Structure and function of type I and II macrophage scavenger receptors

Mechanisms of Ageing and Development

Volumn 111, Issue 2-3, 1999, Pages 107-121

  Shirai, Heigoro ^a   Murakami, Takeshi ^a   Yamada, Yoshihiko ^a   Doi, Takefumi ^a   Hamakubo, Takao ^a   Kodama, Tatsuhiko ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

Alzheimer's disease; Apoptosis; Atherosclerosis; Cholesterol; Endothelial cell; Host defence; Lipoprotein metabolism; Macrophage

Indexed keywords

AMYLOID BETA PROTEIN; APOLIPOPROTEIN B100; CD36 ANTIGEN; CD68 ANTIGEN; CHOLESTEROL; COLLAGEN; CYSTEINE; LIGAND; LIPOPROTEIN; LOW DENSITY LIPOPROTEIN; MESSENGER RNA; OXYGEN RADICAL; SCAVENGER RECEPTOR;

ALZHEIMER DISEASE; APOPTOSIS; ATHEROSCLEROSIS; CONFERENCE PAPER; ENDOTHELIUM CELL; GENE EXPRESSION; HOST RESISTANCE; HUMAN; LIGAND BINDING; LIPOPROTEIN METABOLISM; MACROPHAGE; NONHUMAN; PRIORITY JOURNAL;

ALZHEIMER DISEASE; APOPTOSIS; ARTERIOSCLEROSIS; CELL ADHESION MOLECULES; CHOLESTEROL; HUMANS; MACROPHAGE ACTIVATION; MOLECULAR STRUCTURE; RECEPTORS, IMMUNOLOGIC; RECEPTORS, SCAVENGER;

EID: 0032719197     PISSN: 00476374     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0047-6374(99)00079-2     Document Type: Conference Paper

References (95)

