Requirement for complement in antibody responses is not explained by the classic pathway activator IgM

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 43, 2011, Pages

  Rutemark, Christian ^a   Alicot, Elisabeth ^b,c   Bergman, Anna ^a   Minghe, Ma ^b,c   Getahun, Andrew ^d   Ellmerich, Stephan ^e   Carroll, Michael C ^b,c   Heyman, Birgitta ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

IgM mutation; Natural IgM

Indexed keywords

COMPLEMENT; COMPLEMENT COMPONENT C1Q; COMPLEMENT COMPONENT C2; COMPLEMENT COMPONENT C3; IMMUNOGLOBULIN M; KEYHOLE LIMPET HEMOCYANIN; PROLINE; SERINE;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY RESPONSE; ARTICLE; CONTROLLED STUDY; ERYTHROCYTE; GENE TARGETING; MOUSE; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; SHEEP; WILD TYPE;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODY FORMATION; C-REACTIVE PROTEIN; CHROMATOGRAPHY, AGAROSE; COMPLEMENT PATHWAY, CLASSICAL; COMPLEMENT SYSTEM PROTEINS; DNA PRIMERS; ENZYME-LINKED IMMUNOSORBENT ASSAY; ENZYME-LINKED IMMUNOSPOT ASSAY; FLOW CYTOMETRY; GENE KNOCK-IN TECHNIQUES; IMMUNOGLOBULIN MU-CHAINS; MICE; MICE, INBRED BALB C; MICROSCOPY, CONFOCAL; MUTATION, MISSENSE; POLYMERASE CHAIN REACTION; SERUM AMYLOID P-COMPONENT;

ANIMALIA; MUS; OVIS ARIES;

EID: 80055071471     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1109831108     Document Type: Article

References (65)

