Scavenger receptors as regulators of natural antibody responses and B cell activation in autoimmunity

Molecular Immunology

Volumn 48, Issue 11, 2011, Pages 1307-1318

  Domange Jordö, Emilie ^a   Wermeling, Fredrik ^a   Chen, Yunying ^a   Karlsson, Mikael C I ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Apoptotic cells; Autoantibodies; B cells; Natural antibodies; Oxidation specific epitopes; Scavenger receptors

Indexed keywords

CD36 ANTIGEN; CD5 ANTIGEN; CD6 ANTIGEN; CXCL16 CHEMOKINE; IMMUNOGLOBULIN M; SCAVENGER RECEPTOR; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 5;

ANTIBODY RESPONSE; ATHEROSCLEROSIS; AUTOIMMUNITY; B LYMPHOCYTE ACTIVATION; HOMEOSTASIS; IMMUNIZATION; IMMUNOLOGY; IMMUNOMODULATION; PRIORITY JOURNAL; REVIEW; SYSTEMIC LUPUS ERYTHEMATOSUS;

ANIMALS; ANTIBODY FORMATION; ATHEROSCLEROSIS; AUTOANTIBODIES; AUTOIMMUNITY; B-LYMPHOCYTES; HUMANS; LUPUS ERYTHEMATOSUS, SYSTEMIC; LYMPHOCYTE ACTIVATION; MICE; RECEPTORS, IMMUNOLOGIC; RECEPTORS, SCAVENGER;

EID: 79956317604     PISSN: 01615890     EISSN: 18729142     Source Type: Journal    
DOI: 10.1016/j.molimm.2011.01.010     Document Type: Review

References (178)

1. Abel S., Hundhausen C., Mentlein R., Schulte A., Berkhout T.A., Broadway N., Hartmann D., Sedlacek R., Dietrich S., Muetze B., Schuster B., Kallen K.J., Saftig P., Rose-John S., Ludwig A. The transmembrane CXC-chemokine ligand 16 is induced by IFN-gamma and TNF-alpha and shed by the activity of the disintegrin-like metalloproteinase ADAM10. J. Immunol. 2004, 172:6362-6372.
2. Afek A., George J., Shoenfeld Y., Gilburd B., Levy Y., Shaish A., Keren P., Janackovic Z., Goldberg I., Kopolovic J., Harats D. Enhancement of atherosclerosis in beta-2-glycoprotein I-immunized apolipoprotein E-deficient mice. Pathobiology 1999, 67:19-25.
3. Ait-Oufella H., Herbin O., Bouaziz J.D., Binder C.J., Uyttenhove C., Laurans L., Taleb S., Van Vre E., Esposito B., Vilar J., Sirvent J., Van Snick J., Tedgui A., Tedder T.F., Mallat Z. B cell depletion reduces the development of atherosclerosis in mice. J. Exp. Med. 2010, 207:1579-1587.
4. Albert M.L., Pearce S.F., Francisco L.M., Sauter B., Roy P., Silverstein R.L., Bhardwaj N. Immature dendritic cells phagocytose apoptotic cells via alphavbeta5 and CD36, and cross-present antigens to cytotoxic T lymphocytes. J. Exp. Med. 1998, 188:1359-1368.
5. Allan L.L., Hoefl K., Zheng D.J., Chung B.K., Kozak F.K., Tan R., van den Elzen P. Apolipoprotein-mediated lipid antigen presentation in B cells provides a pathway for innate help by NKT cells. Blood 2009, 114:2411-2416.
6. Alonso R., Buors C., Le Dantec C., Hillion S., Pers J.O., Saraux A., Montero E., Marianowski R., Loisel S., Devauchelle V., Youinou P., Renaudineau Y. Aberrant expression of CD6 on B-cell subsets from patients with Sjogren's syndrome. J. Autoimmun. 2010, 35:336-341.
7. Ameli S., HultgardhNilsson A., Regnstrom J., Calara F., Yano J., Cercek B., Shah P.K., Nilsson J. Effect of immunization with homologous LDL and oxidized LDL on early atherosclerosis in hypercholesterolemic rabbits. Arteriosc. Thromb. Vasc. Biol. 1996, 16:1074-1079.
8. Areschoug T., Gordon S. Scavenger receptors: role in innate immunity and microbial pathogenesis. Cell Microbiol. 2009, 11:1160-1169.
9. Arredouani M.S., Palecanda A., Koziel H., Huang Y.C., Imrich A., Sulahian T.H., Ning Y.Y., Yang Z., Pikkarainen T., Sankala M., Vargas S.O., Takeya M., Tryggvason K., Kobzik L. MARCO is the major binding receptor for unopsonized particles and bacteria on human alveolar macrophages. J. Immunol. 2005, 175:6058-6064.
10. Avalos A.M., Busconi L., Marshak-Rothstein A. Regulation of autoreactive B cell responses to endogenous TLR ligands. Autoimmunity 2010, 43:76-83.
11. Axtell R.C., Webb M.S., Barnum S.R., Raman C. Cutting edge: critical role for CD5 in experimental autoimmune encephalomyelitis: inhibition of engagement reverses disease in mice. J. Immunol. 2004, 173:2928-2932.
12. Barr T.A., Brown S., Ryan G., Zhao J., Gray D. TLR-mediated stimulation of APC: distinct cytokine responses of B cells and dendritic cells. Eur. J. Immunol. 2007, 37:3040-3053.
13. Barral D.C., Brenner M.B. CD1 antigen presentation: how it works. Nat. Rev. Immunol. 2007, 7:929-941.
14. Barrington R.A., Schneider T.J., Pitcher L.A., Mempel T.R., Ma M., Barteneva N.S., Carroll M.C. Uncoupling CD21 and CD19 of the B-cell coreceptor. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:14490-14495.
15. 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.