1. Acton S., Resnick D., Freeman M., Ekkel Y., Ashkenas J., Krieger M. The collagenous domains of macrophage scavenger receptors and complement component C1q mediate their similar, but not identical, binding specificities for polyanionic ligands. J. Biol. Chem. 268:1993;3530-3537.
2. Acton S.L., Scherer P.E., Lodish H.F., Krieger M. Expression cloning of SR-BI, a CD36-related class B scavenger receptor. J. Biol. Chem. 269:1994;21003-21009.
3. Acton S., Rigotti A., Landschulz K.T., Xu S., Hobbs H.H., Krieger M. Identification of scavenger receptor SR-BI as a high density lipoprotein receptor. Science. 271:1996;518-520.
4. Aftring R.P., Freeman M.W. Structure of the murine macrophage scavenger receptor gene and evaluation of sequences that regulate expression in the macrophage cell line, P388D. J. Lipid. Res. 36:1995;1305-1314.
5. Arai H., Kita T., Yokode M., Narumiya S., Kawai C. Multiple receptors for modified low density lipoproteins in mouse peritoneal macrophages: different uptake mechanisms for acetylated and oxidized low densitylipoproteins. Biochem. Biophys. Res. Commun. 159:1989;1375-1382.
6. Araki N., Higashi T., Mori T., Shibayama R., Kawabe Y., Kodama T., Takahashi K. Macrophage scavenger receptor mediates the endocytic uptake and degradation of advanced glycation end products of the Maillard reaction. Eur. J. Biochem. 230:1995;408-415.
7. Auger M.J., Ross J.A. The biology of the macrophages. Lewis C.E.L., McGee J.O.D. The Macrophage. 1991;1-74 IRL press, Oxford.
8. Bell M.D., Lopez-Gonzalez R., Lawson L., Hughes D., Fraser I., Gordon S., Perry V.H. Upregulation of the macrophage scavenger receptor in response to different forms of injury in the CNS. J. Neurocytol. 23:1994;605-613.
9. Berliner J.A., Territo M.C., Sevanian A., Ramin S., Kim J.A., Bamshad B., Esterson M., Fogelman A.M. Minimally modified low density lipoprotein stimulates monocyte endothelial interactions. J. Clin. Invest. 85:1990;1260-1266.
10. Bickel P.E., Freeman M.W. Rabbit aortic smooth muscle cells express inducible macrophage scavenger receptor messenger RNA that is absent from endothelial cells. Clin. Invest. 90:1992;1450-1457.
11. Bodian D.L., Skonier J.E., Bowen M.A., Neubauer M., Siadak A.W., Aruffo A. et al. Identification of residues in CD6 which are critical for ligand binding. Biochemistry. 36:1997;2637-2641.
12. Brown M.S., Basu S.K., Falck J.R., Ho Y.K., Goldstein J.L. The scavenger cell pathway for lipoprotein degradation: specificity of the binding site that mediates the uptake of negatively-charged LDL by macrophages. J. Supramol. Struct. 13:1980;67-81.
13. Brown M.S., Goldstein J.L. Lipoprotein metabolism in the macrophage: implications for cholesterol deposition in atherosclerosis. Annu. Rev. Biochem. 52:1983;223-261.
14. Brown M.S., Goldstein J.L. Atherosclerosis: scavenging for receptors. Nature. 343:1990;508-509.
15. Christie R.H., Freeman M., Hyman B.T. Expression of the macrophage scavenger receptor, a multifunctional lipoprotein receptor, in microglia associated with senile plaques in Alzheimer's disease. Am. J. Pathol. 148:1996;399-403.
16. Daviet L., McGregor J.L. Vascular biology of CD36: roles of this new adhesion molecule family in different disease states. Thromb. Haemost. 78:1997;65-69.
17. Doi T., Higashino K., Kurihara Y., Wada Y., Miyazaki T., Nakamura H. et al. Charged collagen structure mediates the recognition of negatively charged macromolecules by macrophage scavenger receptors. J. Biol. Chem. 268:1993;2126-2133.
18. Doi T., Kurasawa M., Higashino K., Imanishi T., Mori T., Naito M. et al. The histidine interruption of an alpha-helical coiled coil allosterically mediates a pH-dependent ligand dissociation from macrophage scavenger receptors. J. Biol. Chem. 269:1994;25598-25604.
19. Dunne D.W., Resnick D., Greenberg J., Krieger M., Joiner K.A. The type I macrophage scavenger receptor binds to gram-positive bacteria and recognizes lipoteichoic acid. Proc. Natl. Acad. Sci. USA. 91:1994;1863-1867.
