Conserved domains of the class A scavenger receptors: Evolution and function

Immunological Reviews

Volumn 227, Issue 1, 2009, Pages 19-31

  Bowdish, Dawn M E ^a   Gordon, Siamon ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Comparative immunology evolution; Monocytes macrophages; Phagocytosis; Toll like receptors pattern recognition receptors

Indexed keywords

IMMUNOGLOBULIN RECEPTOR; PROTEIN MARCO; PROTEIN SCARA5; PROTEIN SRCL; SCAVENGER RECEPTOR; SCAVENGER RECEPTOR A; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ATHEROSCLEROSIS; CELL AGGREGATION; CYTOPLASM; GENETIC VARIABILITY; HOMEOSTASIS; HUMAN; NONHUMAN; PATTERN RECOGNITION; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW; SINGLE NUCLEOTIDE POLYMORPHISM;

AMINO ACID SEQUENCE; ANIMALS; CONSERVED SEQUENCE; CYSTEINE; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION; HOST-PATHOGEN INTERACTIONS; HUMANS; LIPID METABOLISM; MACROPHAGES; PHAGOCYTOSIS; POLYMORPHISM, GENETIC; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, IMMUNOLOGIC; SCAVENGER RECEPTORS, CLASS A;

EID: 58049193005     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/j.1600-065X.2008.00728.x     Document Type: Review

References (79)