16. Binder C.J., Horkko S., Dewan A., Chang M.K., Kieu E.P., Goodyear C.S., Shaw P.X., Palinski W., Witztum J.L., Silverman G.J. Pneumococcal vaccination decreases atherosclerotic lesion formation: molecular mimicry between Streptococcus pneumoniae and oxidized LDL. Nat. Med. 2003, 9:736-743.
17. Binder C.J., Silverman G.J. Natural antibodies and the autoimmunity of atherosclerosis. Springer Semin. Immunopathol. 2005, 26:385-404.
18. Botto M., Dell'Agnola C., Bygrave A.E., Thompson E.M., Cook H.T., Petry F., Loos M., Pandolfi P.P., Walport M.J. Homozygous C1q deficiency causes glomerulonephritis associated with multiple apoptotic bodies. Nat. Genet. 1998, 19:56-59.
19. Boullier A., Gillotte K.L., Horkko S., Green S.R., Friedmann P., Dennis E.A., Witztum J.L., Steinberg D., Quehenberger O. The binding of oxidized low density lipoprotein to mouse CD36 is mediated in part by oxidized phospholipids that are associated with both the lipid and protein moieties of the lipoprotein. J. Biol. Chem. 2000, 275:9163-9169.
20. Bowdish D.M., Sakamoto K., Kim M.J., Kroos M., Mukhopadhyay S., Leifer C.A., Tryggvason K., Gordon S., Russell D.G. MARCO, TLR2, and CD14 are required for macrophage cytokine responses to mycobacterial trehalose dimycolate and Mycobacterium tuberculosis. PLoS Pathog. 2009, 5:e1000474.
21. Bover L.C., Cardo-Vila M., Kuniyasu A., Sun J., Rangel R., Takeya M., Aggarwal B.B., Arap W., Pasqualini R. A previously unrecognized protein-protein interaction between TWEAK and CD163: potential biological implications. J. Immunol. 2007, 178:8183-8194.
22. Bowen M.A., Patel D.D., Li X., Modrell B., Malacko A.R., Wang W.C., Marquardt H., Neubauer M., Pesando J.M., Francke U., et al. Cloning, mapping, and characterization of activated leukocyte-cell adhesion molecule (ALCAM), a CD6 ligand. J. Exp. Med. 1995, 181:2213-2220.
23. Brown J.M., Swindle E.J., Kushnir-Sukhov N.M., Holian A., Metcalfe D.D. Silica-directed mast cell activation is enhanced by scavenger receptors. Am. J. Respir. Cell Mol. Biol. 2007, 36:43-52.
24. Brown M.H., Lacey E. A ligand for CD5 is CD5. J. Immunol. 2010, 185:6068-6074.
25. Bruce I.N. 'Not only ... but also': factors that contribute to accelerated atherosclerosis and premature coronary heart disease in systemic lupus erythematosus. Rheumatology 2005, 44:1492-1502.
26. Caligiuri G., Khallou-Laschet J., Vandaele M., Gaston A.T., Delignat S., Mandet C., Kohler H.V., Kaveri S.V., Nicoletti A. Phosphorylcholine-targeting immunization reduces atherosclerosis. J. Am. Coll. Cardiol. 2007, 50:540-546.
27. Caligiuri G., Nicoletti A., Poirier B., Hansson G.K. Protective immunity against atherosclerosis carried by B cells of hypercholesterolemic mice. J. Clin. Invest. 2002, 109:745-753.
28. Calvo J., Places L., Padilla O., Vila J.M., Vives J., Bowen M.A., Lozano F. Interaction of recombinant and natural soluble CD5 forms with an alternative cell surface ligand. Eur. J. Immunol. 1999, 29:2119-2129.
29. Carsetti R. Characterization of B-cell maturation in the peripheral immune system. Methods Mol. Biol. 2004, 271:25-35.
30. Chang M.K., Bergmark C., Laurila A., Horkko S., Han K.H., Friedman P., Dennis E.A., Witztum J.L. Monoclonal antibodies against oxidized low-density lipoprotein bind to apoptotic cells and inhibit their phagocytosis by elicited macrophages: evidence that oxidation-specific epitopes mediate macrophage recognition. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:6353-6358.
31. Chen Y., Pikkarainen T., Elomaa O., Soininen R., Kodama T., Kraal G., Tryggvason K. Defective microarchitecture of the spleen marginal zone and impaired response to a thymus-independent type 2 antigen in mice lacking scavenger receptors MARCO and SR-A. J. Immunol. 2005, 175:8173-8180.
32. Chen Y., Wermeling F., Sundqvist J., Jonsson A.B., Tryggvason K., Pikkarainen T., Karlsson M.C. A regulatory role for macrophage class A scavenger receptors in TLR4-mediated LPS responses. Eur. J. Immunol. 2010, 40:1451-1460.
33. Chou M.Y., Fogelstrand L., Hartvigsen K., Hansen L.F., Woelkers D., Shaw P.X., Choi J., Perkmann T., Backhed F., Miller Y.I., Horkko S., Corr M., Witztum J.L., Binder C.J. Oxidation-specific epitopes are dominant targets of innate natural antibodies in mice and humans. J. Clin. Invest. 2009, 119:1335-1349.
34. Cinamon G., Zachariah M.A., Lam O.M., Foss F.W., Cyster J.G. Follicular shuttling of marginal zone B cells facilitates antigen transport. Nat. Immunol. 2008, 9:54-62.
35. Cohen N.R., Garg S., Brenner M.B. Antigen Presentation by CD1 lipids, T cells, and NKT cells in microbial immunity. Adv. Immunol. 2009, 102:1-94.
36. Coller S.P., Paulnock D.M. Signaling pathways initiated in macrophages after engagement of type A scavenger receptors. J. Leuko. Biol. 2001, 70:142-148.