20. El Khoury J., Hickman S.E., Thomas C.A., Cao L., Silverstein S.C., Loike J.D. Scavenger receptor-mediated adhesion of microglia to beta-amyloid fibrils. Nature. 382:1996;716-719.
21. Elomaa O., Kangas M., Sahlberg C., Tuukkanen J., Sormunen R., Liakka A. et al. Cloning of a novel bacteria-binding receptor structurally related to scavenger receptors and expressed in a subset of macrophages. Cell. 80:1995;603-609.
22. Emi M., Asaoka H., Matsumoto A., Itakura H., Kurihara Y., Wada Y. Structure, organization, and chromosomal mapping of the human macrophage scavenger receptor gene. J. Biol. Chem. 268:1993;2120-2125.
23. Endemann G., Stanton L.W., Madden K.S., Bryant C.M., White R.T., Protter A.A. CD36 is a receptor for oxidized low density lipoprotein. J. Biol. Chem. 268:1993;11811-11816.
24. Fraser I., Hughes D., Gordon S. Divalent cation-independent macrophage adhesion inhibited by monoclonal antibody to murine scavenger receptor. Nature. 364:1993;343-346.
25. Freeman M., Ashkenas J., Rees D.J., Kingsley D.M., Copeland N.G., Jenkins N.A. et al. An ancient, highly conserved family of cysteine-rich protein domains revealed by cloning type I and II murine macrophage scavenger receptors. Proc. Natl. Acad. Sci. USA. 87:1990;8810-8814.
26. Geng Y.J., Hansson G.K. Interferon-γ inhibits scavenger receptor expression and foam cell formation in human monocyte-derived macrophages. J. Clin. Invest. 89:1991;1322-1330.
27. Geng Y., Kodama T., Hansson G.K. Differential expression of scavenger receptor isoforms during monocyte-macrophage differentiation and foam cell formation. Arterioscler. Thromb. 14:1994;798-806.
28. Geng Y.J., Hansson G.K. High endothelial cells of postcapillary venules express the scavenger receptor in human peripheral lymph nodes. Scand. J. Immunol. 42:1995;289-296.
29. Goldstein J.L., Ho Y.K., Basu S.K., Brown M.S. Binding site on macrophages that mediates uptake and degradation of acetylated low density lipoprotein, producing massive cholesterol deposition. Proc. Natl. Acad. Sci. USA. 76:1979;333-337.
30. Gong Q., Pitas R.E. Synergistic effects of growth factors on the regulation of smooth muscle cell scavenger receptor activity. J. Biol. Chem. 270:1995;21672-21678.
31. Grewal R.P., Yoshida T., Finch C.E., Morgan T.E. Scavenger receptor mRNAs in rat brain microglia are induced by kainic acid lesioning and by cytokines. Neuroreport. 8:1997;1077-1081.
32. Haberland M.E., Fong D., Cheng L. Malondialdehyde-altered protein occurs in atheroma of Watanabe heritable hyperlipidemic rabbits. Science. 241:1988;215-218.
33. Hampton R.Y., Golenbock D.T., Penman M., Krieger M., Raetz C.R. Recognition and plasma clearance of endotoxin by scavenger receptors. Nature. 352:1991;342-344.
34. Holness C.L., da Silva R.P., Fawcett J., Gordon S., Simmons D.L. Macrosialin, a mouse macrophage-restricted glycoprotein, is a member of the lamp/lgp family. J. Biol. Chem. 268:1993;9661-9666.
35. Honda M., Akiyama H., Yamada Y., Kondo H., Kawabe Y., Takeya M. et al. Immunohistochemical evidence for a macrophage scavenger receptor in Mato cells and reactive microglia of ischemia and Alzheimer's disease. Biochem. Biophys. Res. Commun. 245:1998;734-740.
36. Horvai A., Palinski W., Wu H., Moulton K.S., Kalla K., Glass C.K. Scavenger receptor a gene regulatory elements target gene expression to macrophages and to foam cells of atherosclerotic lesions. Proc. Natl. Acad. Sci. USA. 92:1995;5391-5395.
37. Horvai A.E., Xu L., Korzus E., Brard G., Kalafus D., Mullen T.M. Nuclear integration of JAK/STAT and Ras/AP-1 signaling by CBP and p300. Proc. Natl. Acad. Sci. USA. 94:1997;1074-1079.
38. Inaba T., Gotoda T., Shimano H., Shimada M., Harada K., Kozaki K. et al. Platelet-derived growth factor induces c-fms and scavenger receptor genes in vascular smooth muscle cells. J. Biol. Chem. 267:1992;13107-13112.