1. Janeway CA, Medzhitov R. Innate immune recognition. Annu Rev Immunol 2002 20 : 197 216.
2. Roach JC, et al. The evolution of vertebrate Toll-like receptors. Proc Natl Acad Sci USA 2005 102 : 9577 9582.
3. Williams AF, Barclay AN. The immunoglobulin superfamily - domains for cell surface recognition. Annu Rev Immunol 1988 6 : 381 405.
4. Mokady O. Occam's Razor, invertebrate allorecognition and Ig superfamily evolution. Res Immunol 1996 147 : 241 246.
5. Plytycz B, Seljelid R. MHC molecules and lymphocytes: evolutionary perspective. Arch Immunol Ther Exp (Warsz) 1998 46 : 137 142.
6. Peiser L, Mukhopadhyay S, Gordon S. Scavenger receptors in innate immunity. Curr Opin Immunol 2002 14 : 123 128.
7. Aruffo A, et al. CD6-ligand interactions: a paradigm for SRCR domain function? Immunol Today 1997 18 : 498 504.
8. Goldstein JL, Ho YK, Basu SK, Brown MS. Binding site on macrophages that mediates uptake and degradation of acetylated low density lipoprotein, producing massive cholesterol deposition. Proc Natl Acad Sci USA 1979 76 : 333 337.
9. Plüddemann A, Mukhopadhyay S, Gordon S. The interaction of macrophage receptors with bacterial ligands. Expert Rev Mol Med 2006 8 : 1 25.
10. Plüddemann A, Neyen C, Gordon S. Macrophage scavenger receptors and host-derived ligands. Methods 2007 43 : 207 217.
11. Jiang Y, Oliver P, Davies KE, Platt N. Identification and characterization of murine SCARA5, a novel class A scavenger receptor that is expressed by populations of epithelial cells. J Biol Chem 2006 281 : 11834 11845.
12. Dunne DW, Resnick D, Greenberg J, Krieger M, Joiner KA. The type I macrophage scavenger receptor binds to gram-positive bacteria and recognizes lipoteichoic acid. Proc Natl Acad Sci USA 1994 91 : 1863 1867.
13. Hampton RY, Golenbock DT, Penman M, Krieger M, Raetz CR. Recognition and plasma clearance of endotoxin by scavenger receptors. Nature 1991 352 : 342 344.
14. Haworth R, et al. The macrophage scavenger receptor type A is expressed by activated macrophages and protects the host against lethal endotoxic shock. J Exp Med 1997 186 : 1431 1439.
15. Krieger M. Molecular flypaper and atherosclerosis: structure of the macrophage scavenger receptor. Trends Biochem Sci 1992 17 : 141 146.
16. Pearson AM. Scavenger receptors in innate immunity. Curr Opin Immunol 1996 8 : 20 28.
17. Gough PJ, Greaves DR, Gordon S. A naturally occurring isoform of the human macrophage scavenger receptor (SR-A) gene generated by alternative splicing blocks modified LDL uptake. J Lipid Res 1998 39 : 531 543.
18. Peiser L, et al. Identification of Neisseria meningitidis nonlipopolysaccharide ligands for class A macrophage scavenger receptor by using a novel assay. Infect Immun 2006 74 : 5191 5199.
19. de Villiers WJ, Fraser IP, Hughes DA, Doyle AG, Gordon S. Macrophage-colony-stimulating factor selectively enhances macrophage scavenger receptor expression and function. J Exp Med 1994 180 : 705 709.
20. Becker M, Cotena A, Gordon S, Platt N. Expression of the class A macrophage scavenger receptor on specific subpopulations of murine dendritic cells limits their endotoxin response. Eur J Immunol 2006 36 : 950 960.
21. Elomaa O, et al. Structure of the human macrophage MARCO receptor and characterization of its bacteria-binding region. J Biol Chem 1998 273 : 4530 4538.
22. Mukhopadhyay S, Peiser L, Gordon S. Activation of murine macrophages by Neisseria meningitidis and IFN-gamma in vitro: distinct roles of class A scavenger and Toll-like pattern recognition receptors in selective modulation of surface phenotype. J Leukoc Biol 2004 76 : 577 584.
23. van der Laan LJ, et al. Regulation and functional involvement of macrophage scavenger receptor MARCO in clearance of bacteria in vivo. J Immunol 1999 162 : 939 947.
24. van der Laan LJ, et al. Macrophage scavenger receptor MARCO: in vitro and in vivo regulation and involvement in the anti-bacterial host defense. Immunol Lett 1997 57 : 203 208.
25. Seta N, et al. Expression of host defense scavenger receptors in spondylarthropathy. Arthritis Rheum 2001 44 : 931 939.
26. Arredouani M, et al. The scavenger receptor MARCO is required for lung defense against pneumococcal pneumonia and inhaled particles. J Exp Med 2004 200 : 267 272.
27. Milne SA, McGregor AL, McCulloch J, Sharkey J. Increased expression of macrophage receptor with collagenous structure (MARCO) in mouse cortex following middle cerebral artery occlusion. Neurosci Lett 2005 383 : 58 62.
28. Doyle SE, et al. Toll-like receptors induce a phagocytic gene program through p38. J Exp Med 2004 199 : 81 90.
29. Doi T, et al. Charged collagen structure mediates the recognition of negatively charged macromolecules by macrophage scavenger receptors. J Biol Chem 1993 268 : 2126 2133.