37. Corcoran L., Vremec D., Febbraio M., Baldwin T., Handman E. Differential regulation of CD36 expression in antigen-presenting cells: Oct-2 dependence in B lymphocytes but not dendritic cells or macrophages. Int. Immunol. 2002, 14:1099-1104.
38. Covey S.D., Krieger M., Wang W., Penman M., Trigatti B.L. Scavenger receptor class B type I-mediated protection against atherosclerosis in LDL receptor-negative mice involves its expression in bone marrow-derived cells. Arterioscler. Thromb. Vasc. Biol. 2003, 23:1589-1594.
39. Crampton S.R., Voynova E., Bolland S. Innate pathways to B-cell activation and tolerance. Ann. N. Y. Acad. Sci. 2010, 1183:58-68.
40. Dalloul A. CD5: a safeguard against autoimmunity and a shield for cancer cells. Autoimmun. Rev. 2009, 8:349-353.
41. de Faire U., Frostegard J. Natural antibodies against phosphorylcholine in cardiovascular disease. Ann. N. Y. Acad. Sci. 2009, 1173:292-300.
42. de Faire U., Su J., Hua X., Frostegard A., Halldin M., Hellenius M.L., Wikstrom M., Dahlbom I., Gronlund H., Frostegard J. Low levels of IgM antibodies to phosphorylcholine predict cardiovascular disease in 60-year old men: effects on uptake of oxidized LDL in macrophages as a potential mechanism. J. Autoimmun. 2010, 34:73-79.
43. de Winther M.P.J., van Dijk K.W., Havekes L.M., Hofker M.H. Macrophage scavenger receptor class A - a multifunctional receptor in atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 2000, 20:290-297.
44. Delneste Y., Magistrelli G., Gauchat J., Haeuw J., Aubry J., Nakamura K., Kawakami-Honda N., Goetsch L., Sawamura T., Bonnefoy J., Jeannin P. Involvement of LOX-1 in dendritic cell-mediated antigen cross-presentation. Immunity 2002, 17:353-362.
45. Dighiero G., Lymberi P., Mazie J.C., Rouyre S., Butler-Browne G.S., Whalen R.G., Avrameas S. Murine hybridomas secreting natural monoclonal antibodies reacting with self antigens. J. Immunol. 1983, 131:2267-2272.
46. Duan B., Morel L. Role of B-1a cells in autoimmunity. Autoimmun. Rev. 2006, 5:403-408.
47. Duber S., Hafner M., Krey M., Lienenklaus S., Roy B., Hobeika E., Reth M., Buch T., Waisman A., Kretschmer K., Weiss S. Induction of B-cell development in adult mice reveals the ability of bone marrow to produce B-1a cells. Blood 2009, 114:4960-4967.
48. Edfeldt K., Swedenborg J., Hansson G.K., Yan Z.Q. Expression of toll-like receptors in human atherosclerotic lesions: a possible pathway for plaque activation. Circulation 2002, 105:1158-1161.
49. Ehrenstein M.R., O'Keefe T.L., Davies S.L., Neuberger M.S. Targeted gene disruption reveals a role for natural secretory IgM in the maturation of the primary immune response. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:10089-10093.
50. Elomaa O., Kangas M., Sahlberg C., Tuukkanen J., Sormunen R., Liakka A., Thesleff I., Kraal G., Tryggvason K. Cloning of a novel bacteria-binding receptor structurally related to scavenger receptors and expressed in a subset of macrophages. Cell 1995, 80:603-609.
51. Faria-Neto J.R., Chyu K.Y., Li X., Dimayuga P.C., Ferreira C., Yano J., Cercek B., Shah P.K. Passive immunization with monoclonal IgM antibodies against phosphorylcholine reduces accelerated vein graft atherosclerosis in apolipoprotein E-null mice. Atherosclerosis 2006, 189:83-90.
52. Frostegard J. Low level natural antibodies against phosphorylcholine: a novel risk marker and potential mechanism in atherosclerosis and cardiovascular disease. Clin. Immunol. 2010, 134:47-54.
53. Fujita Y., Kakino A., Harada-Shiba M., Sato Y., Otsui K., Yoshimoto R., Sawamura T. C-reactive protein uptake by macrophage cell line via class-A scavenger receptor. Clin. Chem. 2010, 56:478-481.
54. Fukasawa M., Adachi H., Hirota K., Tsujimoto M., Arai H., Inoue K. SRB1, a class B scavenger receptor, recognizes both negatively charged liposomes and apoptotic cells. Exp. Cell Res. 1996, 222:246-250.
55. Garcia-Bates T.M., Baglole C.J., Bernard M.P., Murant T.I., Simpson-Haidaris P.J., Phipps R.P. Peroxisome proliferator-activated receptor gamma ligands enhance human B cell antibody production and differentiation. J. Immunol. 2009, 183:6903-6912.
56. Geng Y.J., Holm J., Nygren S., Bruzelius M., Stemme S., Hansson G.K. Expression of the macrophage scavenger receptor in atheroma. Relationship to immune activation and the T-cell cytokine interferon-gamma. Arterioscler. Thromb. Vasc. Biol. 1995, 15:1995-2002.
57. George J., Afek A., Gilburd B., Blank M., Levy Y., Aron-Maor A., Levkovitz H., Shaish A., Goldberg I., Kopolovic J., Harats D., Shoenfeld Y. Induction of early atherosclerosis in LDL-receptor-deficient mice immunized with beta(2)-glycoprotein I. Circulation 1998, 98:1108-1115.
58. Gibb D.R., El Shikh M., Kang D.J., Rowe W.J., El Sayed R., Cichy J., Yagita H., Tew J.G., Dempsey P.J., Crawford H.C., Conrad D.H. ADAM10 is essential for Notch2-dependent marginal zone B cell development and CD23 cleavage in vivo. J. Exp. Med. 2010, 207:623-635.
59. Gillotte-Taylor K., Boullier A., Witztum J.L., Steinberg D., Quehenberger O. Scavenger receptor class B type I as a receptor for oxidized low density lipoprotein. J. Lipid. Res. 2001, 42:1474-1482.
