IgM antibodies to apoptosis-associated determinants recruit C1q and enhance dendritic cell phagocytosis of apoptotic cells

Journal of Immunology

Volumn 182, Issue 10, 2009, Pages 6031-6043

  Chen, Yifang ^a   Park, Yong Beom ^a   Patel, Ekta ^a   Silverman, Gregg J ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENT COMPONENT C1Q; EPITOPE; IMMUNOGLOBULIN M ANTIBODY; MALONALDEHYDE; PHOSPHORYLCHOLINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN BINDING; APOPTOSIS; ARTICLE; CELL INTERACTION; CONTROLLED STUDY; DENDRITIC CELL; EXPOSURE; GENE; INHERITANCE; INNATE IMMUNITY; MOUSE; NONHUMAN; OPSONIZATION; OXIDATION; PHAGOCYTOSIS; PRIORITY JOURNAL; PRODUCTIVITY; THYMOCYTE;

ANIMALS; APOPTOSIS; AUTOANTIBODIES; AUTOANTIGENS; COMPLEMENT C1Q; DENDRITIC CELLS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOGLOBULIN M; MALE; MALONDIALDEHYDE; MICE; MICE, CONGENIC; OXIDATION-REDUCTION; PHAGOCYTOSIS; PHOSPHORYLCHOLINE;

EID: 70449710443     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0804191     Document Type: Article

References (71)

1. Steinman, R. M., D. Hawiger, and M. C. Nussenzweig. 2003. Tolerogenic dendritic cells. Annu. Rev. Immunol. 21: 685-711.
2. + T cells produce active immune unresponsiveness. J. Immunol. 168: 5589-5595.
3. Steinman, R. M., S. Turley, I. Mellman, and K. Inaba. 2000. The induction of tolerance by dendritic cells that have captured apoptotic cells. J. Exp. Med. 191: 411-416.
4. Takahashi, M., and Y. Kobayashi. 2003. Cytokine production in association with phagocytosis of apoptotic cells by immature dendritic cells. Cell. Immunol. 226: 105-115. (Pubitemid 38220837)
5. Fraser, D. A., and A. J. Tenner. 2008. Directing an appropriate immune response: the role of defense collagens and other soluble pattern recognition molecules. Curr. Drug Targets 9: 113-122.
6. Bratton, D. L., and P. M. Henson. 2008. Apoptotic cell recognition: will the real phosphatidylserine receptor(s) please stand up? Curr. Biol. 18: R76-R79.
7. Chang, M. K., C. Bergmark, A. Laurila, S. Hörkkö, K. H. Han, P. Friedman, E. A. Dennis, and J. L. Witztum. 1999. 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. USA 96: 6353-6358.
8. Shaw, P. X., C. S. Goodyear, M.-K. Chang, J. Witztum, and G. J. Silverman. 2003. The autoreactivity of anti-phosphorylcholine antibodies for atherosclerosis-associated neo-antigens and apoptotic cells. J. Immunol. 170: 6151-6157.
9. 2 activation during apoptosis promotes the exposure of membrane lysophosphatidylcholine leading to binding by natural immunoglobulin M antibodies and complement activation. J. Exp. Med. 196: 655-665.
10. Chang, M. K., C. J. Binder, Y. I. Miller, G. Subbanagounder, G. J. Silverman, J. A. Berliner, and J. L. Witztum. 2004. Apoptotic cells with oxidation-specific epitopes are immunogenic and proinflammatory. J. Exp. Med. 200: 1359-1370.
11. Mevorach, D., J. L. Zhou, X. Song, and K. B. Elkon. 1998. Systemic exposure to irradiated apoptotic cells induces autoantibody production. J. Exp. Med. 188: 387-392. (Pubitemid 28357766)
12. Shvedova, A. A., Y. Y. Tyurina, V. A. Tyurin, Y. Kikuchi, V. E. Kagan, and P. J. Quinn. 2001. Quantitative analysis of phospholipid peroxidation and antioxidant protection in live human epidermal keratinocytes. Biosci. Rep. 21: 33-43.
