T-cell regulation: with complements from innate immunity (original) (raw)
Medhzitov, R. & Janeway, C. A. Jr. Decoding the patterns of self and non-self by the innate immune system. Science296, 298–300 (2002). Article Google Scholar
Metschnikoff, E. Sur la lutte des cellule de l'organisme contre l'invasion des microbes. Ann. Inst. Pasteur1, 321 (1887) (in French). Google Scholar
Bordet, J. & Gengou, O. Sur l'existence de substances sensibilisatrices dans la plupart des serum antimicrobien. Ann. Inst. Pasteur15, 289–302 (1901) (in French). Google Scholar
Volanakis, J. E. in The Human Complement System in Health and Disease 10th edn (eds Volanakis, J. E. & Frank, M. M.) 9–32 (Marcel Dekker, New York, 1998). Book Google Scholar
Morgan, B. P. & Harris, C. L. Complement Regulatory Proteins (Academic, New York, 1999). Google Scholar
Kim, D. D. & Song, W.-C. Membrane complement regulatory proteins. Clin. Immunol.118, 127–136 (2006). ArticleCASPubMed Google Scholar
Korb, L. C. & Ahearn, J. M. C1q binds directly and specifically to surface blebs of apoptotic human keratinocytes: complement deficiency and systemic lupus erythematosus revisited. J. Immunol.158, 4525–4528 (1997). CASPubMed Google Scholar
Botto M. et al. Homozygous C1q deficiency causes glomerulonephritis associated with multiple apoptotic bodies. Nature Genet.19, 56–59 (1998). ArticleCASPubMed Google Scholar
Riley-Vargas, R. C., Lanzendorf, S. & Atkinson, J. P. Targeted and restricted complement activation on acrosome-reacted spermatozoa. J. Clin. Invest.115, 1241–1249 (2005). ArticleCASPubMedPubMed Central Google Scholar
Harris, C. L., Mizuno, M. & Morgan, B. P. Complement and complement regulators in the male reproductive system. Mol. Immunol.43, 57–67 (2006). ArticleCASPubMed Google Scholar
Nussenzweig, V., Bianco, C., Dukor, P. & Eden, A. in Progress in Immunology Vol. 59 (ed. Amos, B.) 73–81 (Academic, New York, 1971). Book Google Scholar
Carroll, M. C. The complement system in regulation of adaptive immunity. Nature Immunol.10, 981–986 (2004). ArticleCAS Google Scholar
Mastellos, D. & Lambris, J. D. Complement: more than a 'guard' against invading pathogens? Trends Immunol.23, 485–491 (2002). ArticleCASPubMed Google Scholar
Pepys, M. B. 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 (1974). ArticleCASPubMedPubMed Central Google Scholar
Carter, R. H., Spycher, M. O., Ng, Y. C., Hoffman, R. & Fearon, D. T. Synergistic interaction between complement receptor type 2 and membrane IgM on B lymphocytes. J. Immunol.141, 457–467 (1988). CASPubMed Google Scholar
Dempsey, P. W., Allison, M. E., Akkaraju, S., Goodnow, C. C. & Fearon, D. T. C3d of complement as a molecular adjuvant: bridging innate and acquired immunity. Science271, 348–350 (1996). ArticleCASPubMed Google Scholar
Fearon, D. T. & Carter, R. H. The CD19/CR2/TAPA-1 complex of B lymphocytes: linking natural to acquired immunity. Ann. Rev. Immunol.13, 127–149 (1995). ArticleCAS Google Scholar
Fang, Y., Xu, C., Fu, Y., Holer, V. M. & Molina, H. 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 (1998). CASPubMed Google Scholar
Molina, H. et al. Markedly impaired humoral immune response in mice deficient in complement receptors 1 and 2. Proc. Natl Acad. Sci. USA93, 3357–3361 (1996). ArticleCASPubMedPubMed Central Google Scholar
Kemper, C. et al. Activation of human CD4+ cells with CD3 and CD46 induces a T-regulatory cell 1 phenotype. Nature421, 388–392 (2003). Provides evidence that a complement inhibitor influences T-cell responses through the generation of IL-10-producing regulatory T cells. ArticleCASPubMed Google Scholar