39. Inaba T., Gotoda T., Harada K., Shimada M., Ohsuga J., Ishibashi S. et al. Induction of sustained expression of proto-oncogene c-fms by platelet-derived growth factor, epidermal growth factor, and basic fibroblast growth factor, and its suppression by interferon-gamma and macrophage colony-stimulating factor in human aortic medial smooth muscle cells. Clin. Invest. 95:1995;1133-1139.
40. Jurgens G., Hoff H.F., Chisolm G.M., Esterbauer H. Modification of human serum low density lipoprotein by oxidation-characterization and pathophysiological implications. Chem. Phys. Lipids. 45:1987;315-336.
41. Kodama T., Reddy P., Kishimoto C., Krieger M. Purification and characterization of a bovine acetyl low density lipoprotein receptor. Proc. Natl. Acad. Sci. USA. 85:1988;9238-9242.
42. Kodama T., Freeman M., Rohrer L., Zabrecky J., Matsudaira P., Krieger M. Type I macrophage scavenger receptor contains alpha-helical and collagen-like coiled coils. Nature. 343:1990;531-535.
43. Kodama T., Doi T., Suzuki H., Takahashi K., Wada Y., Gordon S. Collagenous macrophage scavenger receptors. Curr. Opin. Lipidol. 7:1996;287-291.
44. Kozarsky K.F., Donahee M.H., Rigotti A., Iqbal S.N., Edelman E.R., Krieger M. Over expression of the HDL receptor SR-BI alters plasma HDL and bile cholesterol levels. Nature. 387:1997;414-417.
45. Krieger M. Molecular flypaper and atherosclerosis: structure of the macrophage scavenger receptor. Trends Biochem. Sci. 17:1992;141-146.
46. Krieger M., Herz J. Structure and functions of multiligand lipoprotein receptors: macrophage scavenger receptors and LDL receptor-related proteins. Annu. Rev. Biochem. 63:1994;601-637.
47. Li H., Freeman M.W., Libby P. Regulation of smooth muscle cell scavenger receptor expression in vivo by atherogenic diets and in vitro by cytokines. J. Clin. Invest. 95:1995;122-133.
48. Liao H.S., Kodama T., Doi T., Emi M., Asaoka H., Itakura H., Matsumoto A. Novel elements located at -504 to -399 bp of the promoter region regulated the expression of the human macrophage scavenger receptor gene in murine macrophages. J. Lipid. Res. 38:1997;1433-1444.
49. Ling W., Lougheed M., Suzuki H., Buchan A., Kodama T., Steinbrecher U.P. Oxidized or acetylated low density lipoproteins are rapidly cleared by the liver in mice with disruption of the e scavenger receptor class A type I/II gene. J. Clin. Invest. 100:1997;244-252.
50. Lougheed M., Lum C.M., Ling W., Suzuki H., Kodama T., Steinbrecher U. 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. 272:1997;12938-12944.
51. Luoma J., Hiltunen T., Sarkioja T., Moestrup S.K., Gliemann J., Kodama T. Expression of alpha 2-macroglobulin receptor/low density lipoprotein receptor-related protein and scavenger receptor in human atherosclerotic lesions. J. Clin. Invest. 93:1994;2014-2021.
52. Mato M., Ookawara S., Kurihara K. Uptake of exogenous substances and marked infoldings of the fluorescent granular pericyte in cerebral fine vessels. Am. J. Anat. 157:1980;329-332.
53. Mato M., Ookawara S., Sakamoto A., Aikawa E., Ogawa T., Mitsuhashi U. et al. Involvement of specific macrophage-lineage cells surrounding arterioles in barrier and scavenger function in brain cortex. Proc. Natl. Acad. Sci. USA. 93:1996;3269-3274.
54. Mato M., Ookawara S., Sakamoto A. Growth retardation of Mato's fluorescent granular perithelial (FGP) cells in scavenger receptor knockout (SRKO) mice. Anat. Rec. 247:1997;307-316.
55. Matsumoto A., Naito M., Itakura H., Ikemoto S., Asaoka H., Hayakawa I. et al. Human macrophage scavenger receptors: primary structure, expression, and localization in atherosclerotic lesions. Proc. Natl. Acad. Sci. USA. 87:1990;9133-9137.
56. Mietus-Snyder M., Friera A., Glass C.K., Pitas R.E. Regulation of scavenger receptor expression in smooth muscle cells by protein kinase C: a role for oxidative stress. Arterioscler. Thromb. Vasc. Biol. 17:1997;969-978.
57. Moulton K.S., Wu H., Barnett J., Parthasarathy S., Glass C.K. Regulated expression of the human acetylated low density lipoprotein receptor gene and isolation of promoter sequences. Proc. Natl. Acad. Sci. USA. 89:1992;8102-8106.
58. Moulton K.S., Semple K., Wu H., Glass C.K. Cell-specific expression of the macrophage scavenger receptor gene is dependent on PU.1 and a composite AP-1/ets motif. Mol. Cell. Biol. 14:1994;4408-4418.
59. Naito M., Kodama T., Matsumoto A., Doi T., Takahashi K. Tissue distribution, intracellular localization, and in vitro expression of bovine macrophage scavenger receptors. Am. J. Pathol. 139:1991;1411-1423.
60. Naito M., Suzuki H., Mori T., Matsumoto A., Kodama T., Takahashi K. Coexpression of type I and type II human macrophage scavenger receptors in macrophages of various organs and foam cells in atherosclerotic lesions. Am. J. Pathol. 141:1992;591-599.
61. Paresce D.M., Ghosh R.N., Maxfield F.R. Microglial cells internalize aggregates of the Alzheimer's disease amyloid beta-protein via a scavenger receptor. Neuron. 17:1996;553-565.
62. Pearson A., Lux A., Krieger M. Expression cloning of dSR-CI, a class C macrophage-specific scavenger receptor from Drosophila melanogaster. Proc. Natl. Acad. Sci. USA. 92:1995;4056-4060.
63. Perry V.H., Andersson P.B. The inflammatory response in the CNS. Neuropathol. Appl. Neurobiol. 18:1992;454-459.
64. Perry V.H. Modulation of microglia phenotype. Neuropathol. Appl. Neurobiol. 20:1994;177.
65. Pitas R.E. Expression of the acetyl low density lipoprotein receptor by rabbit fibroblasts and smooth muscle cells: up-regulation by phorbol esters. J. Biol. Chem. 265:1990;12722-12727.
66. Pitas R.E., Friera A., McGuire J., Dejager S. Further characterization of the acetyl LDL (scavenger) receptor expressed by rabbit smooth muscle cells and fibroblasts. Arterioscler. Thromb. 12:1992;1235-1244.
67. Platt N., Suzuki H., Kurihara Y., Kodama T., Gordon S. Role for the class A macrophage scavenger receptor in the phagocytosis of apoptotic thymocytes in vitro. Proc. Natl. Acad. Sci. USA. 93:1996;12456-12460.
68. Ramprasad M.P., Fischer W., Witztum J.L., Sambrano G.R., Quehenberger O., Steinberg D. The 94- to 97-kDa mouse macrophage membrane protein that recognizes oxidized low density lipoprotein and phosphatidylserine-rich liposomes is identical to macrosialin, the mouse homologue of human CD68. Proc. Natl. Acad. Sci. USA. 92:1995;9580-9584.
69. Ren Y., Silverstein R.L., Allen J., Savill J. CD36 gene transfer confers capacity for phagocytosis of cells undergoing apoptosis. J. Exp. Med. 181:1995;1857-1862.
70. Resnick D., Pearson A., Krieger M. The SRCR superfamily: a family reminiscent of the Ig superfamily. Trends. Biochem. Sci. 19:1994;5-8.
71. Resnick D., Chatterton J.E., Schwartz K., Slayter H., Krieger M. Structures of class A macrophage scavenger receptors: electron microscopic study of flexible, multidomain, fibrous proteins and determination of the disulfide bond pattern of the scavenger receptor cysteine-rich domain. J. Biol. Chem. 271:1996;26924-26930.
72. Rigotti A., Acton S.L., Krieger M. The class B scavenger receptors SR-BI and CD36 are receptors for anionic phospholipids. J. Biol. Chem. 270:1995;16221-16224.
73. Rigotti A., Edelma E.R., Seifert P., Iqbal S.N., DeMattos R.B., Temel R.E. et al. Regulation by adrenocorticotropic hormone of the in vivo expression of scavenger receptor class B type I (SR-BI), a high density lipoprotein receptor, in steroidogeniccells of the murine adrenal gland. J. Biol. Chem. 271:1996;33545-33549.
74. Rigotti A., Trigatti B., Babitt J., Penman M., Xu S., Krieger M. Scavenger receptor BI - a cell surface receptor for high density lipoprotein. Curr. Opin. Lipidol. 8:1997;181-188.
75. Rohrer L., Freeman M., Kodama T., Penman M., Krieger M. Coiled-coil fibrous domains mediate ligand binding by macrophage scavenger receptor type II. Nature. 343(6258):1990;570-572.