13. Friedman, P., S. Horkko, D. Steinberg, J. L. Witztum, and E. A. Dennis. 2002. Correlation of antiphospholipid antibody recognition with the structure of synthetic oxidized phospholipids: importance of Schiff base formation and aldol concentration. J. Biol. Chem. 277: 7010-7020. (Pubitemid 34953088)
14. Pryor, W. A., and J. P. Stanley. 1975. Letter: a suggested mechanism for the production of malonaldehyde during the autoxidation of polyunsaturated fatty acids: nonenzymatic production of prostaglandin endoperoxides during autoxidation. J. Org. Chem. 40: 3615-3617.
15. Yang, Y., R. Sharma, A. Sharma, S. Awasthi, and Y. C. Awasthi. 2003. Lipid peroxidation and cell cycle signaling: 4-hydroxynonenal, a key molecule in stress mediated signaling. Acta Biochim. Pol. 50: 319-336. (Pubitemid 37034689)
16. Moore, K., and L. J. Roberts, 2nd. 1998. Measurement of lipid peroxidation. Free Radical Res. 28: 659-671.
17. Mi, Q. S., L. Zhou, D. H. Schulze, R. T. Fischer, A. Lustig, L. J. Rezanka, D. M. Donovan, D. L. Longo, and J. J. Kenny. 2000. Highly reduced protection against Streptococcus pneumoniae after deletion of a single heavy chain gene in mouse. Proc. Natl. Acad. Sci. USA 97: 6031-6036.
18. Shaw, P. X., S. Horkko, M. K. Chang, L. K. Curtiss, W. Palinski, G. J. Silverman, and J. L. Witztum. 2000. Natural antibodies with the T15 idiotype may act in atherosclerosis, apoptotic clearance, and protective immunity. J. Clin. Invest. 105: 1731-1740.
19. +) B cells that recognize phosphatidyl choline. J. Exp. Med. 169: 1869-1877.
20. Silverman, G. J., S. P. Cary, D. C. Dwyer, L. Luo, R. Wagenknecht, and V. E. Curtiss. 2000. A B cell superantigen-induced persistent "Hole" in the B-1 repertoire. J. Exp. Med. 192: 87-98.
21. Silverman, G. J., R. Srikrishnan, K. Germar, C. S. Goodyear, K. A. Andrews, E. M. Ginzler, and B. P. Tsao. 2008. Genetic imprinting of autoantibody repertoires in SLE patients. Clin. Exp. Immunol. 153: 102-116.
22. Nauta, A. J., N. Raaschou-Jensen, A. Roos, M. R. Daha, H. O. Madsen, M. C. Borrias-Essers, L. P. Ryder, C. Koch, and P. Garred. 2003. Mannosebinding lectin engagement with late apoptotic and necrotic cells. Eur. J. Immunol. 33: 2853-2863.
23. Inaba, K., S. Turley, F. Yamaide, T. Iyoda, K. Mahnke, M. Inaba, M. Pack, M. Subklewe, B. Sauter, D. Sheff, et al. 1998. Efficient presentation of phagocytosed cellular fragments on the major histocompatibility complex class II products of dendritic cells. J. Exp. Med. 188: 2163-2173.
24. Hart, S. P., I. Dransfield, and A. G. Rossi. 2008. Phagocytosis of apoptotic cells. Methods 44: 280-285.
25. Lillis, A. P., M. C. Greenlee, I. Mikhailenko, S. V. Pizzo, A. J. Tenner, D. K. Strickland, and S. S. Bohlson,. 2008. Murine low-density lipoprotein receptor-related protein 1 (LRP) is required for phagocytosis of targets bearing LRP ligands but is not required for C1q-triggered enhancement of phagocytosis. J. Immunol. 181: 364-373.