Morgan, B. P., Marchbank, K. J., Longhi M. P., Harris, C. L. & Gallimore, A. M. Complement: central to innate immunity and bridging to adaptive responses. Immunol. Lett.97, 171–179 (2005). ArticleCASPubMed Google Scholar
Longhi, M. P., Harris, C. L., Morgan, B. P. & Gallimore, A. Holding T cell in check — a new role for complement regulators? Trends Immunol.27, 102–108 (2006). ArticleCASPubMed Google Scholar
Hawlisch, H. & Köhl, J. Complement and Toll-like receptors: key regulators of adaptive immune responses. Mol. Immunol.43, 13–21 (2006). ArticleCASPubMed Google Scholar
Castellano, G. et al. Maturation of dendritic cells abrogates C1q production in vivo and in vitro. Blood103, 3813–3820 (2004). ArticleCASPubMed Google Scholar
Jiang, K., Chen, Y., Xu, C. S. & Jarvis, J. N. T cell activation by soluble C1q-bearing immune complexes: implications for the pathogenisis of rheumatoid arthritis. Clin. Exp. Immunol.131, 61–67 (2003). ArticleCASPubMedPubMed Central Google Scholar
Jacquier-Sarlin, M. R., Gabert, F. M., Villiers, M. B. & Colomb, M. G. Modulation of antigen processing and presentation by covalently linked complement C3b fragment. Immunology84, 164–170 (1995). CASPubMedPubMed Central Google Scholar
Kerekes, K. et al. Adjuvant effect of γ-inulin is mediated by C3 fragments deposited on antigen-presenting cells. J. Leuk. Biol.69, 69–74 (2001). CAS Google Scholar
Hawlisch, H., Wills-Karp, M., Karp, C. L. & Köhl, J. The anaphylatoxins bridge innate and adaptive immune responses in allergic asthma. Mol. Immunol.41, 123–131 (2004). ArticleCASPubMed Google Scholar
Sozzani, S. et al. Migration of dendritic cells in response to formyl peptides, C5a, and a distinct set of chemokines. J. Immunol.155, 3292–3295 (1995). CASPubMed Google Scholar
Wetsel, R. A. Structure, function and cellular expression of complement anaphylatoxin receptors. Curr. Opin. Immunol.7, 48–53 (1995). ArticleCASPubMed Google Scholar
Drouin, S. M., Corry, D. B., Kildsgaard, J. & Wetsel, R. A. Cutting edge: the absence of C3 demonstrates a role for complement in TH2 effector functions in a murine model of pulmonary allergy. J. Immunol.167, 4141–4145 (2001). This report, along with references 38–41 and 56, delineates the impact of the anaphylatoxins on T-cell lineage commitment during APC–T-cell interactions. ArticleCASPubMed Google Scholar
Drouin, S. M., Corry, D. B., Hollman, T. J., Kildsgaard, J. & Wetsel, R. A. Absence of the complement anaphylatoxin C3a receptor suppresses TH2 functions in a murine model of pulmonary allergy. J. Immunol.169, 5926–5933 (2002). ArticleCASPubMed Google Scholar
Gerard, N. P. & Gerard, C. Complement in allergy and asthma. Curr. Opin. Immunol.14, 705–708 (2002). ArticleCASPubMed Google Scholar
Kawamoto, S. et al. The anaphylatoxin C3a downregulates the TH2 response to epicutaneously introduced antigen. J. Clin. Invest.114, 399–407 (2004). ArticleCASPubMedPubMed Central Google Scholar
Hawlisch, H. et al. C5a negatively regulates Toll-like receptor 4-induced immune responses. Immunity22, 415–426 (2005). ArticleCASPubMed Google Scholar
Källström, H., Islam, M. S., Berggren, P. O. & Jonsson, A. B. Cell signaling by the type IV pili of pathogenic Neisseria. J. Biol. Chem.273, 21777–21782 (1998). ArticlePubMed Google Scholar