30. Nakamura K, Funakoshi H, Miyamoto K, Tokunaga F, Nakamura T. Molecular cloning and functional characterization of a human scavenger receptor with C-type lectin (SRCL), a novel member of a scavenger receptor family. Biochem Biophys Res Commun 2001 280 : 1028 1035.
31. Nakamura K, Funakoshi H, Tokunaga F, Nakamura T. Molecular cloning of a mouse scavenger receptor with C-type lectin (SRCL)(1), a novel member of the scavenger receptor family. Biochim Biophys Acta 2001 1522 : 53 58.
32. Hohenester E, Sasaki T, Timpl R. Crystal structure of a scavenger receptor cysteine-rich domain sheds light on an ancient superfamily. Nat Struct Biol 1999 6 : 228 232.
33. Resnick D, Chatterton JE, 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 1996 271 : 26924 26930.
34. Rodamilans B, et al. Crystal structure of the third extracellular domain of CD5 reveals the fold of a group B scavenger cysteine-rich receptor domain. J Biol Chem 2007 282 : 12669 12677.
35. Graversen JH, Madsen M, Moestrup SK. CD163: a signal receptor scavenging haptoglobin-hemoglobin complexes from plasma. Int J Biochem Cell Biol 2002 34 : 309 314.
36. Madsen M, et al. Molecular characterization of the haptoglobin/hemoglobin receptor CD163. Ligand binding properties of the scavenger receptor cysteine-rich domain region. J Biol Chem 2004 279 : 51561 51567.
37. Hughes DA, Fraser IP, Gordon S. Murine M phi scavenger receptor: adhesion function and expression. Immunol Lett 1994 43 : 7 14.
38. Fraser I, Hughes D, Gordon S. Divalent cation-independent macrophage adhesion inhibited by monoclonal antibody to murine scavenger receptor. Nature 1993 364 : 343 346.
39. Gowen BB, Borg TK, Ghaffar A, Mayer EP. Selective adhesion of macrophages to denatured forms of type I collagen is mediated by scavenger receptors. Matrix Biol 2000 19 : 61 71.
40. Gowen BB, Borg TK, Ghaffar A, Mayer EP. The collagenous domain of class A scavenger receptors is involved in macrophage adhesion to collagens. J Leukoc Biol 2001 69 : 575 582.
41. Andersson L, Freeman MW. Functional changes in scavenger receptor binding conformation are induced by charge mutants spanning the entire collagen domain. J Biol Chem 1998 273 : 19592 19601.
42. Ashkenas J, Penman M, Vasile E, Acton S, Freeman M, Krieger M. Structures and high and low affinity ligand binding properties of murine type I and type II macrophage scavenger receptors. J Lipid Res 1993 34 : 983 1000.
43. Fong LG, Le D. The processing of ligands by the class A scavenger receptor is dependent on signal information located in the cytoplasmic domain. J Biol Chem 1999 274 : 36808 36816.
44. Heider H, Wintergerst ES. Mimicking phosphorylation at Ser-48 strongly reduces surface expression of human macrophage scavenger receptor class A: implications on cell motility. FEBS Lett 2001 505 : 185 190.
45. Kosswig N, Rice S, Daugherty A, Post SR. Class A scavenger receptor-mediated adhesion and internalization require distinct cytoplasmic domains. J Biol Chem 2003 278 : 34219 34225.
46. Blumbach B, et al. The putative sponge aggregation receptor. Isolation and characterization of a molecule composed of scavenger receptor cysteine-rich domains and short consensus repeats. J Cell Sci 1998 111 : 2635 2644.
47. Davis RS, et al. Fc receptor homologs: newest members of a remarkably diverse Fc receptor gene family. Immunol Rev 2002 190 : 123 136.
48. Endo Y, Matsushita M, Fujita T. Role of ficolin in innate immunity and its molecular basis. Immunobiology 2007 212 : 371 379.
49. Sekine H, et al. An ancient lectin-dependent complement system in an ascidian:novel lectin isolated from the plasma of the solitary ascidian, Halocynthia roretzi. J Immunol 2001 167 : 4504 4510.
50. Kenjo A, et al. Cloning and characterization of novel ficolins from the solitary ascidian, Halocynthia roretzi. J Biol Chem 2001 276 : 19959 19965.
51. Endo Y, et al. Origin of mannose-binding lectin-associated serine protease (MASP)-1 and MASP-3 involved in the lectin complement pathway traced back to the invertebrate, amphioxus. J Immunol 2003 170 : 4701 4707.
52. Fujita T, Matsushita M, Endo Y. The lectin-complement pathway - its role in innate immunity and evolution. Immunol Rev 2004 198 : 185 202.
53. Matsushita M, et al. Origin of the classical complement pathway: Lamprey orthologue of mammalian C1q acts as a lectin. Proc Natl Acad Sci USA 2004 101 : 10127 10131.
54. Karlsson MC, Guinamard R, Bolland S, Sankala M, Steinman RM, Ravetch JV. Macrophages control the retention and trafficking of B lymphocytes in the splenic marginal zone. J Exp Med 2003 198 : 333 340.
