Autoantibodies against complement C1q specifically target C1q bound on early apoptotic cells

Journal of Immunology

Volumn 183, Issue 5, 2009, Pages 3512-3521

  Bigler, Cornelia ^a   Schaller, Monica ^a   Perahud, Iryna ^a   Osthoff, Michael ^a   Trendelenburg, Marten ^a  

^a UNIVERSITY HOSPITAL BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIBODY; COMPLEMENT COMPONENT C1Q; COMPLEMENT COMPONENT C1Q ANTIBODY; EPITOPE; IMMUNOGLOBULIN G; IMMUNOGLOBULIN F(AB) FRAGMENT; MONOCLONAL ANTIBODY;

ANTIGEN ANTIBODY COMPLEX; ANTIGEN BINDING; ANTIGENICITY; APOPTOSIS; ARTICLE; AUTOIMMUNITY; CELL DEATH; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CELL; HYPOCOMPLEMENTEMIC URTICARIAL VASCULITIS; PRIORITY JOURNAL; PROTEIN TARGETING; SYSTEMIC LUPUS ERYTHEMATOSUS; VASCULITIS; ANIMAL; ANTIBODY COMBINING SITE; BAGG ALBINO MOUSE; BIOSYNTHESIS; IMMUNOLOGY; LEUKEMIA CELL LINE; METABOLISM; MOUSE; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGEN-ANTIBODY COMPLEX; APOPTOSIS; AUTOANTIBODIES; BINDING SITES, ANTIBODY; CELL LINE, TUMOR; COMPLEMENT C1Q; EPITOPES; HUMANS; IMMUNOGLOBULIN FAB FRAGMENTS; JURKAT CELLS; LUPUS ERYTHEMATOSUS, SYSTEMIC; MICE; MICE, INBRED BALB C; VASCULITIS;

EID: 70349238894     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0803573     Document Type: Article

References (53)