60. 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. U. S. A. 1979, 76:333-337.
61. Gonzalez S.F., Lukacs-Kornek V., Kuligowski M.P., Pitcher L.A., Degn S.E., Kim Y.A., Cloninger M.J., Martinez-Pomares L., Gordon S., Turley S.J., Carroll M.C. Capture of influenza by medullary dendritic cells via SIGN-R1 is essential for humoral immunity in draining lymph nodes. Nat. Immunol. 2010, 11:427-490.
62. Grabar P. Hypothesis. Auto-antibodies and immunological theories: an analytical review. Clin. Immunol. Immunopathol. 1975, 4:453-466.
63. Granucci F., Petralia F., Urbano M., Citterio S., Di Tota F., Santambrogio L., Ricciardi-Castagnoli P. The scavenger receptor MARCO mediates cytoskeleton rearrangements in dendritic cells and microglia. Blood 2003, 102:2940-2947.
64. Greco T.P., Conti-Kelly A.M., Greco T., Doyle R., Matsuura E., Anthony J.R., Lopez L.R. Newer antiphospholipid antibodies predict adverse outcomes in patients with acute coronary syndrome. Am. J. Clin. Pathol. 2009, 132:613-620.
65. Grolleau A., Misek D.E., Kuick R., Hanash S., Mule J.J. Inducible expression of macrophage receptor Marco by dendritic cells following phagocytic uptake of dead cells uncovered by oligonucleotide arrays. J. Immunol. 2003, 171:2879-2888.
66. Guiducci C., Ott G., Chan J.H., Damon E., Calacsan C., Matray T., Lee K.D., Coffman R.L., Barrat F.J. Properties regulating the nature of the plasmacytoid dendritic cell response to Toll-like receptor 9 activation. J. Exp. Med. 2006, 203:1999-2008.
67. Guo L., Song Z.Q., Li M.T., Wu Q.G., Wang D., Feng H., Bernard P., Daugherty A., Huang B., Li X.A. Scavenger receptor BI protects against septic death through its role in modulating inflammatory response. J. Biol. Chem. 2009, 284:19826-19834.
68. Gursel M., Gursel I., Mostowski H.S., Klinman D.M. CXCL16 influences the nature and specificity of CpG-induced immune activation. J. Immunol. 2006, 177:1575-1580.
69. Han J.H., Hajjar D.P., Febbraio M., Nicholson A.C. Native and modified low density lipoproteins increase the functional expression of the macrophage class B scavenger receptor, CD36. J. Biol. Chem. 1997, 272:21654-21659.
70. Hanayama R., Tanaka M., Miyasaka K., Aozasa K., Koike M., Uchiyama Y., Nagata S. Autoimmune disease and impaired uptake of apoptotic cells in MFG-E8-deficient mice. Science 2004, 304:1147-1150.
71. Harvey B.P., Quan T.E., Rudenga B.J., Roman R.M., Craft J., Mamula M.J. Editing antigen presentation: antigen transfer between human B lymphocytes and macrophages mediated by class A scavenger receptors. J. Immunol. 2008, 181:4043-4051.
72. Hernandez-Vargas P., Ortiz-Munoz G., Lopez-Franco O., Suzuki Y., Gallego-Delgado J., Sanjuan G., Lazaro A., Lopez-Parra V., Ortega L., Egido J., Gomez-Guerrero C. Fc gamma receptor deficiency confers protection against atherosclerosis in apolipoprotein E knockout mice. Circ. Res. 2006, 99:1188-1196.
73. Hippen K.L., Tze L.E., Behrens T.W. CD5 maintains tolerance in anergic B cells. J. Exp. Med. 2000, 191:883-890.
74. Hirano K., Yamashita S., Nakagawa Y., Ohya T., Matsuura F., Tsukamoto K., Okamoto Y., Matsuyama A., Matsumoto K., Miyagawa J., Matsuzawa Y. Expression of human scavenger receptor class B type I in cultured human monocyte-derived macrophages and atherosclerotic lesions. Circ. Res. 1999, 85:108-116.
75. Hogger P., Dreier J., Droste A., Buck F., Sorg C. Identification of the integral membrane protein RM3/1 on human monocytes as a glucocorticoid-inducible member of the scavenger receptor cysteine-rich family (CD163). J. Immunol. 1998, 161:1883-1890.
76. Hooijkaas H., Benner R., Pleasants J.R., Wostmann B.S. Isotypes and specificities of immunoglobulins produced by germ-free mice fed chemically defined ultrafiltered antigen-free diet. Eur. J. Immunol. 1984, 14:1127-1130.
77. Horkko S., Bird D.A., Miller E., Itabe H., Leitinger N., Subbanagounder G., Berliner J.A., Friedman P., Dennis E.A., Curtiss L.K., Palinski W., Witztum J.L. Monoclonal autoantibodies specific for oxidized phospholipids or oxidized phospholipid-protein adducts inhibit macrophage uptake of oxidized low-density lipoproteins. J. Clin. Invest. 1999, 103:117-128.
78. Hsu H.Y., Chiu S.L., Wen M.H., Chen K.Y., Hua K.F. Ligands of macrophage scavenger receptor induce cytokine expression via differential modulation of protein kinase signaling pathways. J. Biol. Chem. 2001, 276:28719-28730.
79. Huh H.Y., Lo S.K., Yesner L.M., Silverstein R.L. CD36 induction on human monocytes upon adhesion to tumor necrosis factor-activated endothelial-cells. J. Biol. Chem. 1995, 270:6267-6271.
80. Janabi M., Yamashita S., Hirano K., Sakai N., Hiraoka H., Matsumoto K., Zhang Z.Y., Nozaki S., Matsuzawa Y. Oxidized LDL-induced NF-kappa B activation and subsequent expression of proinflammatory genes are defective in monocyte-derived macrophages from CD36-deficient patients. Arterioscler. Thromb. Vasc. Biol. 2000, 20:1953-1960.