Karp, C. L. et al. Mechanisms of suppression of cell-mediated immunity by measles virus. Science273, 228–231 (1996). Measles virus uses the immunomodulatory properties of a complement regulator to suppress the immune response. ArticleCASPubMed Google Scholar
Cattaneo, R. Four viruses, two bacteria, and one receptor: membrane cofactor protein (CD46) as pathogens' magnet. J. Virol.78, 4385–4388 (2004). ArticleCASPubMedPubMed Central Google Scholar
Heeger, P. S. et al. Decay-accelerating factor modulates induction of T cell immunity. J. Exp. Med.201, 1523–1530 (2005). Shows that complement components produced by APCs on antigen encounter modulate subsequent cytokine production by T cells. ArticleCASPubMedPubMed Central Google Scholar
Helmy, K. Y. et al. CRIg: a macrophage complement receptor required for phagocytosis of circulating pathogens. Cell124, 915–927 (2006). ArticleCASPubMed Google Scholar
Kang, Y.-S. et al. A dominant complement fixation pathway for pneumococcal polysaccharides initiated by SIGN-R1 interacting with C1q. Cell125, 47–58 (2006). ArticleCASPubMed Google Scholar
Wagner, C. & Hänsch, G. M. Receptors for complement C3 on T-lymphocytes: relics of evolution or functional molecules. Mol. Immunol.43, 22–30 (2006). ArticleCASPubMed Google Scholar
Wilson, J. G., Tedder, T. F. & Fearon, D. T. Characterization of human T cells that express the C3b receptor. J. Immunol.131, 684–689 (1983). CASPubMed Google Scholar
Wagner, C. The complement receptor 1, CR1 (CD35), mediates inhibitory signals in human T-lymphocytes. Mol. Immunol.43, 643–651 (2006). ArticleCASPubMed Google Scholar
Muto, S., Vetvicka, V. & Ross, G. D. CR3 (CD11b/CD18) expressed by cytotoxic T cells and natural killer cells is upregulated in a manner similar to neutrophil CR3 following stimulation with various activating agents. J. Clin. Immunol.13, 175–184 (1993). ArticleCASPubMed Google Scholar
Chen, A. et al. Human T cells express specific sites for C1q: role in T cell activation and proliferation. J. Immunol.153, 1430–1440 (1994). CASPubMed Google Scholar
Nataf, S., Davoust, N., Ames, R. S. & Barnum, S. A. Human T cells express the C5a receptor and are chemoattracted to C5a. J. Immunol.162, 4018–4023 (1999). CASPubMed Google Scholar
Tsuji, R. F. et al. Early local generation of C5a initiates the elicitation of contact sensitivity by leading to early T cell recruitment. J. Immunol.165, 1588–1598 (2000). ArticleCASPubMed Google Scholar
Grant, E. P. et al. Essential role for the C5a receptor in regulating the effector phase of synovial infiltration and joint destruction in experimental arthritis. J. Exp. Med.196, 1461–1471 (2002). ArticleCASPubMedPubMed Central Google Scholar
Werfel, T. et al. Activated human T lymphocytes express a functional C3a receptor. J. Immunol.165, 6599–6605 (2000). ArticleCASPubMed Google Scholar
Astier, A. L., Trescol-Biemont, M.-C., Azocar, O., Lamouille, B. & Rabourdin-Combe, C. Cutting edge: CD46, a new costimulatory molecule for T cells, that induces p120CBL and LAT phosphorylation. J. Immunol.164, 6091–6095 (2000). Establishes that signalling through CD46 modulates T-cell proliferation. This paper laid the ground work for the subsequent studies of the effects on T-cell function induced by CD46 crosslinking. ArticleCASPubMed Google Scholar
Grossman, W. J. et al. Human T regulatory cells can use the perforin pathway to cause autologous target cell death. Immunity21, 589–601 (2004). Establishes a simple paradigm for how regulatory T cells might influence immune responses. In humans, natural TRegcells synthesize granzyme A, whereas adaptive regulatory T cells produce granzyme B. On CD46 activation both cell types can kill activated, immunocompetent cells. ArticleCASPubMed Google Scholar