1. Mok, C. C., and C. S. Lau. 2003. Pathogenesis of systemic lupus erythematosus. J. Clin. Pathol. 56: 481-490.
2. Lipsky, P. E. 2001. Systemic lupus erythematosus: an autoimmune disease of B cell hyperactivity. Nat. Immunol. 2: 764-766.
3. Barilla-LaBarca, M. L., and J. P. Atkinson. 2003. Rheumatic syndromes associated with complement deficiency. Curr. Opin. Rheumatol. 15: 55-60.
4. Pickering, M. C., S. Fischer, M. R. Lewis, M. J. Walport, M. Botto, and H. T. Cook. 2001. Ultraviolet-radiation-induced keratinocyte apoptosis in C1q-deficient mice. J. Invest. Dermatol. 117: 52-58.
5. Agnello, V. 1978. Association of systemic lupus erythematosus and SLE-like syndromes with hereditary and acquired complement deficiency states. Arthritis Rheum. 21: S146-S152.
6. Jennette, J. C., and C. G. Hipp. 1985. Immunohistopathologic evaluation of C1q in 800 renal biopsy specimens. Am. J. Clin. Pathol. 83: 415-420.
7. Lachmann, P. J., H. J. Muller-Eberhard, H. G. Kunkel, and F. Paronetto. 1962. The localization of in vivo bound complement in tissue section. J. Exp. Med. 115: 63-82.
8. Trendelenburg, M., S. Courvoisier, P. J. Spath, S. Moll, M. Mihatsch, P. Itin, and J. A. Schifferli. 1999. Hypocomplementemic urticarial vasculitis or systemic lupus erythematosus? Am. J. Kidney Dis. 34: 745-751. (Pubitemid 29473064)
9. Trendelenburg, M., M. Lopez-Trascasa, E. Potlukova, S. Moll, S. Regenass, V. Fremeaux-Bacchi, J. Martinez-Ara, E. Jancova, M. L. Picazo, E. Honsova, et al. 2006. High prevalence of anti-C1q antibodies in biopsy-proven active lupus nephritis. Nephrol. Dial. Transplant. 21: 3115-3121.
10. Siegert, C., M. Daha, M. L. Westedt, E. van der Voort, and F. Breedveld. 1991. IgG autoantibodies against C1q are correlated with nephritis, hypocomplementemia, and dsDNA antibodies in systemic lupus erythematosus. J. Rheumatol. 18: 230-234.
11. Botto, M., and M. J. Walport. 2002. C1q, autoimmunity and apoptosis. Immunobiology 205: 395-406.
12. Charles, P. J. 2003. Defective waste disposal: does it induce autoantibodies in SLE? Ann. Rheum. Dis. 62: 1-3.
13. Savill, J. 2000. Apoptosis in resolution of inflammation. Kidney Blood Press Res. 23: 173-174.
14. Grodzicky, T., and K. B. Elkon. 2000. Apoptosis in rheumatic diseases. Am. J. Med. 108: 73-82.
15. Cohen, P. L., R. Caricchio, V. Abraham, T. D. Camenisch, J. C. Jennette, R. A. Roubey, H. S. Earp, G. Matsushima, and E. A. Reap. 2002. Delayed apoptotic cell clearance and lupus-like autoimmunity in mice lacking the c-mer membrane tyrosine kinase. J. Exp. Med. 196: 135-140.
16. Potter, P. K., J. Cortes-Hernandez, P. Quartier, M. Botto, and M. J. Walport. 2003. Lupus-prone mice have an abnormal response to thioglycolate and an impaired clearance of apoptotic cells. J. Immunol. 170: 3223-3232.
17. Herrmann, M., R. E. Voll, O. M. Zoller, M. Hagenhofer, B. B. Ponner, and J. R. Kalden. 1998. Impaired phagocytosis of apoptotic cell material by monocyte- derived macrophages from patients with systemic lupus erythematosus. Arthritis Rheum. 41: 1241-1250.
18. Casciola-Rosen, L. A., G. Anhalt, and A. Rosen. 1994. Autoantigens targeted in systemic lupus erythematosus are clustered in two populations of surface structures on apoptotic keratinocytes. J. Exp. Med. 179: 1317-1330.
19. 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.
20. Gaipl, U. S., S. Kuenkele, R. E. Voll, T. D. Beyer, W. Kolowos, P. Heyder, J. R. Kalden, and M. Herrmann. 2001. Complement binding is an early feature of necrotic and a rather late event during apoptotic cell death. Cell Death Differ. 8: 327-334.
21. 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.
22. 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.
23. 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.
24. 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.
25. Mevorach, D., J. O. Mascarenhas, D. Gershov, and K. B. Elkon. 1998. Complement-dependent clearance of apoptotic cells by human macrophages. J. Exp. Med. 188: 2313-2320.
26. Fremeaux-Bacchi, V., L. Weiss, C. Demouchy, J. Blouin, and M. D. Kazatchkine. 1996. Autoantibodies to the collagen-like region of C1q are strongly associated with classical pathway-mediated hypocomplementemia in systemic lupus erythematosus. Lupus 5: 216-220.
27. Walport, M. J. 2002. Complement and systemic lupus erythematosus. Arthritis Res. 4(Suppl. 3): S279-S293.
28. Trendelenburg, M., J. Marfurt, I. Gerber, A. Tyndall, and J. A. Schifferli. 1999. Lack of occurrence of severe lupus nephritis among anti-C1q autoantibody-negative patients. Arthritis Rheum. 42: 187-188. (Pubitemid 29042588)
29. Agnello, V., D. Koffler, J. W. Eisenberg, R. J. Winchester, and H. G. Kundel. 1971. C1g precipitins in the sera of patients with systemic lupus erythematosus and other hypocomplementemic states: characterization of high and low molecular weight types. J. Exp. Med. 134: 228s-241s.
30. Antes, U., H. P. Heinz, and M. Loos. 1988. Evidence for the presence of autoantibodies to the collagen-like portion of C1q in systemic lupus erythematosus. Arthritis Rheum. 31: 457-464.