55. Harshyne LA, Zimmer MI, Watkins SC, Barratt-Boyes SM. A role for class A scavenger receptor in dendritic cell nibbling from live cells. J Immunol 2003 170 : 2302 2309.
56. Freeman M, et al. An ancient, highly conserved family of cysteine-rich protein domains revealed by cloning type I and type II murine macrophage scavenger receptors. Proc Natl Acad Sci USA 1990 87 : 8810 8814.
57. Murphy JE, Tedbury PR, Homer-Vanniasinkam S, Walker JH, Ponnambalam S. Biochemistry and cell biology of mammalian scavenger receptors. Atherosclerosis 2005 182 : 1 15.
58. Pancer Z, Munkner J, Muller I, Muller WE. A novel member of an ancient superfamily: sponge (Geodia cydonium, Porifera) putative protein that features scavenger receptor cysteine-rich repeats. Gene 1997 193 : 211 218.
59. Kaur H, Jaso-Friedmann L, Evans DL. Identification of a scavenger receptor homologue on nonspecific cytotoxic cells and evidence for binding to oligodeoxyguanosine. Fish Shellfish Immunol 2003 15 : 169 181.
60. Froystad MK, Rode M, Berg T, Gjoen T. A role for scavenger receptors in phagocytosis of protein-coated particles in rainbow trout head kidney macrophages. Dev Comp Immunol 1998 22 : 533 549.
61. Pancer Z. Dynamic expression of multiple scavenger receptor cysteine-rich genes in coelomocytes of the purple sea urchin. Proc Natl Acad Sci USA 2000 97 : 13156 13161.
62. Pahler S, Blumbach B, Muller I, Muller EW. Putative multiadhesive protein from the marine sponge Geodia cydonium: cloning of the cDNA encoding a fibronectin-, an SRCR-, and a complement control protein module. J Exp Zool 1998 282 : 332 343.
63. Wheeler GL, Miranda-Saavedra D, Barton GJ. Genome analysis of the unicellular green alga Chlamydomonas reinhardtii indicates an ancient evolutionary origin for key pattern recognition and cell-signaling protein families. Genetics 2008 179 : 193 197.
64. Suzuki H, et al. A role for macrophage scavenger receptors in atherosclerosis and susceptibility to infection. Nature 1997 386 : 292 296.
65. Thomas CA, Li Y, Kodama T, Suzuki H, Silverstein SC, El Khoury J. Protection from lethal Gram-positive infection by macrophage scavenger receptor-dependent phagocytosis. J Exp Med 2000 191 : 147 156.
66. Paresce DM, Ghosh RN, Maxfield FR. Microglial cells internalize aggregates of the Alzheimer's disease amyloid beta-protein via a scavenger receptor. Neuron 1996 17 : 553 565.
67. El Khoury J, Hickman SE, Thomas CA, Cao L, Silverstein SC, Loike JD. Scavenger receptor-mediated adhesion of microglia to beta-amyloid fibrils. Nature 1996 382 : 716 719.
68. Xu J, et al. Germline mutations and sequence variants of the macrophage scavenger receptor 1 gene are associated with prostate cancer risk. Nat Genet 2002 32 : 321 325.
69. Xu J, et al. Common sequence variants of the macrophage scavenger receptor 1 gene are associated with prostate cancer risk. Am J Hum Genet 2003 72 : 208 212.
70. Murabito JM, et al. A genome-wide association study of breast and prostate cancer in the NHLBI's Framingham Heart Study. BMC Med Genet 2007 8 (Suppl. S6.
71. Engert JC, et al. Identification of a chromosome 8p locus for early-onset coronary heart disease in a French Canadian population. Eur J Hum Genet 2008 16 : 105 114.
72. Hersh CP, et al. Genetic linkage and association analysis of COPD-related traits on chromosome 8p. COPD 2006 3 : 189 194.
73. Chen YC, Giovannucci E, Kraft P, Hunter DJ. Association between genetic polymorphisms of macrophage scavenger receptor 1 gene and risk of prostate cancer in the health professionals follow-up study. Cancer Epidemiol Biomarkers Prev 2008 17 : 1001 1003.
74. Hsing AW, et al. MSR1 variants and the risks of prostate cancer and benign prostatic hyperplasia: a population-based study in China. Carcinogenesis 2007 28 : 2530 2536.
75. Miller DC, et al. Germ-line mutations of the macrophage scavenger receptor 1 gene: association with prostate cancer risk in African-American men. Cancer Res 2003 63 : 3486 3489.
76. Robertson G, et al. cisRED: a database system for genome-scale computational discovery of regulatory elements. Nucleic Acids Res 2006 34 : D68 D73.
77. King DC, Taylor J, Elnitski L, Chiaromonte F, Miller F, Hardison RD. Evaluation of regulatory potential and conservation scores for detecting cis-regulatory modules in aligned mammalian genome sequences. Genome Res 2005 15 : 1051 1060.
78. Taylor J, Tyekucheva S, King DC, Hardison RC, Miller W, Chiaromonte F. ESPERR: learning strong and weak signals in genomic sequence alignments to identify functional elements. Genome Res 2006 16 : 1596 1604.
79. The International HapMap Consortium. The International HapMap Project. Nature 2003 426 : 789 796.