Sanchez, A., Feito, M. J. & Rojo, J. M. CD46-mediated costimulation induces a TH1-biased response and enhances early TCR/CD3 signaling in human CD4+ T lymphocytes. Eur. J. Immunol.34, 2439–2448 (2004). ArticleCASPubMed Google Scholar
Liu, J. et al. The complement inhibitory protein DAF (CD55) suppresses T cell immunity in vivo. J. Exp. Med.201, 567–577 (2005). This report, together with reference 45, shows that complement deposition on APCs and T cells influences T-cell proliferation and cytokine production during APC–T-cell interactions. ArticleCASPubMedPubMed Central Google Scholar
Korty, P. E., Brando, C. & Shevach, E. M. CD59 functions as a signal-transducing molecule for human T cell activation. J. Immunol.146, 4092–4098 (1991). CASPubMed Google Scholar
Kopf, M., Abel, B., Gallimore, A., Carroll, M. & Bachmann, M. F. Complement component C3 promotes T-cell priming and lung migration to control acute influenza virus infection. Nature Med.8, 373–378 (2002). References 63–68 indicate that complement activation (and natural antibodies) are required for optimal CD4+ and CD8+ T-cell responses to viral infections. ArticleCASPubMed Google Scholar
Suresh, M. et al. Complement component 3 is required for optimal expansion of CD8 T cells during a system viral infection. J. Immunol.170, 788–794 (2003). ArticleCASPubMed Google Scholar
Verschoor, A., Brockman, M. A., Gadjeva, M., Knipe, D. M. & Carroll, M. C. Myeloid C3 determines induction of humoral responses to peripheral herpes simplex virus infection. J. Immunol.171, 5363–5371 (2003). ArticleCASPubMed Google Scholar
Stager, S. et al. Natural antibodies and complement are endogenous adjuvants for vaccine-induced CD8+ T cell responses. Nature Med.9, 1287–1292 (2003). ArticlePubMedCAS Google Scholar
Hopken, U. E., Lu, B., Gerard, N. P. & Gerard, C. The C5a chemoattractant receptor mediates mucosal defence to infection. Nature383, 86–89 (1996). ArticleCASPubMed Google Scholar
Kim, A. H. et al. Complement C5a receptor is essential for the optimal generation of CD8+ T cell responses. J. Immunol.173, 2524–2529 (2004). ArticleCASPubMed Google Scholar
Karp, C. L. et al. Identification of complement factor 5 as a susceptibility locus for experimental allergic asthma. Nature Immunol.1, 221–226 (2000). ArticleCAS Google Scholar
Wittman, M. et al. C5a suppresses the production of IL-12 by IFN-γ-primed and lipopolysaccharide-challenged human monocytes. J. Immunol.162, 6763–6769 (1999). Google Scholar
Marie, J. C. et al. Linking innate and acquired immunity: divergent role of CD46 cytoplasmic domains in T cell induced inflammation. Nature Immunol.3, 659–666 (2002). Thisin vivostudy supports a role for CD46 in the regulation of T-cell responses. The authors used mice transgenic for human CD46 to modulate T-cell responses in a contact-hypersensitivity model. ArticleCAS Google Scholar
Longhi, M. P., Sivasankar, B., Omidvar, N., Morgan, B. P. & Gallimore, A. Cutting edge: murine CD59a modulates antiviral CD4+ T cell activity in a complement-independent manner. J. Immunol.175, 7098–7102 (2005). ArticleCASPubMed Google Scholar
Riley-Vargas, R. C., Gill, D. B., Kemper, C., Liszewski, M. K. & Atkinson, J. P. CD46: expanding beyond complement regulation. Trends Immunol.25, 496–503 (2004). ArticleCASPubMed Google Scholar