76. Sakai M., Miyazaki A., Hakamata H., Kodama T., Suzuki H., Kobori S., Schichiri M., Horiuchi S. The scavenger receptor serves as a route for internalization of lysophosphatidylcholine in oxidized low density lipoprotein-induced macrophage proliferation. J. Biol. Chem. 271:1996;27346-27352.
77. Sambrano G.R., Parthasarathy S., Steinberg D. Recognition of oxidatively damaged erythrocytes by a macrophage receptor with specificity for oxidized low density lipoprotein. Proc. Natl. Acad. Sci. USA. 91:1994;3265-3269.
78. Sambrano G.R., Steinberg D. Recognition of oxidatively damaged and apoptotic cells by an oxidized low density lipoprotein receptor on mouse peritoneal macrophages: role of membrane phosphatidylserine. Proc. Natl. Acad. Sci. USA. 92:1995;1396-1400.
79. Sawamura T., Kume N., Aoyama T., Moriwaki H., Hoshikawa H., Aiba Y. et al. An endothelial receptor for oxidized low-density lipoprotein. Nature. 386:1997;73-77.
80. Sparrow C.P., Parthasarathy S., Steinberg D. A macrophage receptor that recognizes oxidized low density lipoprotein but not acetylated low density lipoprotein. J. Biol. Chem. 264:1989;2599-2604.
81. Stanton L.W., White R.T., Bryant C.M., Protter A.A., Endemann G. A macrophage Fc receptor for IgG is also a receptor for oxidized low density lipoprotein. J. Biol. Chem. 267:1992;22446-22451.
82. Steinberg D., Parthasarathy S., Carew T.E., Khoo J.C., Witztum J.L. Beyond cholesterol: modifications of low-density lipoprotein that increase its atherogenicity. N. Engl. J. Med. 320:1989;915-924.
83. Steinbrecher U.P., Parthasarathy S., Leake D.S., Witztum J.L., 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. 81:1984;3883-3887.
84. Suzuki H., Kurihara Y., Takeya M., Kamada N., Kataoka M., Jishage K. et al. A role for macrophage scavenger receptors in atherosclerosis and susceptibility to infection. Nature. 386:1997;292-296.
85. Tanaka T., Wada Y., Nakamura H., Doi T., Imanishi T., Kodama T. A synthetic model of collagen structure taken from bovine macrophage scavenger receptor. FEBS Lett. 334:1993;272-276.
86. Tanaka T., Nishikawa A., Tanaka Y., Nakamura H., Kodama T., Imanishi T., Doi T. Synthetic collagen-like domain derived from the macrophage scavenger receptor binds acetylated low-density lipoprotein in vitro. Protein Eng. 9:1996;307-313.
87. Terpstra V., Kondratenko N., Steinberg D. Macrophages lacking scavenger receptor A show a decrease in binding and uptake of acetylated low-density lipoprotein and of apoptotic thymocytes, but not of oxidatively damaged red blood cells. Proc. Natl. Acad. Sci. USA. 94:1997;8127-8131.
88. Via D.P., Dresel H.A., Cheng S.L., Gotto A.M. Jr Murine macrophage tumors are a source of a 260 000-Da acetyl-low density lipoprotein receptor. J. Biol. Chem. 260:1985;7379-7386.
89. de Villiers W.J., Fraser I.P., Hughes D.A., Doyle A.G., Gordon S. Macrophage-colony-stimulating factor selectively enhances macrophage scavenger receptor expression and function. J. Exp. Med. 180:1994;705-709.
90. de Villiers W.J., Fraser I.P., Gordon S. Cytokine and growth factor regulation of macrophage scavenger receptor expression and function. Immunol. Lett. 43:1994;73-79.
91. Wada Y., Doi T., Matsumoto A., Asaoka H., Honda M., Hatano H. et al. Structure and function of macrophage scavenger receptors. Ann. N.Y. Acad. Sci. 748:1995;226-238.
92. Wu H., Moulton K., Horvai A., Parik S., Glass C.K. Combinatorial interactions between AP-1 and ets domain proteins contribute to the developmental regulation of the macrophage scavenger receptor gene. Mol. Cell. Biol. 14:1994;2129-2139.
93. Yan S.D., Chen X., Fu J., Chen M., Zhu H., Roher A., Slattery T. et al. RAGE and amyloid-beta peptide neurotoxicity in Alzheimer's disease. Nature. 382:1996;685-691.
94. Yla-Herttuala S. Expression of lipoprotein receptors and related molecules in atherosclerotic lesions. Curr. Opin. Lipidol. 7:1996;292-297.
95. Zhang S.H., Reddick R.L., Piedrahita J.A., Maeda N. Spontaneous hypercholesterolemia and arterial lesions in mice lacking apolipoprotein E. Science. 258:1992;468-471.