26. Quartier, P., P. K. Potter, M. R. Ehrenstein, M. J. Walport, and M. Botto. 2005. Predominant role of IgM-dependent activation of the classical pathway in the clearance of dying cells by murine bone marrow-derived macrophages in vitro. Eur. J. Immunol. 35: 252-260. (Pubitemid 40123872)
27. Lee, W., H. Cosenza, and H. Kohler. 1974. Clonal restriction of the immune response to phosphorylcholine. Nature 247: 55-57.
28. + B lymphocytes. Int. Immunol. 2: 515-520.
29. Cohn, M., G. Notani, and S. A. Rice. 1969. Characterization of the antibody to the C-carbohydrate produced by a transplantable mouse plasmacytoma. Immunochemistry 6: 111-123.
30. Fung, J., and H. Kohler. 1980. Immune response to phosphorylcholine, VII: Functional evidence for three separate B cell subpopulations responding to TI and TD PC-antigens. J. Immunol. 125: 640-646. (Pubitemid 10045640)
31. Slack, J., G. P. Der-Balian, M. Nahm, and J. M. Davie. 1980. Subclass restriction of murine antibodies, II: The IgG plaque-forming cell response to thymus-independent type 1 and type 2 antigens in normal mice and mice expressing an X-linked immunodeficiency. J. Exp. Med. 151: 853-862. (Pubitemid 10118524)
32. Korb, L. C., and J. M. Ahearn. 1997. C1q binds directly and specifically to surface blebs of apoptotic human keratinocytes: complement deficiency and systemic lupus erythematosus revisited. J. Immunol. 158: 4525-4528.
33. Ogden, C. A., A. deCathelineau, P. R. Hoffmann, D. Bratton, B. Ghebrehiwet, V. A. Fadok, and P. M. Henson. 2001. C1q and mannose binding lectin engagement of cell surface calreticulin and CD91 initiates macropinocytosis and uptake of apoptotic cells. J. Exp. Med. 194: 781-795.
34. Vandivier, R. W., C. A. Ogden, V. A. Fadok, P. R. Hoffmann, K. K. Brown, M. Botto, M. J. Walport, J. H. Fisher, P. M. Henson, and K. E. Greene. 2002. Role of surfactant proteins A, D, and C1q in the clearance of apoptotic cells in vivo and in vitro: calreticulin and CD91 as a common collectin receptor complex. J. Immunol. 169: 3978-3986.
35. Taylor, P. R., A. Carugati, V. A. Fadok, H. T. Cook, M. Andrews, M. C. Carroll, J. S. Savill, P. M. Henson, M. Botto, and M. J. Walport. 2000. A hierarchical role for classical pathway complement proteins in the clearance of apoptotic cells in vivo. J. Exp. Med. 192: 359-366.
36. Kitamura, D., J. Roes, R. Kuhn, and K. Rajewsky. 1991. A B cell-deficient mouse by targeted disruption of the membrane exon of the immunoglobulin mu chain gene. Nature 350: 423-426. (Pubitemid 21912244)
37. Navratil, J. S., S. C. Watkins, J. J. Wisnieski, and J. M. Ahearn. 2001. The globular heads of C1q specifically recognize surface blebs of apoptotic vascular endothelial cells. J. Immunol. 166: 3231-3239.
38. Strobl, H., and W. Knapp. 1999. TGF-β1 regulation of dendritic cells. Microbes Infect. 1: 1283-1290.
39. Bensa, J. C., A. Reboul, and M. G. Colomb. 1983. Biosynthesis in vitro of complement subcomponents C1q, C1s and C1 inhibitor by resting and stimulated human monocytes. Biochem. J. 216: 385-392.
40. Reboul, A., M. H. Prandini, J. C. Bensa, and M. G. Colomb. 1985. Characterization of C1q, C1s and C-1 Inh synthesized by stimulated human monocytes in vitro. FEBS Lett. 190: 65-68. (Pubitemid 16251320)
41. Lutz, H. U. Homeostatic roles of naturally occurring antibodies: an overview. J. Autoimmun. 29: 287-294.
42. Sigal, N. H., P. J. Gearhart, and N. R. Klinman. 1975. The frequency of phosphorylcholine-specific B cells in conventional and germfree BALB/C mice. J. Immunol. 114: 1354-1358.