81. Janeway C.A., Medzhitov R. Innate immune recognition. Annu. Rev. Immunol. 2002, 20:197-216.
82. Jeannin P., Jaillon S., Delneste Y. Pattern recognition receptors in the immune response against dying cells. Curr. Opin. Immunol. 2008, 20:530-537.
83. Joly A.L., Wettstein G., Mignot G., Ghiringhelli F., Garrido C. Dual role of heat shock proteins as regulators of apoptosis and innate immunity. J. Innate. Immun. 2010, 2:238-247.
84. Karlsson M.C., Guinamard R., Bolland S., Sankala M., Steinman R.M., Ravetch J.V. Macrophages control the retention and trafficking of B lymphocytes in the splenic marginal zone. J. Exp. Med. 2003, 198:333-340.
85. Kraal G. Cells in the marginal zone of the spleen. Int. Rev. Cytol. 1992, 132:31-74.
86. Kraal G., Mebius R. New insights into the cell biology of the marginal zone of the spleen. Int. Rev. Cytol. 2006, 250:175-215.
87. Kraal G., van der Laan L.J.W., Elomaa O., Tryggvason K. The macrophage receptor MARCO. Microbes Infect. 2000, 2:313-316.
88. Kuchibhotla S., Vanegas D., Kennedy D.J., Guy E., Nimako G., Morton R.E., Febbraio M. Absence of CD36 protects against atherosclerosis in ApoE knock-out mice with no additional protection provided by absence of scavenger receptor A I/II. Cardiovasc. Res. 2008, 78:185-196.
89. Kunjathoor V.V., Febbraio M., Podrez E.A., Moore K.J., Andersson L., Koehn S., Rhee J.S., Silverstein R., Hoff H.F., Freeman M.W. Scavenger receptors class A-I/II and CD36 are the principal receptors responsible for the uptake of modified low density lipoprotein leading to lipid loading in macrophages. J. Biol. Chem. 2002, 277:49982-49988.
90. Lankester A.C., van Schijndel G.M., Cordell J.L., van Noesel C.J., van Lier R.A. CD5 is associated with the human B cell antigen receptor complex. Eur. J. Immunol. 1994, 24:812-816.
91. Lundberg A.M., Hansson G.K. Innate immune signals in atherosclerosis. Clin. Immunol. 2010, 134:5-24.
92. Luoma J., Hiltunen T., Sarkioja T., Moestrup S.K., Gliemann J., Kodama T., Nikkari T., Yla-Herttuala S. Expression of alpha 2-macroglobulin receptor/low density lipoprotein receptor-related protein and scavenger receptor in human atherosclerotic lesions. J. Clin. Invest. 1994, 93:2014-2021.
93. MacLennan I.C., Toellner K.M., Cunningham A.F., Serre K., Sze D.M., Zuniga E., Cook M.C., Vinuesa C.G. Extrafollicular antibody responses. Immunol. Rev. 2003, 194:8-18.
94. Magalhaes R., Stiehl P., Morawietz L., Berek C., Krenn V. Morphological and molecular pathology of the B cell response in synovitis of rheumatoid arthritis. Virchows Arch. 2002, 441:415-427.
95. Major A.S., Fazio S., Linton M.F. B-Lymphocyte deficiency increases atherosclerosis in LDL receptor-null mice. Arterioscler. Thromb. Vasc. Biol. 2002, 22:1892-1898.
96. Major A.S., Singh R.R., Joyce S., Van Kaer L. The role of invariant natural killer T cells in lupus and atherogenesis. Immunol. Res. 2006, 34:49-66.
97. Marai I., Shechter M., Langevitz P., Gilburd B., Rubenstein A., Matssura E., Sherer Y., Shoenfeld Y. Anti-cardiolipin antibodies and endothelial function in patients with coronary artery disease. Am. J. Cardiol. 2008, 101:1094-1097.
98. Marshak-Rothstein A. Toll-like receptors in systemic autoimmune disease. Nat. Rev. Immunol. 2006, 6:823-835.
99. Martin F., Kearney J.F. B-cell subsets and the mature preimmune repertoire. Marginal zone and B1 B cells as part of a " natural immune memory" Immunol. Rev. 2000, 175:70-79.
100. Martin F., Oliver A.M., Kearney J.F. Marginal zone and B1 B cells unite in the early response against T-independent blood-borne particulate antigens. Immunity 2001, 14:617-629.
101. Martinon F., Mayor A., Tschopp J. The inflammasomes: guardians of the body. Annu. Rev. Immunol. 2009, 27:229-265.
102. Masedunskas A., King J.A., Tan F., Cochran R., Stevens T., Sviridov D., Ofori-Acquah S.F. Activated leukocyte cell adhesion molecule is a component of the endothelial junction involved in transendothelial monocyte migration. FEBS Lett. 2006, 580:2637-2645.
103. Matloubian M., David A., Engel S., Ryan J.E., Cyster J.G. A transmembrane CXC chemokine is a ligand for HIV-coreceptor Bonzo. Nat. Immunol. 2000, 1:298-304.
104. Matsushita N., Komine H., Grolleau-Julius A., Pilon-Thomas S., Mule J.J. Targeting MARCO can lead to enhanced dendritic cell motility and anti-melanoma activity. Cancer Immunol. Immunother. 2010, 59:875-884.
105. Means T.K., Luster A.D. Toll-like receptor activation in the pathogenesis of systemic lupus erythematosus. Ann. N. Y. Acad. Sci. 2005, 1062:242-251.
106. Mevorach D., Zhou J.L., Song X., Elkon K.B. Systemic exposure to irradiated apoptotic cells induces autoantibody production. J. Exp. Med. 1998, 188:387-392.