31. Uwatoko, S., and M. Mannik. 1988. Low-molecular weight C1q-binding immunoglobulin G in patients with systemic lupus erythematosus consists of autoantibodies to the collagen-like region of C1q. J. Clin. Invest. 82: 816-824.
32. Wisnieski, J. J., and S. M. Jones. 1992. IgG autoantibody to the collagen-like region of Clq in hypocomplementemic urticarial vasculitis syndrome, systemic lupus erythematosus, and 6 other musculoskeletal or rheumatic diseases. J. Rheumatol. 19: 884-888.
33. Wisnieski, J. J., and S. M. Jones. 1992. Comparison of autoantibodies to the collagen-like region of C1q in hypocomplementemic urticarial vasculitis syndrome and systemic lupus erythematosus. J. Immunol. 148: 1396-1403.
34. Prada, A. E., and C. F. Strife. 1992. IgG subclass restriction of autoantibody to solid-phase C1q in membranoproliferative and lupus glomerulonephritis. Clin. Immunol. Immunopathol. 63: 84-88.
35. Siegert, C. E., M. R. Daha, E. A. van der Voort, and F. C. Breedveld. 1990. IgG and IgA antibodies to the collagen-like region of C1q in rheumatoid vasculitis. Arthritis Rheum. 33: 1646-1654.
36. Martensson, U., S. Thiel, J. C. Jensenius, and A. G. Sjoholm. 1996. Human autoantibodies against Clq: lack of cross reactivity with the collectins mannanbinding protein, lung surfactant protein A and bovine conglutinin. Scand. J. Immunol. 43: 314-320. (Pubitemid 26097603)
37. Sjoholm, A. G., U. Martensson, and G. Sturfelt. 1997. Serial analysis of autoantibody responses to the collagen-like region of Clq, collagen type II, and double stranded DNA in patients with systemic lupus erythematosus. J. Rheumatol. 24: 871-878.
38. Hochberg, M. C. 1997. Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 40: 1725.
39. Tan, E. M., A. S. Cohen, J. F. Fries, A. T. Masi, D. J. McShane, N. F. Rothfield, J. G. Schaller, N. Talal, and R. J. Winchester. 1982. The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 25: 1271-1277.
40. Kohler, G., and C. Milstein. 1976. Derivation of specific antibody-producing tissue culture and tumor lines by cell fusion. Eur. J. Immunol. 6: 511-519.
41. Kohro-Kawata, J., M. H. Wener, and M. Mannik. 2002. The effect of high salt concentration on detection of serum immune complexes and autoantibodies to C1q in patients with systemic lupus erythematosus. J. Rheumatol. 29: 84-89.
42. Trendelenburg, M. 2005. Antibodies against C1q in patients with systemic lupus erythematosus. Springer Semin. Immunopathol. 28: 1-10.
43. Paidassi, H., P. Tacnet-Delorme, V. Garlatti, C. Darnault, B. Ghebrehiwet, C. Gaboriaud, G. J. Arlaud, and P. Frachet. 2008. C1q binds phosphatidylserine and likely acts as a multiligand-bridging molecule in apoptotic cell recognition. J. Immunol. 180: 2329-2338.
44. Flierman, R., and M. R. Daha. 2007. Pathogenic role of anti-C1q autoantibodies in the development of lupus nephritis: a hypothesis. Mol. Immunol. 44: 133-138.
45. Golan, M. D., R. Burger, and M. Loos. 1982. Conformational changes in C1q after binding to immune complexes: detection of neoantigens with monoclonal antibodies. J. Immunol. 129: 445-447.
46. Amoura, Z., H. Chabre, S. Koutouzov, C. Lotton, A. Cabrespines, J. F. Bach, and L. Jacob. 1994. Nucleosome-restricted antibodies are detected before anti-dsDNA and/or antihistone antibodies in serum of MRL-Mp lpr/lpr and +/+ mice, and are present in kidney eluates of lupus mice with proteinuria. Arthritis Rheum. 37: 1684-1688.
47. Laderach, D., S. Koutouzov, J. F. Bach, and A. M. Yamamoto. 2003. Concomitant early appearance of anti-ribonucleoprotein and anti-nucleosome antibodies in lupus prone mice. J. Autoimmun. 20: 161-170.
48. Reed, J. H., M. W. Jackson, and T. P. Gordon. 2008. A B cell apotope of Ro 60 in systemic lupus erythematosus. Arthritis Rheum. 58: 1125-1129.
49. Gaboriaud, C., J. Juanhuix, A. Gruez, M. Lacroix, C. Darnault, D. Pignol, D. Verger, J. C. Fontecilla-Camps, and G. J. Arlaud. 2003. The crystal structure of the globular head of complement protein C1q provides a basis for its versatile recognition properties. J. Biol. Chem. 278: 46974-46982.
50. Roumenina, L. T., M. M. Ruseva, A. Zlatarova, R. Ghai, M. Kolev, N. Olova, M. Gadjeva, A. Agrawal, B. Bottazzi, A. Mantovani, et al. 2006. Interaction of C1q with IgG1, C-reactive protein and pentraxin 3: mutational studies using recombinant globular head modules of human C1q A, B, and C chains. Biochemistry 45: 4093-4104.
51. Castellano, G., A. M. Woltman, A. J. Nauta, A. Roos, L. A. Trouw, M. A. Seelen, F. P. Schena, M. R. Daha, and C. van Kooten. 2004. Maturation of dendritic cells abrogates C1q production in vivo and in vitro. Blood 103: 3813-3820.
52. Castellano, G., A. M. Woltman, N. Schlagwein, W. Xu, F. P. Schena, M. R. Daha, and C. van Kooten. 2007. Immune modulation of human dendritic cells by complement. Eur. J. Immunol. 37: 2803-2811.
53. Botto, M., C. Dell'Agnola, A. E. Bygrave, E. M. Thompson, H. T. Cook, F. Petry, 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.