxidation and its pathobiological significance. J. Biol. Chem. 272: 20963-20966.
62. DeMaeyer-Gulgnard, J., and E. DeMaeyer. 1985. Immunomodulation by interferons: recent developments. In Interferon 6. I. Gresser, editor. Academic Press, London. 69-91.
63. Heron, I., M. Hokland, and K. Berg. 1978. Enhanced expression of β2-microglobulin and HLA antigens on human lymphoid cells by interferon. Proc. Natl. Acad. Sci. USA. 75: 6215-6219.
64. Fridman, W. H., I. Gresser, M. T. Bandu, M. Aguet, and C. Neauport-Sautes. 1980. Interferon enhances the expression of Fc-γ receptors. J. Immunol. 124: 2436-2441.
65. Fleischmann, W. R. J., and L. A. Schwarz. 1981. Demonstration of potentiation of the antiviral and antitumor actions of interferon. Methods Enzymol. 79: 432-440.
66. Garotta, G., K. W. Talmadge, J. R. Pink, B. Dewald, and M. Baggiolini. 1986. Functional antagonism between type I and type II interferons on human macrophages. Biochem. Biophys. Res. Commun. 140: 948-954.
67. Zhang, S. H., R. L. Reddick, B. Burkey, and N. Maeda. 1994. Diet-induced atherosclerosis in mice heterozygous and homozygous for apolipoprotein E gene disruption. J. Clin. Invest. 94: 937-945.
68. Hiltunen, T. P., J. S. Luoma, T. Nikkari, and S. Yla-Herttuala. 1998. Expression of LDL receptor, VLDL receptor, LDL receptor-related protein, and scavenger receptor in rabbit atherosclerotic lesions: marked induction of scavenger receptor and VLDL receptor expression during lesion development. Circulation. 97: 1079-1086.
69. van Dijk, K. W., B. J. van Vlijmen, A. van der Zee, B. van't Hof, H. van der Boom, K. Kobayashi, L. Chan, L. Havekes, and M. H. Hofker. 1998. Reversal of hypercholesterolemia in apolipoprotein E2 and apolipoprotein E3-Leiden transgenic mice by adenovirus-mediated gene transfer of the VLDL receptor. Arterioscler. Thromb. Vasc. Biol. 18: 7-12.
70. Kuchenhoff, A., B. Harrach-Ruprecht, and H. Robenek. 1997. Interaction of apoE-containing lipoproteins with the LDL receptor-related protein LRP. Am. J. Physiol. 272: C369-C382.
71. Lougheed, M., C. M. Lum, W. Ling, H. Suzuki, T. Kodama, and U. P. Steinbrecher. 1997. High affinity saturable uptake of oxidized low density lipoprotein by macrophages from mice lacking the scavenger receptor class A type I/II. J. Biol. Chem. 272: 12938-12944.
72. Han, J., D. P. Hajjar, M. Febbraio, and A. C. Nicholson. 1997. Native and modified low density lipoproteins increase the functional expression of the macrophage class B scavenger receptor, CD36. J. Biol. Chem. 272: 21654-21659.
73. Tabas, I. 1997. Free cholesterol-induced cytotoxicity: a possible contributing factor to macrophage foam cell necrosis in advanced atherosclerotic lesions. Trends Cardiovasc. Med. 7: 256-263.