107. Michelsen K.S., Wong M.H., Zhang W.X., Yano J., Rajavashisth T.B., Doherty T.M., Shah P.K., Arditi M. Toll-like receptor 4 deficiency reduces atherosclerosis and alters plaque phenotype in Apo E-null mice without changing circulating cholesterol levels. Circulation 2004, 110:844.
108. Minami M., Kume N., Shimaoka T., Kataoka H., Hayashida K., Akiyama Y., Nagata I., Ando K., Nobuyoshi M., Hanyuu M., Komeda M., Yonehara S., Kita T. Expression of SR-PSOX, a novel cell-surface scavenger receptor for phosphatidylserine and oxidized LDL in human atherosclerotic lesions. Arterioscler. Thromb. Vasc. Biol. 2001, 21:1796-1800.
109. Mold C., Rodriguez W., Rodic-Polic B., Du Clos T.W. C-reactive protein mediates protection from lipopolysaccharide through interactions with Fc gamma R. J. Immunol. 2002, 169:7019-7025.
110. Moreno J.A., Munoz-Garcia B., Martin-Ventura J.L., Madrigal-Matute J., Orbe J., Paramo J.A., Ortega L., Egido J., Blanco-Colio L.M. The CD163-expressing macrophages recognize and internalize TWEAK: potential consequences in atherosclerosis. Atherosclerosis 2009, 207:103-110.
111. Mosser D.M., Edwards J.P. Exploring the full spectrum of macrophage activation. Nat. Rev. Immunol. 2008, 8:958-969.
112. Muroi K., Toya K., Suzuki T., Suda T., Sakamoto S., Miura Y. Expression of CD11B, CD14 and CD36 antigens by B-cell lymphoma. Br. J. Haematol. 1992, 80:126-127.
113. Muzio M., Bertilaccio M.T.S., Simonetti G., Frenquelli M., Caligaris-Cappio F. The role of Toll-like receptors in chronic B cell malignancies. Leukemia Lymphoma 2009, 50:1573-1580.
114. Nagy L., Tontonoz P., Alvarez J.G.A., Chen H.W., Evans R.M. Oxidized LDL regulates macrophage gene expression through ligand activation of PPAR gamma. Cell 1998, 93:229-240.
115. Nakagawa T., Akagi M., Hoshikawa H., Chen M., Yasuda T., Mukai S., Ohsawa K., Masaki T., Nakamura T., Sawamura T. Lectin-like oxidized low-density lipoprotein receptor 1 mediates leukocyte infiltration and articular cartilage destruction in rat zymosan-induced arthritis. Arthritis Rheum. 2002, 46:2486-2494.
116. Nakayama T., Hieshima K., Izawa D., Tatsumi Y., Kanamaru A., Yoshie O. Cutting edge: profile of chemokine receptor expression on human plasma cells accounts for their efficient recruitment to target tissues. J. Immunol. 2003, 170:1136-1140.
117. Nanki T., Shimaoka T., Hayashida K., Taniguchi K., Yonehara S., Miyasaka N. Pathogenic role of the CXCL16-CXCR6 pathway in rheumatoid arthritis. Arthritis Rheum. 2005, 52:3004-3014.
118. Nicholson A.C. Expression of CD36 in macrophages and atherosclerosis the role of lipid regulation of PPAR-gamma signaling. Trends Cardiovasc. Med. 2004, 14:8-12.
119. Nicholson A.C., Frieda S., Pearce A., Silverstein R.L. Oxidized LDL binds to CD36 on human monocyte-derived macrophages and transfected cell-lines - evidence implicating the lipid moiety of the lipoprotein as the lipoprotein as the binding-site. Arterioscler. Thromb. Vasc. Biol. 1995, 15:269-275.
120. Nickel T., Schmauss D., Hanssen H., Sicic Z., Krebs B., Jankl S., Summo C., Fraunberger P., Walli A.K., Pfeiler S., Weis M. oxLDL uptake by dendritic cells induces upregulation of scavenger-receptors, maturation and differentiation. Atherosclerosis 2009, 205:442-450.
121. Nicoletti A., Caligiuri G., Tornberg I., Kodama T., Stemme S., Hansson G.K. The macrophage scavenger receptor type A directs modified proteins to antigen presentation. Eur. J. Immunol. 1999, 29:512-521.
122. Nilsen N.J., Deininger S., Nonstad U., Skjeldal F., Husebye H., Rodionov D., von Aulock S., Hartung T., Lien E., Bakke O., Espevik T. Cellular trafficking of lipoteichoic acid and Toll-like receptor 2 in relation to signaling: role of CD14 and CD36. J. Leukoc. Biol. 2008, 84:280-291.
123. Osorio L.M., De Santiago A., Aguilar-Santelises M., Mellstedt H., Jondal M. CD6 ligation modulates the Bcl-2/Bax ratio and protects chronic lymphocytic leukemia B cells from apoptosis induced by anti-IgM. Blood 1997, 89:2833-2841.
124. Palinski W., Miller E., Witztum J.L. Immunization of low density lipoprotein (LDL) receptor-deficient rabbits with homologous malondialdehyde-modified LDL reduces atherogenesis. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:821-825.
125. Palm N.W., Medzhitov R. Immunostimulatory activity of haptenated proteins. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:4782-4787.
126. Peng Y., Kowalewski R., Kim S., Elkon K.B. The role of IgM antibodies in the recognition and clearance of apoptotic cells. Mol. Immunol. 2005, 42:781-787.
127. Phan T.G., Grigorova I., Okada T., Cyster J.G. Subcapsular encounter and complement-dependent transport of immune complexes by lymph node B cells. Nat. Immunol. 2007, 8:992-1000.
128. Platt N., Gordon S. Is the class A macrophage scavenger receptor (SR-A) multifunctional? - The mouse's tale. J. Clin. Invest. 2001, 108:649-654.