43. McDaniel, L. S., W. H. J. Benjamin, C. Forman, and D. E. Briles. 1984. Blood clearance by anti-phosphocholine antibodies as a mechanism of protection in experimental pneumococcal bacteremia. J. Immunol. 133: 3308-3312.
44. Gearhart, P. J., N. H. Sigal, and N. R. Klinman. 1977. The monoclonal anti-phosphorylcholine antibody response in several murine strains: genetic implications of a diverse repertoire. J. Exp. Med. 145: 876-891.
45. Crews, S., J. Griffin, H. Huang, K. Calame, and L. Hood. 1981. A single VH gene segment encodes the immune response to phosphorylcholine: somatic mutation is correlated with the class of the antibody. Cell 25: 59-66. (Pubitemid 11087435)
46. H1 heavy chain of anti-phosphocholine antibodies alter binding to and protection against Streptococcus pneumoniae. Int. Immunol. 9: 665-677.
47. Kenny, J. J., C. M. Moratz, G. Guelde, C. D. O'Connell, J. George, C. Dell, S. J. Penner, J. S. Weber, J. Berry, C. L. Claflin, and D. L. Longo. 1992. Antigen binding and idiotype analysis of antibodies obtained after electroporation of heavy and light chain genes encoding phosphocholine-specific antibodies: a model for T15-idiotype dominance. J. Exp. Med. 176: 1637-1643.
48. Chen, C., V. A. Roberts, S. Stevens, M. Brown, M. P. Stenzel-Poore, and M. B. Rittenberg. 1995. Enhancement and destruction of antibody function by somatic mutation: unequal occurrence is controlled by V gene combinatorial associations. EMBO J. 14: 2784-2794.
49. Stenzel-Poore, M. P., U. Bruderer, and M. B. Rittenberg. 1988. The adaptive potential of the memory response: clonal recruitment and epitope recognition. Immunol. Rev. 105: 113-136.
50. H CDR 2: a means of minimizing B cell wastage from somatic hypermutation? J. Immunol. 156: 3285-3291.
51. H complementarity-determining region 2 and framework region 2: differential effects on antigen binding and Ig secretion. J. Immunol. 159: 1293-1302.
52. H11 in the Ly-1 B cell lineage. J. Exp. Med. 172: 371-374.
53. + (CD5) B cells that recognize phosphatidyl choline: relationship to cells that secrete hemolytic antibody specific for autologous erythrocytes. J. Exp. Med. 168: 687-698.
54. Ogden, C. A., R. Kowalewski, Y. Peng, V. Montenegro, and K. B. Elkon. 2005. IGM is required for efficient complement mediated phagocytosis of apoptotic cells in vivo. Autoimmunity 38: 259-264.
55. Behrens, E. M., U. Sriram, D. K. Shivers, M. Gallucci, Z. Ma, T. H. Finkel, and S. Gallucci. 2007. Complement receptor 3 ligation of dendritic cells suppresses their stimulatory capacity. J. Immunol. 178: 6268-6279.
56. 5, is a regulator of human dendritic-cell immunostimulatory function. Blood 108: 947-955.
57. Morelli, A. E., A. T. Larregina, W. J. Shufesky, A. F. Zahorchak, A. J. Logar, G. D. Papworth, Z. Wang, S. C. Watkins, L. D. Falo, Jr., and A. W. Thomson. 2003. Internalization of circulating apoptotic cells by splenic marginal zone dendritic cells: dependence on complement receptors and effect on cytokine production. Blood 101: 611-620.