1. Pepys MB (1976) Role of complement in the induction of immunological responses. Transplant Rev 32:93-120.
2. Carroll MC (2004) The complement system in regulation of adaptive immunity. Nat Immunol 5:981-986.
3. Heyman B (2000) Regulation of antibody responses via antibodies, complement, and Fc receptors. Annu Rev Immunol 18:709-737.
4. Pepys MB (1974) Role of complement in induction of antibody production in vivo. Effect of cobra factor and other C3-reactive agents on thymus-dependent and thymus-independent antibody responses. J Exp Med 140:126-145.
5. Jackson CG, Ochs HD, Wedgwood RJ (1979) Immune response of a patient with deficiency of the fourth component of complement and systemic lupus erythematosus. N Engl J Med 300:1124-1129. (Pubitemid 9175612)
6. Ochs HD, Wedgwood RJ, Frank MM, Heller SR, Hosea SW (1983) The role of complement in the induction of antibody responses. Clin Exp Immunol 53:208-216. (Pubitemid 13106768)
7. Böttger EC, Hoffmann T, Hadding U, Bitter-Suermann D (1985) Influence of genetically inherited complement deficiencies on humoral immune response in guinea pigs. J Immunol 135:4100-4107. (Pubitemid 16250398)
8. Fischer MB, et al. (1996) Regulation of the B cell response to T-dependent antigens by classical pathway complement. J Immunol 157:549-556. (Pubitemid 26231355)
9. O'Neil KM, et al. (1988) Role of C3 in humoral immunity. Defective antibody production in C3-deficient dogs. J Immunol 140:1939-1945.
10. Heyman B, Wiersma EJ, Kinoshita T (1990) In vivo inhibition of the antibody response by a complement receptor-specific monoclonal antibody. J Exp Med 172:665-668. (Pubitemid 20248411)
11. Martinelli GP, Matsuda T, Waks HS, Osler AG (1978) Studies on immunosuppression by cobra venom factor. III. On early responses to sheep erythrocytes in C5-deficient mice. J Immunol 121:2052-2055. (Pubitemid 9053611)
12. Ahearn JM, et al. (1996) Disruption of the Cr2 locus results in a reduction in B-1a cells and in an impaired B cell response to T-dependent antigen. Immunity 4:251-262. (Pubitemid 26131008)
13. Molina H, et al. (1996) Markedly impaired humoral immune response in mice deficient in complement receptors 1 and 2. Proc Natl Acad Sci USA 93:3357-3361. (Pubitemid 26125624)
14. Fang Y, Xu C, Fu Y-X, Holers VM, Molina H (1998) Expression of complement receptors 1 and 2 on follicular dendritic cells is necessary for the generation of a strong antigen-specific IgG response. J Immunol 160:5273-5279. (Pubitemid 28267813)
15. Roozendaal R, Carroll MC (2007) Complement receptors CD21 and CD35 in humoral immunity. Immunol Rev 219:157-166. (Pubitemid 47390008)
16. Papamichail M, et al. (1975) Complement dependence of localisation of aggregated IgG in germinal centres. Scand J Immunol 4:343-347.
17. Ferguson AR, Youd ME, Corley RB (2004) Marginal zone B cells transport and deposit IgM-containing immune complexes onto follicular dendritic cells. Int Immunol 16:1411-1422. (Pubitemid 39341554)
18. Cinamon G, Zachariah MA, Lam OM, Foss FW, Jr., Cyster JG (2008) Follicular shuttling of marginal zone B cells facilitates antigen transport. Nat Immunol 9:54-62. (Pubitemid 350286204)
19. Thornton BP, Větvicka V, Ross GD (1994) Natural antibody and complement-mediated antigen processing and presentation by B lymphocytes. J Immunol 152:1727-1737. (Pubitemid 24075703)
20. Carter RH, Spycher MO, Ng YC, Hoffman R, Fearon DT (1988) Synergistic interaction between complement receptor type 2 and membrane IgMon B lymphocytes. J Immunol 141:457-463.
21. Ohishi K, Kanoh M, Shinomiya H, Hitsumoto Y, Utsumi S (1995) Complement activation by cross-linked B cell-membrane IgM. J Immunol 154:3173-3179.
22. Rossbacher J, Shlomchik MJ (2003) The B cell receptor itself can activate complement to provide the complement receptor 1/2 ligand required to enhance B cell immune responses in vivo. J Exp Med 198:591-602. (Pubitemid 37040393)
23. Matsumoto M, et al. (1997) Abrogation of the alternative complement pathway by targeted deletion of murine factor B. Proc Natl Acad Sci USA 94:8720-8725. (Pubitemid 27335106)
24. Mehlhop E, Diamond MS (2006) Protective immune responses against West Nile virus are primed by distinct complement activation pathways. J Exp Med 203:1371-1381. (Pubitemid 43736604)
25. Carter T, et al. (2007) Mannose-binding lectin A-deficient mice have abrogated antigen-specific IgM responses and increased susceptibility to a nematode infection. J Immunol 178:5116-5123. (Pubitemid 46595295)
26. Ruseva M, et al. (2009) Mannan-binding lectin deficiency modulates the humoral immune response dependent on the genetic environment. Immunology 127:279-288.
27. Guttormsen HK, et al. (2009) Deficiency of mannose-binding lectin greatly increases antibody response in a mouse model of vaccination. Clin Immunol 130:264-271.
28. Lawrence RA, et al. (2009) Altered antibody responses in mannose-binding lectin-A deficient mice do not affect Trichuris muris or Schistosoma mansoni infections. Parasite Immunol 31:104-109.
29. Cutler AJ, et al. (1998) T cell-dependent immune response in C1q-deficient mice: Defective interferon gamma production by antigen-specific T cells. J Exp Med 187:1789-1797.
30. Taylor PR, Seixas E, Walport MJ, Langhorne J, Botto M (2001) Complement contributes to protective immunity against reinfection by Plasmodium chabaudi chabaudi parasites. Infect Immun 69:3853-3859. (Pubitemid 32493305)
31. Clarke CA, et al. (1963) Further experimental studies on the prevention of Rh haemolytic disease. BMJ 1:979-984.
32. Henry C, Jerne NK (1968) Competition of 19S and 7S antigen receptors in the regulation of the primary immune response. J Exp Med 128:133-152.
33. Heyman B, Andrighetto G, Wigzell H (1982) Antigen-dependent IgM-mediated enhancement of the sheep erythrocyte response in mice. Evidence for induction of B cells with specificities other than that of the injected antibodies. J Exp Med 155:994-1009. (Pubitemid 12142717)