129. Platt N., Suzuki H., Kodama T., Gordon S. Apoptotic thymocyte clearance in scavenger receptor class A-deficient mice is apparently normal. J. Immunol. 2000, 164:4861-4867.
130. 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. U. S. A. 1996, 93:12456-12460.
131. Pluddemann A., Neyen C., Gordon S. Macrophage scavenger receptors and host-derived ligands. Methods 2007, 43:207-217.
132. Pospisil R., Fitts M.G., Mage R.G. CD5 is a potential selecting ligand for B cell surface immunoglobulin framework region sequences. J. Exp. Med. 1996, 184:1279-1284.
133. Pryshchep O., Ma-Krupa W., Younge B.R., Goronzy J.J., Weyand C.M. Vessel-specific Toll-like receptor profiles in human medium and large arteries. Circulation 2008, 118:1276-1284.
134. Puurunen M., Vaarala O., Julkunen H., Aho K., Palosuo T. Antibodies to phospholipid-binding plasma proteins and occurrence of thrombosis in patients with systemic lupus erythematosus. Clin. Immunol. Immunopathol. 1996, 80:16-22.
135. Rahaman S.O., Lennon D.J., Febbraio M., Podrez E.A., Hazen S.L., Silverstein R.L. A CD36-dependent signaling cascade is necessary for macrophage foam cell formation. Cell Metabol. 2006, 4:211-221.
136. Ramprasad M.P., Terpstra V., Kondratenko N., Quehenberger O., Steinberg D. Cell surface expression of mouse macrosialin and human CD68 and their role as macrophage receptors for oxidized low density lipoprotein. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:14833-14838.
137. Ricote M., Li A.C., Willson T.M., Kelly C.J., Glass C.K. The peroxisome proliferator-activated receptor-gamma is a negative regulator of macrophage activation. Nature 1998, 391:79-82.
138. Rigotti A., Trigatti B., Babitt J., Penman M., Xu S.H., Krieger M. Scavenger receptor BI - a cell surface receptor for high density lipoprotein. Curr. Opin. Lipidol. 1997, 8:181-188.
139. Rogers N.J., Lees M.J., Gabriel L., Maniati E., Rose S.J., Potter P.K., Morley B.J. A defect in Marco expression contributes to systemic lupus erythematosus development via failure to clear apoptotic cells. J. Immunol. 2009, 182:1982-1990.
140. Rubtsov A.V., Swanson C.L., Troy S., Strauch P., Pelanda R., Torres R.M. TLR agonists promote marginal zone B cell activation and facilitate T-dependent IgM responses. J. Immunol. 2008, 180:3882-3888.
141. Rutella S., Rumi C., Puggioni P., Barberi T., Di Mario A., Larocca L.M., Leone G. Expression of thrombospondin receptor (CD36) in B-cell chronic lymphocytic leukemia as an indicator of tumor cell dissemination. Haematologica 1999, 84:419-424.
142. Sakai M., Miyazaki A., Hakamata H., Kodama T., Suzuki H., Kobori S., Shichiri 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. 1996, 271:27346-27352.
143. Santiago-Garcia J., Kodama T., Pitas R.E. The class A scavenger receptor binds to proteoglycans and mediates adhesion of macrophages to the extracellular matrix. J. Biol. Chem. 2003, 278:6942-6946.
144. Sarrias M.R., Farnos M., Mota R., Sanchez-Barbero F., Ibanez A., Gimferrer I., Vera J., Fenutria R., Casals C., Yelamos J., Lozano F. CD6 binds to pathogen-associated molecular patterns and protects from LPS-induced septic shock. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:11724-11729.
145. Sarrias M.R., Gronlund J., Padilla O., Madsen J., Holmskov U., Lozano F. The scavenger receptor cysteine-rich (SRCR) domain: an ancient and highly conserved protein module of the innate immune system. Crit. Rev. Immunol. 2004, 24:1-37.
146. Satoh J., Prabhakar B.S., Haspel M.V., Ginsberg-Fellner F., Notkins A.L. Human monoclonal autoantibodies that react with multiple endocrine organs. N. Engl. J. Med. 1983, 309:217-220.
147. Scott R.S., McMahon E.J., Pop S.M., Reap E.A., Caricchio R., Cohen P.L., Earp H.S., Matsushima G.K. Phagocytosis and clearance of apoptotic cells is mediated by MER. Nature 2001, 411:207-211.
148. Shashkin P., Simpson D., Mishin V., Chesnutt B., Ley K. Expression of CXCL16 in human T cells. Arterioscler. Thromb. Vasc. Biol. 2003, 23:148-149.
149. Shaw P.X., Horkko S., Chang M.K., Curtiss L.K., Palinski W., Silverman G.J., Witztum J.L. Natural antibodies with the T15 idiotype may act in atherosclerosis, apoptotic clearance, and protective immunity. J. Clin. Invest. 2000, 105:1731-1740.
150. Sheikine Y, Sirsjo A. CXCL16/SR-PSOX - a friend or a foe in atherosclerosis?. Atherosclerosis 2008, 197:487-495.
151. Sherer Y., Zinger H., Shoenfeld Y. Atherosclerosis in systemic lupus erythematosus. Autoimmunity 2010, 43:98-102.
152. Silverman G.J., Srikrishnan R., Germar K., Goodyear C.S., Andrews K.A., Ginzler E.M., Tsao B.P. Genetic imprinting of autoantibody repertoires in systemic lupus erythematosus patients. Clin. Exp. Immunol. 2008, 153:102-116.
153. Stewart C.R., Stuart L.M., Wilkinson K., van Gils J.M., Deng J., Halle A., Rayner K.J., Boyer L., Zhong R., Frazier W.A., Lacy-Hulbert A., Khoury J.E., Golenbock D.T., Moore K.J. CD36 ligands promote sterile inflammation through assembly of a Toll-like receptor 4 and 6 heterodimer. Nat. Immunol. 2010, 11:155-161.