Kemper, C., Verbsky, J. W., Price, J. D. & Atkinson, J. P. T cell stimulation and regulation: with complements from CD46. Immunol. Res.32, 31–43 (2005). ArticleCASPubMed Google Scholar
Foley, S., Li, B., Dehoff, M., Molina, M. & Holers, V. M. Mouse Crry/p65 is a regulator of the alternative pathway of complement activation. Euro. J. Immunol.23, 1381–1384 (1993). ArticleCAS Google Scholar
Fernandez-Centeno, E., de Ojeda, G., Rojo, J. M. & Portoles, P. Crry/p65, a membrane complement regulatory protein, has costimulatory properties on mouse T cells. J. Immunol.164, 4533–4542 (2000). ArticleCASPubMed Google Scholar
Elward, et al. CD46 plays a key role in tailoring innate immune recognition of apoptotic and necrotic cells. J. Biol. Chem.280, 36342–36354 (2005). Shows that the expression profile of complement receptors and regulators can send inhibitory (or inducing) phagocytic signals. Proposes, together with reference 79, new roles for complement in the apoptotic process in addition to its function in the safe removal of dead cells. ArticleCASPubMed Google Scholar
Cole, D. S., Hughes, T. R., Gasque, P. & Morgan, B. P. Complement regulator loss on apoptotic neuronal cells causes increased complement activation and promotes both phagocytosis and cell lysis. Mol. Immunol.43, 1953–1964 (2006). ArticleCASPubMed Google Scholar
Legembre, P. et al. Cutting edge: modulation of Fas-mediated apoptosis by lipid rafts in T lymphocytes. J. Immunol.176, 716–720 (2006). ArticleCASPubMed Google Scholar
Grossmann, W. et al. Differential expression of granzymes A and B in human cytotoxic lymphocyte subsets and T regulatory cells. Blood104, 2840–2848 (2004). ArticleCAS Google Scholar
Bluestone, J. A. & Abbas, A. K. Natural versus adapative regulatory T cells. Nature Rev. Immunol.3, 253–257 (2003). ArticleCAS Google Scholar
Jonuleit, H. & Schmitt, E. The regulatory T cell family: distinct subsets and their interrelations. J. Immunol.171, 6323–6327 (2003). ArticleCASPubMed Google Scholar
Price, J. D. et al. Induction of a regulatory phenotype in human CD4+ T cells by streptococcal M protein. J. Immunol.175, 677–684 (2005). ArticleCASPubMed Google Scholar
Groux, H. et al. A CD4+ T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature389, 737–742 (1997). ArticleCASPubMed Google Scholar
Asseman, C., Mauze, S., Leach, M. W., Coffman, R. L. & Powrie, F. An essential role for interleukin-10 in the function of regulatory T cells that inhibit intestinal inflammation. J. Exp. Med.190, 995–1004 (1999). ArticleCASPubMedPubMed Central Google Scholar
Gondek, D. C., Lu, L. F., Quezada, S. A., Sakaguchi, S. & Noelle, R. J. Cutting edge: contact-mediated suppression by CD4+CD25+ regulatory cells involves a granzyme B-dependent, perforin-independent mechanism. J. Immunol.174, 1783–1786 (2005). ArticleCASPubMed Google Scholar
Sakaguchi, S. Naturally arising Foxp3-expressing CD25+CD4+ regulatory T cells in immunological tolerance to self and non-self. Nature Immunol.6, 345–352 (2005). ArticleCAS Google Scholar
Fukaura, H. et al. Induction of circulating myelin basic protein and proteolipid protein-specific transforming growth factor-β1-secreting TH3 T cells by oral administration of myelin in multiple sclerosis patients. J. Clin. Invest.98, 70–77 (1996). ArticleCASPubMedPubMed Central Google Scholar
O'Garra, A. & Vieira, P. Regulatory T cells and mechanisms of immune system control. Nature Med.10, 801–805 (2004). ArticleCASPubMed Google Scholar