34. Heyman B, Pilström L, Shulman MJ (1988) Complement activation is required for IgM-mediated enhancement of the antibody response. J Exp Med 167:1999-2004.
35. Youd ME, Ferguson AR, Corley RB (2002) Synergistic roles of IgM and complement in antigen trapping and follicular localization. Eur J Immunol 32:2328-2337. (Pubitemid 34965896)
36. Ehrenstein MR, O'Keefe TL, Davies SL, Neuberger MS (1998) Targeted gene disruption reveals a role for natural secretory IgM in the maturation of the primary immune response. Proc Natl Acad Sci USA 95:10089-10093. (Pubitemid 28415299)
37. Boes M, et al. (1998) Enhanced B-1 cell development, but impaired IgG antibody responses in mice deficient in secreted IgM. J Immunol 160:4776-4787. (Pubitemid 28215311)
38. Baumgarth N, et al. (2000) B-1 and B-2 cell-derived immunoglobulin M antibodies are nonredundant components of the protective response to influenza virus infection. J Exp Med 192:271-280. (Pubitemid 30470309)
39. Kang YS, et al. (2006) A dominant complement fixation pathway for pneumococcal polysaccharides initiated by SIGN-R1 interacting with C1q. Cell 125:47-58.
40. Hicks PS, Saunero-Nava L, Du Clos TW, Mold C (1992) Serum amyloid P component binds to histones and activates the classical complement pathway. J Immunol 149:3689-3694.
41. Suresh MV, Singh SK, Ferguson DA, Jr., Agrawal A (2006) Role of the property of C-reactive protein to activate the classical pathway of complement in protecting mice from pneumococcal infection. J Immunol 176:4369-4374. (Pubitemid 44264417)
42. Shulman MJ, Collins C, Pennell N, Hozumi N (1987) Complement activation by IgM: Evidence for the importance of the third constant domain of the mu heavy chain. Eur J Immunol 17:549-554. (Pubitemid 17094155)
43. Wright JF, Shulman MJ, Isenman DE, Painter RH (1988) C1 binding by murine IgM. The effect of a Pro-to-Ser exchange at residue 436 of the mu-chain. J Biol Chem 263:11221-11226.
44. Köntgen F, Süss G, Stewart C, Steinmetz M, Bluethmann H (1993) Targeted disruption of the MHC class II Aa gene in C57BL/6 mice. Int Immunol 5:957-964. (Pubitemid 23241767)
45. Shulman MJ, Heusser C, Filkin C, Köhler G (1982) Mutations affecting the structure and function of immunoglobulin M. Mol Cell Biol 2:1033-1043. (Pubitemid 13227226)
46. Kang YS, et al. (2004) The C-type lectin SIGN-R1 mediates uptake of the capsular polysaccharide of Streptococcus pneumoniae in the marginal zone of mouse spleen. Proc Natl Acad Sci USA 101:215-220.
47. Piskurich JF, Blanchard MH, Youngman KR, France JA, Kaetzel CS (1995) Molecular cloning of the mouse polymeric Ig receptor. Functional regions of the molecule are conserved among five mammalian species. J Immunol 154:1735-1747.
48. Shibuya A, et al. (2000) Fc alpha/mu receptor mediates endocytosis of IgM-coated microbes. Nat Immunol 1:441-446.
49. Shima H, et al. (2010) Identification of TOSO/FAIM3 as an Fc receptor for IgM. Int Immunol 22:149-156.
50. Baker N, Ehrenstein MR (2002) Cutting edge: Selection of B lymphocyte subsets is regulated by natural IgM. J Immunol 169:6686-6690. (Pubitemid 36899252)
51. Karlsson MCI, Wernersson S, Diaz de Ståhl T, Gustavsson S, Heyman B (1999) Efficient IgG-mediated suppression of primary antibody responses in Fcgamma receptor-deficient mice. Proc Natl Acad Sci USA 96:2244-2249. (Pubitemid 29117899)
52. Brüggemann M, Rajewsky K (1982) Regulation of the antibody response against hapten-coupled erythrocytes by monoclonal antihapten antibodies of various isotypes. Cell Immunol 71:365-373. (Pubitemid 12036920)
53. Heyman B, Wigzell H (1984) Immunoregulation by monoclonal sheep erythrocyte-specific IgG antibodies: Suppression is correlated to level of antigen binding and not to isotype. J Immunol 132:1136-1143. (Pubitemid 14155348)
54. Hughes-Jones NC, Gorick BD, Howard JC (1983) The mechanism of synergistic complement-mediated lysis of rat red cells by monoclonal IgG antibodies. Eur J Immunol 13:635-641. (Pubitemid 13047051)
55. Manderson AP, Pickering MC, Botto M, Walport MJ, Parish CR (2001) Continual low-level activation of the classical complement pathway. J Exp Med 194:747-756. (Pubitemid 32983011)
56. Applequist SE, Dahlström J, Jiang N, Molina H, Heyman B (2000) Antibody production in mice deficient for complement receptors 1 and 2 can be induced by IgG/Ag and IgE/Ag, but not IgM/Ag complexes. J Immunol 165:2398-2403. (Pubitemid 30660682)
57. Botto M, et al. (1998) Homozygous C1q deficiency causes glomerulonephritis associated with multiple apoptotic bodies. Nat Genet 19:56-59. (Pubitemid 28242023)
58. Botto M, et al. (1997) Amyloid deposition is delayed in mice with targeted deletion of the serum amyloid P component gene. Nat Med 3:855-859. (Pubitemid 27353444)
59. Loeffler JM, et al. (2009) C-reactive protein is essential for host resistance to pneumococci. Abstr Q J Med 102:644 (abstr).
60. García-González M, et al. (1988) Purification of murine IgG3 and IgM monoclonal antibodies by euglobulin precipitation. J Immunol Methods 111:17-23.
61. Hamad OA, et al. (2008) Complement activation triggered by chondroitin sulfate released by thrombin receptor-activated platelets. J Thromb Haemost 6:1413-1421. (Pubitemid 352016323)
62. Mollnes TE, et al. (2002) Essential role of the C5a receptor in E coli-induced oxidative burst and phagocytosis revealed by a novel lepirudin-based human whole blood model of inflammation. Blood 100:1869-1877. (Pubitemid 34925168)
63. Getahun A, Heyman B (2009) Studies on the mechanism by which antigen-specific IgG suppresses primary antibody responses: Evidence for epitope masking and decreased localization of antigen in the spleen. Scand J Immunol 70:277-287.
64. Jerne NK, Nordin AA (1963) Plaque formation in agar by single antibody-producing cells. Science 140:405.
65. Carlsson F, Getahun A, Rutemark C, Heyman B (2009) Impaired antibody responses but normal proliferation of specific CD4+ T cells in mice lacking complement receptors 1 and 2. Scand J Immunol 70:77-84.