154. Su J., Hua X., Concha H., Svenungsson E., Cederholm A., Frostegard J. Natural antibodies against phosphorylcholine as potential protective factors in SLE. Rheumatology 2008, 47:1144-1150.
155. ter Borg E.J., Horst G., Limburg P.C., van Rijswijk M.H., Kallenberg C.G. C-reactive protein levels during disease exacerbations and infections in systemic lupus erythematosus: a prospective longitudinal study. J. Rheumatol. 1990, 17:1642-1648.
156. Torchinsky M.B., Garaude J., Blander J.M. Infection and apoptosis as a combined inflammatory trigger. Curr. Opin. Immunol. 2010, 22:55-62.
157. Trigatti B., Covey S., Rizvi A. Scavenger receptor class B type I in high-density lipoprotein metabolism, atherosclerosis and heart disease: lessons from gene-targeted mice. Biochem. Soc. Trans. 2004, 32:116-120.
158. Van de Velde H., von Hoegen I., Luo W., Parnes J.R., Thielemans K. The B-cell surface protein CD72/Lyb-2 is the ligand for CD5. Nature 1991, 351:662-665.
159. Van Eck M., Bos I.S.T., Hildebrand R.B., Van Rij B.T., Van Berkel T.J.C. Dual role for scavenger receptor class B, type I on bone marrow-derived cells in atherosclerotic lesion development. Am. J. Pathol. 2004, 165:785-794.
160. Van Gorp H., Delputte P.L., Nauwynck H.J. Scavenger receptor CD163, a Jack-of-all-trades and potential target for cell-directed therapy. Mol. Immunol. 2010, 47:1650-1660.
161. Wardemann H., Nussenzweig M.C. B-cell self-tolerance in humans. Adv. Immunol. 2007, 95:83-110.
162. Wardemann H., Yurasov S., Schaefer A., Young J.W., Meffre E., Nussenzweig M.C. Predominant autoantibody production by early human B cell precursors. Science 2003, 301:1374-1377.
163. Watanabe K., Shin E.K., Hashino M., Tachibana M., Watarai M. Toll-like receptor 2 and class B scavenger receptor type I are required for bacterial uptake by trophoblast giant cells. Mol. Immunol. 2010, 47:1989-1996.
164. Weaver L.K., Pioli P.A., Wardwell K., Vogel S.N., Guyre P.M. Up-regulation of human monocyte CD163 upon activation of cell-surface Toll-like receptors. J. Leukoc. Biol. 2007, 81:663-671.
165. Vera J., Fenutria R., Canadas O., Figueras M., Mota R., Sarrias M.R., Williams D.L., Casals C., Yelamos J., Lozano F. The CD5 ectodomain interacts with conserved fungal cell wall components and protects from zymosan-induced septic shock-like syndrome. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:1506-1511.
166. Wermeling F., Chen Y., Pikkarainen T., Scheynius A., Winqvist O., Izui S., Ravetch J.V., Tryggvason K., Karlsson M.C. Class A scavenger receptors regulate tolerance against apoptotic cells, and autoantibodies against these receptors are predictive of systemic lupus. J. Exp. Med. 2007, 204:2259-2265.
167. Wermeling F., Lind S.M., Jordo E.D., Cardell S.L., Karlsson M.C. Invariant NKT cells limit activation of autoreactive CD1d-positive B cells. J. Exp. Med. 2010, 207:943-952.
168. Viau M., Zouali M. B-lymphocytes, innate immunity, and autoimmunity. Clin. Immunol. 2005, 114:17-26.
169. Wilbanks A., Zondlo S.C., Murphy K., Mak S., Soler D., Langdon P., Andrew D.P., Wu L., Briskin M. Expression cloning of the STRL33/BONZO/TYMSTRligand reveals elements of CC, CXC, and CX3C chemokines. J. Immunol. 2001, 166:5145-5154.
170. Voll R.E., Herrmann M., Roth E.A., Stach C., Kalden J.R., Girkontaite I. Immunosuppressive effects of apoptotic cells. Nature 1997, 390:350-351.
171. Won W.J., Bachmann M.F., Kearney J.F. CD36 is differentially expressed on B cell subsets during development and in responses to antigen. J. Immunol. 2008, 180:230-237.
172. Yassin L.M., Londono J., Montoya G., De Sanctis J.B., Rojas M., Ramirez L.A., Garcia L.F., Vasquez G. Atherosclerosis development in SLE patients is not determined by monocytes ability to bind/endocytose Ox-LDL. Autoimmunity 2011, 44:1-10.
173. Yokota T., Ehlin-Henriksson B., Hansson G.K. Scavenger receptors mediate adhesion of activated B lymphocytes. Exp. Cell Res. 1998, 239:16-22.
174. Yung S., Chan T.M. Anti-DNA antibodies in the pathogenesis of lupus nephritis - the emerging mechanisms. Autoimmun. Rev. 2008, 7:317-321.
175. Zhang P., Li W., Wang Y., Hou L., Xing Y., Qin H., Wang J., Liang Y., Han H. Identification of CD36 as a new surface marker of marginal zone B cells by transcriptomic analysis. Mol. Immunol. 2007, 44:332-337.
176. Zhang W.W., Yancey P.G., Su Y.R., Babaev V.R., Zhang Y.M., Fazio S., Linton M.F. Inactivation of macrophage scavenger receptor class B type I promotes atherosclerotic lesion development in apolipoprotein E-deficient mice. Circulation 2003, 108:2258-2263.
177. Zheng T.S., Burkly L.C. No end in site: TWEAK/Fn14 activation and autoimmunity associated-end-organ pathologies. J. Leukoc. Biol. 2008, 84:338-347.
178. Zhu P., Liu X., Treml L.S., Cancro M.P., Freedman B.D. Mechanism and regulatory function of CpG signaling via scavenger receptor B1 in primary B cells. J. Biol. Chem. 2009, 284:22878-22887.