Barchet, W. et al. Complement-induced regulatory T cells suppress T cell responses but allow for dendritic cell activation. Blood107, 1497–1504 (2006). ArticleCASPubMedPubMed Central Google Scholar
Cong, Y., Weaver, C. T., Lazenby, A. & Elson, C. O. Bacterial-reactive T regulatory cells inhibit pathogenic immune responses to enteric flora. J. Immunol.169, 6112–6119 (2002). ArticleCASPubMed Google Scholar
Kuhn, R., Lohler, J., Rennick, D., Rajewski, K. & Müller, W. Interleukin-10-deficient mice develop chronic enterocolitis. Cell75, 263–274 (1993). ArticleCASPubMed Google Scholar
Sadlack, B. et al. Ulcerative colitis-like disease in mice with a disrupted interleukin-2 gene. Cell75, 253–261 (1993). ArticleCASPubMed Google Scholar
McGuirk, P., McCann, C. & Mills, K. H. Pathogen-specific T regulatory 1 cells induced in the respiratory tract by a bacterial molecule that stimulates interleukin 10 production by dendritic cells: a novel strategy for evasion of protective T helper type 1 responses by Bordetella pertussis. J. Exp. Med.195, 221–231 (2002). ArticleCASPubMedPubMed Central Google Scholar
Lavelle, E. C. et al. Cholera toxin promotes the induction of regulatory T cells specific for bystander antigens by modulating dendritic cell activation. J. Immunol.171, 2384–2392 (2003). ArticleCASPubMed Google Scholar
Russel, S. CD46: a complement regulator and pathogen receptor that mediates links between innate and acquired immune function. Tissue Antigens64, 111–118 (2004). ArticleCAS Google Scholar
Wang, G., Liszewski, M. K., Chan, A. C. & Atkinson, J. P. Membrane cofactor protein (MCP; CD46): isoform-specific tyrosine phosphorylation. J. Immunol.164, 1839–1846 (2000). ArticleCASPubMed Google Scholar
Kurita-Taniguchi, M. et al. Functional modulation of human macrophages through CD46 (measles virus receptor): production of IL-12 p40 and nitric oxide in association with recruitment of protein-tyrosine phosphatase SHP-1 to CD46. J. Immunol.165, 5143–5152 (2000). ArticleCASPubMed Google Scholar
Ludford-Menting, M. J. et al. A functional interaction between CD46 and DLG4: a role for DLG4 in epithelial polarization. J. Biol. Chem.277, 4477–4484 (2002). ArticleCASPubMed Google Scholar
Zaffran, Y. et al. CD46/CD3 costimulation induces morphological changes of human T cells and activation of Vav, Rac, and extracellular signal-regulated kinase mitogen-activated protein kinase. J. Immunol.167, 6780–6785 (2001). ArticleCASPubMed Google Scholar
Davis, L. S., Patel, S. S., Atkinson, J. P. & Lipsky, P. E. Decay-accelerating factor functions as a signal transducing molecule for human T cells. J. Immunol.141, 2246–2252 (1988). CASPubMed Google Scholar
Loertscher, R. & Lavery, P. The role of glycosyl phosphatidyl inositol (GPI)-anchored cell surface proteins in T-cell activation. Transpl. Immunol.9, 93–96 (2002). ArticleCASPubMed Google Scholar
Pratt, J. R., Basher, S. A. & Sacks, S. H. Local synthesis of complement component C3 regulates acute renal transplant rejection. Nature Med.8, 582–587 (2002). Complement mediates graft rejection through mechanisms that include increases in pro-inflammatory cytokine secretion by vessel walls and the recruitment of effector T cells. ArticleCASPubMed Google Scholar
Sacks, S. H., Chowdhury, P. & Zhou, W. Role of the complement system in rejection. Curr. Opin. Immunol.15, 487–492 (2003). ArticleCASPubMed Google Scholar
Makrides, S. C. Therapeutic inhibition of the complement system. Pharm. Rev.50, 59–87 (1998). CASPubMed Google Scholar