A new role for complement C3: Regulation of antigen processing through an inhibitory activity

Molecular Immunology

Volumn 45, Issue 13, 2008, Pages 3509-3516

  Villiers, Christian L ^a,b   Cretin, François ^b,c,d   Lefebvre, Nicole ^a,b   Marche, Patrice N ^a,b   Villiers, Marie Bernadette ^a,b  

^a INSERM   (France)

^b UNIV GRENOBLE ALPES   (France)

^c CEA GRENOBLE   (France)

^d CNRS   (France)

Author keywords

Antigen presentation; C3; Complement; Macrophages; Proteolysis

Indexed keywords

COMPLEMENT COMPONENT C3; SERINE PROTEINASE; TETANUS TOXIN;

ANTIGEN PRESENTATION; ARTICLE; CELL STRAIN U937; CELLULAR DISTRIBUTION; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNE RESPONSE; PRIORITY JOURNAL; PROTEIN DEGRADATION;

EID: 46949098148     PISSN: 01615890     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molimm.2008.05.015     Document Type: Article

References (56)

1. Al Salihi A., Ripoche J., Pruvost L., and Fontaine M. Purification of complement components by hydrophobic affinity chromatography on phenyl-sepharose: purification of human C5. FEBS Lett. 150 (1982) 238-242
2. Armstrong P.B., and Quigley J.P. Alpha2-macroglobulin: an evolutionarily conserved arm of the innate immune system. Dev. Comp. Immunol. 23 (1999) 375-390
3. Bottger E.C., Metzger S., Bitter-Suermann D., Stevenson G., Kleindienst S., and Burger R. Impaired humoral immune response in complement C3-deficient guinea pigs: absence of secondary antibody response. Eur. J. Immunol. 16 (1986) 1231-1235
4. Burster T., Beck A., Tolosa E., Schnorrer P., Weissert R., Reich M., Kraus M., Kalbacher H., Haring H.U., Weber E., Overkleeft H., and Driessen C. Differential processing of autoantigens in lysosomes from human monocyte-derived and peripheral blood dendritic cells. J. Immunol. 175 (2005) 5940-5949
5. Carroll M.C. The complement system in regulation of adaptive immunity. Nat. Immunol. 5 (2004) 981-986
6. Cherukuri A., Cheng P.C., Sohn H.W., and Pierce S.K. The CD19/CD21 complex functions to prolong B cell antigen receptor signaling from lipid rafts. Immunity 14 (2001) 169-179
7. Cretin F.C., Serra V.A., Villiers M.B., Laharie A.M., Marche P.N., and Gabert F.M. C3b complexation diversifies naturally processed T cell epitopes. Mol. Immunol. 44 (2007) 2893-2899
8. Delamarre L., Pack M., Chang H., Mellman I., and Trombetta E.S. Differential lysosomal proteolysis in antigen-presenting cells determines antigen fate. Science 307 (2005) 1630-1634
9. Delamarre L., Couture R., Mellman I., and Trombetta E.S. Enhancing immunogenicity by limiting susceptibility to lysosomal proteolysis. J. Exp. Med. 203 (2006) 2049-2055
10. Dempsey P.W., Allison M.E., Akkaraju S., Goodnow C.C., and Fearon D.T. C3d of complement as a molecular adjuvant: bridging innate and acquired immunity. Science 271 (1996) 348-350
11. Dodds A.W., and Law S.K. Structural basis of the binding specificity of the thioester-containing proteins, C4, C3 and alpha-2-macroglobulin. Complement 5 (1988) 89-97
12. Einstein L.P., Hansen P.J., Ballow M., Davis III A.E., Davis J.S.T., Alper C.A., Rosen F.S., and Colten H.R. Biosynthesis of the third component of complement (C3) in vitro by monocytes from both normal and homozygous C3-deficient humans. J. Clin. Invest. 60 (1977) 963-969
13. Fearon D.T., and Carter R.H. The CD19/CR2/TAPA-1 complex of B lymphocytes: linking natural to acquired immunity. Annu. Rev. Immunol. 13 (1995) 127-149
14. Fischer M.B., Ma M., Hsu N.C., and Carroll M.C. Local synthesis of C3 within the splenic lymphoid compartment can reconstitute the impaired immune response in C3-deficient mice. J. Immunol. 160 (1998) 2619-2625
15. Hawlisch H., Wills-Karp M., Karp C.L., and Kohl J. The anaphylatoxins bridge innate and adaptive immune responses in allergic asthma. Mol. Immunol. 41 (2004) 123-131
16. Hewitt E.W., Treumann A., Morrice N., Tatnell P.J., Kay J., and Watts C. Natural processing sites for human cathepsin E and cathepsin D in tetanus toxin: implications for T cell epitope generation. J. Immunol. 159 (1997) 4693-4699
17. Hsieh C.S., deRoos P., Honey K., Beers C., and Rudensky A.Y. A role for cathepsin L and cathepsin S in peptide generation for MHC class II presentation. J. Immunol. 168 (2002) 2618-2625
18. Jacquier-Sarlin M.R., Gabert F.M., Villiers M.B., and Colomb M.G. Modulation of antigen processing and presentation by covalently linked complement C3b fragment. Immunology 84 (1995) 164-170
19. Janssen B.J., Huizinga E.G., Raaijmakers H.C., Roos A., Daha M.R., Nilsson-Ekdahl K., Nilsson B., and Gros P. Structures of complement component C3 provide insights into the function and evolution of immunity. Nature 437 (2005) 505-511
20. Law S.K., Lichtenberg N.A., and Levine R.P. Evidence for an ester linkage between the labile binding site of C3b and receptive surfaces. J. Immunol. 123 (1979) 1388-1394
21. Lopez-Rodriguez C., and Corbi A.L. PU.1 negatively regulates the CD11c integrin gene promoter through recognition of the major transcriptional start site. Eur. J. Immunol. 27 (1997) 1843-1847
22. Manoury B., Hewitt E.W., Morrice N., Dando P.M., Barrett A.J., and Watts C. An asparaginyl endopeptidase processes a microbial antigen for class II MHC presentation. Nature 396 (1998) 695-699
23. Morgan B.P., Marchbank K.J., Longhi M.P., Harris C.L., and Gallimore A.M. Complement: central to innate immunity and bridging to adaptive responses. Immunol. Lett. 97 (2005) 171-179
24. Ochs H.D., Wedgwood R.J., Frank M.M., Heller S.R., and Hosea S.W. The role of complement in the induction of antibody responses. Clin. Exp. Immunol. 53 (1983) 208-216
25. Peng Q., Li K., Patel H., