Regulation of antibody responses via antibodies, complement, and Fc receptors.

Antibodies can completely suppress or enhance the antibody response to their specific antigen by several hundredfold. Immunoglobulin M (IgM) enhances antibody responses via the complement system, and complement activation by IgM probably starts the chain of events leading to antibody responses to suboptimal antigen doses. IgG can enhance primary antibody responses in the absence of the complement system and seems to be dependent on Fc receptors for IgG (FcgammaRs). IgE enhances antibody responses via the low-affinity receptor for IgE (FcepsilonRII/CD23). The precise effector mechanisms that cause enhancement are not known, but direct B-cell signaling, antigen presentation, and increased follicular localization are all possibilities. IgG, IgE, and IgM may also suppress antibody responses when used in certain immunization regimes, and it seems reasonable that an important mechanism behind suppression is the masking of antigenic epitopes by antibodies. In addition, FcgammaRIIB, which contains a cytoplasmic inhibitory motif, acts as a negative regulator of antibody responses. This receptor, however, may prevent the antibody responses from exceeding a certain level rather than causing complete suppression.

[1]  J. G. Walker,et al.  STUDIES ON THE CONTROL OF ANTIBODY SYNTHESIS : INTERACTION OF ANTIGENIC COMPETITION AND SUPPRESSION OF ANTIBODY FORMATION BY PASSIVE ANTIBODY ON THE IMMUNE RESPONSE , 1967 .

[2]  G. Möller,et al.  Regulation of the antibody response to sheep erythrocytes by monoclonal IgG antibodies , 1987, European journal of immunology.

[3]  D. Fearon,et al.  Synergistic interaction between complement receptor type 2 and membrane IgM on B lymphocytes. , 1988, Journal of immunology.

[4]  F. Finkelman,et al.  Antigen presentation is enhanced by targeting antigen to the Fc epsilon RII by antigen-anti-Fc epsilon RII conjugates. , 1994, Journal of immunology.

[5]  P. Murdock,et al.  IgE secretion is attenuated by an inhibitor of proteolytic processing of CD23 (FcεRII) , 1997 .

[6]  M. Kehry,et al.  Low-affinity IgE receptor (CD23) function on mouse B cells: role in IgE-dependent antigen focusing. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[7]  A. G. Osler,et al.  Studies of immunosuppression by cobra venom factor. I. On early IgG and IgM responses to sheep erythrocytes and DNP-protein conjugates. , 1978, Journal of immunology.

[8]  K. Rajewsky,et al.  Regulation of the antibody response against hapten-coupled erythrocytes by monoclonal antihapten antibodies of various isotypes. , 1982, Cellular immunology.

[9]  N. K. Jerne,et al.  Plaque Formation in Agar by Single Antibody-Producing Cells , 1963, Science.

[10]  M. Ono,et al.  Augmented humoral and anaphylactic responses in FcγRII-deficient mice , 1996, Nature.

[11]  B. J. Sutton,et al.  The human IgE network , 1993, Nature.

[12]  H. Taylor,et al.  Crystal Structure of Ettringite , 1968, Nature.

[13]  D. Bitter‐Suermann,et al.  Influence of genetically inherited complement deficiencies on humoral immune response in guinea pigs. , 1985, Journal of immunology.

[14]  R. Mcconnell,et al.  Further Experimental Studies on the Prevention of Rh Haemolytic Disease , 1963, British medical journal.

[15]  G. Klaus.  Generation of memory cells. III. Antibody class requirements for the generation of B-memory cells by antigen--antibody complexes. , 1979, Immunology.

[16]  S. Fournier,et al.  The Low‐Affinity Receptor for IgE , 1992, Immunological reviews.

[17]  M. Carroll,et al.  Evidence for an important interaction between a complement-derived CD21 ligand on follicular dendritic cells and CD21 on B cells in the initiation of IgG responses. , 1998, Journal of immunology.

[18]  B. Heyman,et al.  Specific IgM Enhances and IgG Inhibits the Induction of Immunological Memory in Mice , 1985, Scandinavian journal of immunology.

[19]  A. Cooke,et al.  Specific monoclonal IgM is a potent adjuvant in murine malaria vaccination , 1983, Nature.

[20]  P. Ricciardi-Castagnoli,et al.  Fcγ Receptor–mediated Induction of Dendritic Cell Maturation and Major Histocompatibility Complex Class I–restricted Antigen Presentation after Immune Complex Internalization , 1999, The Journal of experimental medicine.

[21]  H. Eibel,et al.  Transgene CD23 expression on lymphoid cells modulates IgE and IgG1 responses. , 1994, Journal of immunology.

[22]  R. Holmdahl,et al.  No role of interleukin‐4 in CD23/IgE‐mediated enhancement of the murine antibody response in vivo , 1995, European journal of immunology.

[23]  J. Cerottini,et al.  The immunosuppressive effect of passively administered antibody IgG fragments. , 1969, Journal of immunology.

[24]  E. Kremmer,et al.  Regulation of the B cell response to T-dependent antigens by classical pathway complement. , 1996, Journal of immunology.

[25]  A. Cooke,et al.  Antibody mediated regulation of immune responses. I. Enhancement of specific antibody responses through IgM antibodies. , 1982, Immunology letters.

[26]  E. Rieber,et al.  IgE‐dependent antigen focusing by human B lymphocytes is mediated by the low‐affinity receptor for IgE , 1990, European journal of immunology.

[27]  P. Hogarth,et al.  Cutting Edge: Identification of the Mouse IgG3 Receptor: Implications for Antibody Effector Function at the Interface Between Innate and Adaptive Immunity , 1998, The Journal of Immunology.

[28]  F. Celada,et al.  Effect of antigen/antibody ratio on macrophage uptake, processing, and presentation to T cells of antigen complexed with polyclonal antibodies , 1991, The Journal of experimental medicine.

[29]  W. Fridman,et al.  Regulation of high-affinity IgE receptor-mediated mast cell activation by murine low-affinity IgG receptors. , 1995, The Journal of clinical investigation.

[30]  H. Colten,et al.  Abrogation of the alternative complement pathway by targeted deletion of murine factor B. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[31]  F. Karush,et al.  Interaction of a bivalent ligand with IgM anti-lactose antibody. , 1979, Biochemistry.

[32]  C. Anderson,et al.  The protection receptor for IgG catabolism is the beta2-microglobulin-containing neonatal intestinal transport receptor. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[33]  F. Finkelman,et al.  Co‐crosslinking FcϵRII/CD23 and B cell surface immunoglobulin modulates B cell activation , 1992 .

[34]  B. Heyman.  Antibody feedback suppression: towards a unifying concept? , 1999, Immunology letters.

[35]  T. Hamaoka,et al.  Antibody production in mice. II. The mechanism of antigenic stimulation in the secondary immune response. , 1971, Immunology.

[36]  C. Bruijnzeel-Koomen,et al.  Consequences of IgE/CD23-mediated antigen presentation in allergy. , 1995, Immunology today.

[37]  J. Uhr,et al.  REGULATION OF ANTIBODY FORMATION BY SERUM ANTIBODY : II. REMOVAL OF SPECIFIC ANTIBODY BY MEANS OF EXCHANGE TRANSFUSION , 1970 .

[38]  J. G. Walker,et al.  STUDIES ON THE CONTROL OF ANTIBODY SYNTHESIS II. EFFECT OF ANTIGEN DOSE AND OF SUPPRESSION BY PASSIVE ANTIBODY ON THE AFFINITY OF ANTIBODY SYNTHESIZED , 1968 .

[39]  B. Heyman,et al.  CD23/IgE-mediated regulation of the specific antibody response in vivo. , 1994, Journal of immunology.

[40]  B. Heyman.  Complement and Fc-receptors in regulation of the antibody response. , 1996, Immunology letters.

[41]  B. Heyman,et al.  Efficient IgG-mediated suppression of primary antibody responses in Fcgamma receptor-deficient mice. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[42]  S. Pierce,et al.  Regulation of B cell receptor-mediated MHC class II antigen processing by FcgammaRIIB1. , 1999, Journal of immunology.

[43]  J. Ravetch,et al.  FcR γ chain deletion results in pleiotrophic effector cell defects , 1994, Cell.

[44]  B. Heyman,et al.  Impaired antibody responses in H-2Ab mice. , 1998, Journal of immunology.

[45]  J. Schrader.  Regulation of the immune response by IgM antibody: a paradoxical suppression of the in vitro primary immune response to sheep erythrocytes by passive IgM. , 1973, The Australian journal of experimental biology and medical science.

[46]  P. Coulie,et al.  Enhancement of IgG anti‐carrier responses by IgG2 anti‐hapten antibodies in mice , 1985, European journal of immunology.

[47]  G. Köhler,et al.  Negative feedback regulation of IgE synthesis by murine CD23 , 1994, Nature.

[48]  R Bheekha Escura,et al.  Regulation and targeting of T-cell immune responses by IgE and IgG antibodies. , 1995, Immunology.

[49]  Walker Jg,et al.  Studies on the control of antibody synthesis. Effect of antibody affinity upon its ability to suppress antibody formation. , 1968 .

[50]  G. Dennert.  Effects of IgM on the in Vivo and in Vitro Immune Response , 1973, Proceedings of the Society for Experimental Biology and Medicine. Society for Experimental Biology and Medicine.

[51]  D. Conrad,et al.  Humoral response suppression observed with CD23 transgenics. , 1999, Journal of immunology.

[52]  B. Heyman,et al.  Inhibition of immunological memory and T‐independent humoral responses by monoclonal antibodies specific for murine complement receptors , 1991, European journal of immunology.

[53]  J. Kinet,et al.  Identification of the low affinity receptor for immunoglobulin E on mouse mast cells and macrophages as Fc gamma RII and Fc gamma RIII , 1992, The Journal of experimental medicine.

[54]  N. Sinclair,et al.  Regulation of the immune response. VI. Inability of F(ab') 2 antibody to terminate established immune responses and its ability to interfere with IgG antibody-mediated immunosuppression. , 1973, Immunology.

[55]  J. Bonnefoy,et al.  Structure and functions of CD23. , 1997, International reviews of immunology.

[56]  D. Dresser.  Feedback by early and late primary antisera on the primary and secondary adoptive immune responses of mice to burro erythrocytes. , 1990, Cellular immunology.

[57]  J. Cerny,et al.  Immunization with immune complex alters the repertoire of antigen‐reactive B cells in the germinal centers , 1997, European journal of immunology.

[58]  B. Heyman,et al.  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 , 1982, The Journal of experimental medicine.

[59]  D. Conrad,et al.  Chromosomal location and isoform analysis of mouse Fcϵ RII/CD23 , 1993 .

[60]  G. Terres,et al.  Enhanced immunological sensitization of mice by the simultaneous injection of antigen and specific antiserum. I. Effect of varying the amount of antigen used relative to the antiserum. , 1961, Journal of immunology.

[61]  W. Fridman,et al.  FcγRII expression in resting and activated B lymphocytes , 1989 .

[62]  A. Cooke,et al.  II. IgM-mediated enhancement: dependency on antigen dose, T-cell requirement and lack of evidence for an idiotype-related mechanism. , 1983, Immunology.

[63]  M. Turner,et al.  Mannose-binding lectin: the pluripotent molecule of the innate immune system. , 1996, Immunology today.

[64]  D. Conrad,et al.  Homotypic aggregation of murine B lymphocytes is independent of CD23 , 1995, European journal of immunology.

[65]  Göran Möller,et al.  ANTIBODY SYNTHESIS AT THE CELLULAR LEVEL. ANTIBODY-INDUCED SUPPRESSION OF 19S AND 7S ANTIBODY RESPONSE. , 1965 .

[66]  B. Heyman,et al.  In vivo enhancement of the specific antibody response via the low‐affinity receptor for IgE , 1993, European journal of immunology.

[67]  H. Kikutani,et al.  The absence of IgE antibody-mediated augmentation of immune responses in CD23-deficient mice. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[68]  G. Möller.  Antibody‐mediated suppression of the immune response is determinant specific , 1985, European journal of immunology.

[69]  A. Helenius,et al.  Transport of macrophage Fc receptors and Fc receptor-bound ligands to lysosomes , 1986, The Journal of experimental medicine.

[70]  B. Heyman,et al.  Early Expansion of Secondary B Cells after Primary Immunization with Antigen Complexed with IgE , 1997, Scandinavian journal of immunology.

[71]  G. Kelsoe,et al.  Antibody response to a T-dependent antigen requires B cell expression of complement receptors , 1996, The Journal of experimental medicine.

[72]  B. Heyman.  Inhibition of IgG‐Mediated Immunosuppression by a Monoclonal Anti‐Fc Receptor Antibody , 1989, Scandinavian journal of immunology.

[73]  T. Yoshino,et al.  Modulation of Immunoglobulin (Ig)E-mediated Systemic Anaphylaxis by Low-Affinity Fc Receptors for IgG , 1999, The Journal of experimental medicine.

[74]  T. Yoshino,et al.  Deletion of Fcγ Receptor IIB Renders H-2b Mice Susceptible to Collagen-induced Arthritis , 1999, The Journal of experimental medicine.

[75]  J. Bowman,et al.  The prevention of Rh immunization. , 1988, Transfusion medicine reviews.

[76]  G. Klaus,et al.  Follicular trapping of hapten-erythrocyte-antibody complexes in mouse spleen. , 1984, Immunology.

[77]  F. Finkelman,et al.  Modulation of mouse complement receptors 1 and 2 suppresses antibody responses in vivo. , 1991, Journal of immunology.

[78]  B. Heyman,et al.  Carbohydrate chains on IgG2b: a requirement for efficient feedback immunosuppression. , 1985, Journal of immunology.

[79]  M. Nussenzweig,et al.  A 13-amino-acid motif in the cytoplasmic domain of FcγRIIB modulates B-cell receptor signalling , 1994, Nature.

[80]  R. D. Stoner,et al.  ENHANCED ANTITOXIN RESPONSES IN IRRADIATED MICE ELICITED BY COMPLEXES OF TETANUS TOXOID AND SPECIFIC ANTIBODY. , 1963, Journal of immunology.

[81]  Christopher C. Goodnow,et al.  C3d of Complement as a Molecular Adjuvant: Bridging Innate and Acquired Immunity , 1996, Science.

[82]  B. Heyman,et al.  Antibodies to murine complement receptor 1 and 2 can inhibit the antibody response in vivo without inhibiting T helper cell induction. , 1995, Journal of immunology.

[83]  S. Christensen,et al.  The murine complement receptor gene family. IV. Alternative splicing of Cr2 gene transcripts predicts two distinct gene products that share homologous domains with both human CR2 and CR1. , 1990, Journal of immunology.

[84]  R. D. Stoner,et al.  Specificity of Enhanced Immunological Sensitization of Mice Following Injections of Antigens and Specific Antisera.∗ , 1962, Proceedings of the Society for Experimental Biology and Medicine. Society for Experimental Biology and Medicine.

[85]  D. Conrad,et al.  Mouse CD23 regulates monocyte activation through an interaction with the adhesion molecule CD11b/CD18 , 1997, European journal of immunology.

[86]  D. Pearlman.  THE INFLUENCE OF ANTIBODIES ON IMMUNOLOGIC RESPONSES I. THE EFFECT ON THE RESPONSE TO PARTICULATE ANTIGEN IN THE RABBIT , 1967 .

[87]  E. Wiersma.  Enhancement of the Antibody Response to Protein Antigens by Specific IgG under Different Experimental Conditions , 1992, Scandinavian journal of immunology.

[88]  M. Neuberger,et al.  Targeted gene disruption reveals a role for natural secretory IgM in the maturation of the primary immune response. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[89]  A. Schreiber,et al.  Inhibition of Fcγ receptor-mediated phagocytosis by a nonphagocytic Fcγ receptor , 1998 .

[90]  J. Uhr,et al.  Capacity of Pepsin-digested Antibody to inhibit Antibody Formation , 1966, Nature.

[91]  Kazuhiro Nakamura,et al.  Cloning of cDNAs for New Subtypes of Murine Low-Affinity Fc Receptor for IgE (FcεRII/CD23) , 1994 .

[92]  H. Eibel,et al.  Mice deficient in CD23 reveal its modulatory role in IgE production but no role in T and B cell development. , 1994, Journal of immunology.

[93]  M. Pepys.  ROLE OF COMPLEMENT IN INDUCTION OF ANTIBODY PRODUCTION IN VIVO , 1974, The Journal of experimental medicine.

[94]  G. Klaus.  The generation of memory cells. II. Generation of B memory cells with preformed antigen-antibody complexes. , 1978, Immunology.

[95]  J. Kappler,et al.  Regulation of the immune response. I. Differential effect of passively administered antibody on the thymus-derived and bone marrow-derived lymphocytes. , 1971 .

[96]  A. Coutinho,et al.  The enhancement of antibody response by IgM antibodies is dependent on antigen-specific T helper cells. , 1981, Immunobiology.

[97]  R. A. Murgita,et al.  Specific antibody-mediated effect on the immune response. Suppression and augmentation of the primary immune response in mice by different classes of antibodies. , 1972, Immunology.

[98]  M. Ono,et al.  Modulation of Immune Complex–induced Inflammation In Vivo by the Coordinate Expression of Activation and Inhibitory Fc Receptors , 1999, The Journal of experimental medicine.

[99]  B. Heyman,et al.  Restoration of the Antibody Response to IgE/Antigen Complexes in CD23-Deficient Mice by CD23+ Spleen or Bone Marrow Cells1 , 2000, The Journal of Immunology.

[100]  G. Habicht,et al.  Carrier-specific enhancement of the immune response using antigen-antibody complexes. , 1974, Journal of immunology.

[101]  H. Ochs,et al.  The role of complement in the induction of antibody responses. , 1983, Clinical and experimental immunology.

[102]  G. Klaus,et al.  The generation of memory cells. IV. Immunization with antigen-antibody complexes accelerates the development of B-memory cells, the formation of germinal centres and the maturation of antibody affinity in the secondary response. , 1981, Immunology.

[103]  C. Bruijnzeel-Koomen,et al.  Antigen focusing by specific monomeric immunoglobulin E bound to CD23 on Epstein-Barr virus-transformed B cells. , 1993, Human immunology.

[104]  P. Marche,et al.  Amplification of the antibody response by C3b complexed to antigen through an ester link. , 1998, Journal of immunology.

[105]  M. Daëron,et al.  Fc receptor biology. , 2003, Annual review of immunology.

[106]  M. Nose,et al.  Evidence of IgG‐mediated enhancement of the antibody response in vivo without complement activation via the classical pathway , 1990, European journal of immunology.

[107]  E. Holborow,et al.  Complement Dependence of Localisation of Aggregated IgG in Germinal Centres , 1975, Scandinavian journal of immunology.

[108]  G. Klaus,et al.  Crosslinking of surface immunoglobulin and Fc receptors on B lymphocytes inhibits stimulation of inositol phospholipid breakdown via the antigen receptors , 1985, The Journal of experimental medicine.

[109]  V. Holers,et al.  Expression of complement receptors 1 and 2 on follicular dendritic cells is necessary for the generation of a strong antigen-specific IgG response. , 1998, Journal of immunology.

[110]  G. Dennert,et al.  The mechanism of antibody-induced stimulation and inhibition of the immune response. , 1971, Journal of immunology.

[111]  J. Uhr,et al.  Regulatory effect of antibody on the immune response. , 1968, Advances in immunology.

[112]  H. Rapp,et al.  Complement Fixation on Cell Surfaces by 19S and 7S Antibodies , 1965, Science.

[113]  H. Ochs,et al.  Regulation of antibody responses: the role of complement and adhesion molecules. , 1993, Clinical immunology and immunopathology.

[114]  F. Sallusto,et al.  Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor alpha , 1994, The Journal of experimental medicine.

[115]  D. Karp,et al.  Complement opsonization is required for presentation of immune complexes by resting peripheral blood B cells. , 1998, Journal of immunology.

[116]  J. Ahearn,et al.  Disruption of the Cr2 locus results in a reduction in B-1a cells and in an impaired B cell response to T-dependent antigen. , 1996, Immunity.

[117]  B. Heyman,et al.  Immunoregulation by monoclonal sheep erythrocyte-specific IgG antibodies: suppression is correlated to level of antigen binding and not to isotype. , 1984, Journal of immunology.

[118]  D. Parker,et al.  Cross-linking of B lymphocyte Fc gamma receptors and membrane immunoglobulin inhibits anti-immunoglobulin-induced blastogenesis. , 1984, Journal of immunology.

[119]  H. Bazin,et al.  Inhibition of an in vivo antigen-specific IgE response by antibodies to CD23. , 1993, Science.

[120]  J. G. Michael,et al.  Immunoregulation of the anti-bovine serum albumin response by polyclonal and monoclonal antibodies. , 1983, Cellular immunology.

[121]  Gustavsson,et al.  Low Responsiveness to Immunization with Immunoglobulin E/Antigen and Immunoglobulin G/Antigen Complexes in H‐2Ab Mice , 1999, Scandinavian journal of immunology.

[122]  E. Collisson,et al.  Potentiation of antibody responses by specific IgM: specificity and thymus dependency. , 1983, Cellular immunology.

[123]  G. Klaus,et al.  Differing effects of monoclonal anti-hapten antibodies on humoral responses to soluble or particulate antigens. , 1984, Immunology.

[124]  D. Fearon,et al.  CD19: lowering the threshold for antigen receptor stimulation of B lymphocytes. , 1992, Science.

[125]  B. Heyman,et al.  IgG-mediated enhancement of antibody responses is low in Fc receptor gamma chain-deficient mice and increased in Fc gamma RII-deficient mice. , 1999, Journal of immunology.

[126]  B. Heyman.  Fc‐Dependent IgG‐Mediated Suppression of the Antibody Response: Fact or Artefact? , 1990, Scandinavian journal of immunology.

[127]  J. Bonnefoy,et al.  Marked amelioration of established collagen-induced arthritis by treatment with antibodies to CD23 in vivo , 1995, Nature Medicine.

[128]  B. Andersson,et al.  Modulation of Hapten-Specific Antibody Responses with Anticarrier Antibody: I. Differential Effects of IgM and IgG Anticarrier on Primary Direct and Indirect Hapten-Specific Plaque-Forming Cells 1 , 1979, Proceedings of the Society for Experimental Biology and Medicine. Society for Experimental Biology and Medicine.

[129]  P. Debré,et al.  CD23/Fc epsilon RII: signaling and clinical implication. , 1997, International reviews of immunology.

[130]  Jianzhu Chen,et al.  Enhanced B-1 cell development, but impaired IgG antibody responses in mice deficient in secreted IgM. , 1998, Journal of immunology.

[131]  B. Heyman,et al.  Complement activation is not required for IgG‐mediated suppression of the antibody response , 1988, European journal of immunology.

[132]  B. Heyman,et al.  Importance of CD23 for collagen-induced arthritis: delayed onset and reduced severity in CD23-deficient mice. , 1999, Journal of immunology.

[133]  P. Butko,et al.  Studies of group B streptococcal infection in mice deficient in complement component C3 or C4 demonstrate an essential role for complement in both innate and acquired immunity. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[134]  I. Mellman,et al.  Cutting Edge: FcγRII-B1 Regulates the Presentation of B Cell Receptor-Bound Antigens , 1998, The Journal of Immunology.

[135]  J. Prechl,et al.  Modulation of the humoral immune response by antibody-mediated antigen targeting to complement receptors and Fc receptors. , 1999, Journal of immunology.

[136]  H. Ochs,et al.  Role of C3 in humoral immunity. Defective antibody production in C3-deficient dogs. , 1988, Journal of immunology.

[137]  H. Ochs,et al.  Immune response of a patient with deficiency of the fourth component of complement and systemic lupus erythematosus. , 1979, The New England journal of medicine.

[138]  R. Karr,et al.  Markedly impaired humoral immune response in mice deficient in complement receptors 1 and 2. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[139]  H. Heiken,et al.  The IgG Fc receptor family , 1998, Annals of Hematology.

[140]  D. Bitter‐Suermann,et al.  Linkage of total deficiency of the second component (C2) of the complement system and of genetic C2-polymorphism to the major histocompatibility complex of the guinea pig. , 1981, Journal of immunology.

[141]  B. Heyman,et al.  IgM-mediated enhancement of in vivo anti-sheep erythrocyte antibody responses: isotype analysis of the enhanced responses. , 1985, Cellular immunology.

[142]  D. Fearon,et al.  The CD19/CR2/TAPA-1 complex of B lymphocytes: linking natural to acquired immunity. , 1995, Annual review of immunology.

[143]  B. Heyman,et al.  In vivo inhibition of the antibody response by a complement receptor- specific monoclonal antibody , 1990, The Journal of experimental medicine.

[144]  N. Sinclair.  REGULATION OF THE IMMUNE RESPONSE , 1969, The Journal of Experimental Medicine.

[145]  D. Bitter‐Suermann,et al.  The role and mechanism of cobra venom factor-induced suppression of the humoral immune response in guinea pigs. , 1986, Journal of immunology.

[146]  M. Carroll,et al.  The role of complement and complement receptors in induction and regulation of immunity. , 1998, Annual review of immunology.

[147]  D. Fearon,et al.  Suppression of the immune response by a soluble complement receptor of B lymphocytes. , 1991, Science.

[148]  V. Vetvicka,et al.  Natural antibody and complement-mediated antigen processing and presentation by B lymphocytes. , 1994, Journal of immunology.

[149]  W. M. Wason.  Regulation of the immune response with antigen specific IgM antibody: a dual role. , 1973, Journal of immunology.

[150]  S. Pincus,et al.  Absolute requirement for complement in monoclonal IgM antibody-mediated protection against experimental infection with type III group B streptococci. , 1984, The Journal of infectious diseases.

[151]  J. Bonnefoy,et al.  CD21 is a ligand for CD23 and regulates IgE production , 1992, Nature.

[152]  N. K. Jerne,et al.  COMPETITION OF 19S AND 7S ANTIGEN RECEPTORS IN THE REGULATION OF THE PRIMARY IMMUNE RESPONSE , 1968, The Journal of experimental medicine.

[153]  M. Hulett,et al.  Molecular basis of Fc receptor function. , 1994, Advances in immunology.

[154]  W. Fridman,et al.  The same tyrosine-based inhibition motif, in the intracytoplasmic domain of Fc gamma RIIB, regulates negatively BCR-, TCR-, and FcR-dependent cell activation. , 1995, Immunity.

[155]  B. Heyman,et al.  Dual Immunoregulatory Effects of Monoclonal IgG‐Antibodies: Suppression and Enhancement of the Antibody Response , 1989, Scandinavian journal of immunology.

[156]  Á. Corbí,et al.  CD23 regulates monocyte activation through a novel interaction with the adhesion molecules CD11b-CD18 and CD11c-CD18. , 1995, Immunity.

[157]  J. Engel,et al.  Dimeric, trimeric and tetrameric complexes of immunoglobulin G fix complement. , 1980, The Biochemical journal.

[158]  D. Conrad,et al.  Murine follicular dendritic cells and low affinity Fc receptors for IgE (Fc epsilon RII). , 1992, Journal of immunology.

[159]  W. Fridman,et al.  Cytoplasmic domain heterogeneity and functions of IgG Fc receptors in B lymphocytes. , 1992, Science.

[160]  D. Beale,et al.  Structure and function of the constant regions of immunoglobulins , 1976, Quarterly Reviews of Biophysics.

[161]  B. Heyman,et al.  Complement activation is required for IgM-mediated enhancement of the antibody response , 1988, The Journal of experimental medicine.

[162]  M. Walport,et al.  Splenic uptake of immune complexes in man is complement-dependent. , 1993, Journal of immunology.

[163]  J. Sidney,et al.  Functional consequences of engagement of the T cell receptor by low affinity ligands. , 1993, Journal of immunology.