58. Verbovetski, I., H. Bychkov, U. Trahtemberg, I. Shapira, M. Hareuveni, O. Ben-Tal, I. Kutikov, O. Gill, and D. Mevorach. 2002. Opsonization of apoptotic cells by autologous iC3b facilitates clearance by immature dendritic cells, down-regulates DR and CD86, and up-regulates CC chemokine receptor 7. J. Exp. Med. 196: 1553-1561. (Pubitemid 36026467)
59. Gershov, D., S. Kim, N. Brot, and K. B. Elkon. 2000. C-reactive protein binds to apoptotic cells, protects the cells from assembly of the terminal complement components, and sustains an antiinflammatory innate immune response: implications for systemic autoimmunity. J. Exp. Med. 192: 1353-1364.
60. Mitchell, D. A., P. R. Taylor, H. T. Cook, J. Moss, A. E. Bygrave, M. J. Walport, and M. Botto. 1999. Cutting edge: C1q protects against the development of glomerulonephritis independently of C3 activation. J. Immunol. 162: 5676-5679.
61. Botto, M., C. Dell'Agnola, A. E. Bygrave, E. M. Thompson, H. T. Cook, F. Petry, R. M. Loos, P. P. Pandolfi, and M. J. Walport. 1998. Homozygous C1q deficiency causes glomerulonephritis associated with multiple apoptotic bodies. Nat. Genet. 19: 56-59. (Pubitemid 28242023)
62. Hughey, C. T., J. W. Brewer, A. D. Colosia, W. F. Rosse, and R. B. Corley. 1998. Production of IgM hexamers by normal and autoimmune B cells: implications for the physiologic role of hexameric IgM. J. Immunol. 161: 4091-4097.
63. Behrens, E. M., Y. Ning, N. Muvarak, P. W. Zoltick, A. W. Flake, and S. Gallucci. 2008. Apoptotic cell-mediated immunoregulation of dendritic cells does not require iC3b opsonization. J. Immunol. 181: 3018-3026.
64. Cortes-Hernandez, J., L. Fossati-Jimack, A. Carugati, P. K. Potter, M. J. Walport, H. T. Cook, and M. Botto. 2002. Murine glomerular mesangial cell uptake of apoptotic cells is inefficient and involves serum-mediated but complement-independent mechanisms. Clin. Exp. Immunol. 130: 459-466. (Pubitemid 35418329)
65. Hanayama, R., M. Tanaka, K. Miwa, A. Shinohara, A. Iwamatsu, and S. Nagata. 2002. Identification of a factor that links apoptotic cells to phagocytes. Nature 417: 182-187. (Pubitemid 34506799)
66. Ezekowitz, R. A. 2002. Local opsonization for apoptosis? Nat. Immunol. 3: 510-512.
67. Ezekowitz, R. A., R. B. Sim, G. G. MacPherson, and S. Gordon. 1985. Interaction of human monocytes, macrophages, and polymorphonuclear leukocytes with zymosan in vitro: role of type 3 complement receptors and macrophage-derived complement. J. Clin. Invest. 76: 2368-2376.
68. Padilla, N. D., C. Ciurana, J. van Oers, A. C. Ogilvie, and C. E. Hack. 2004. Levels of natural IgM antibodies against phosphorylcholine in healthy individuals and in patients undergoing isolated limb perfusion. J. Immunol. Methods 293: 1-11.
69. Su, J., X. Hua, H. Concha, E. Svenungsson, A. Cederholm, and J. Frostegard. 2008. Natural antibodies against phosphorylcholine as potential protective factors in SLE. Rheumatology (Oxford) 47: 1144-1150.
70. Bladon, J., and P. C. Taylor. 2006. Extracorporeal photopheresis: a focus on apoptosis and cytokines. J. Dermatol. Sci. 43: 85-94. (Pubitemid 44094006)
71. Binder, C., S. Hörkkö, A. Dewan, M.-K. Chang, E. Kieu, C. Goodyear, P. Shaw, W. Palinski, J. Witztum, and G. J. Silverman. 2003. Pneumococcal vaccination decreases atherosclerotic lesion formation: molecular mimicry between oxidized LDL and Streptococcus pneumoniae. Nat. Med. 9: 736-743. (Pubitemid 36749223)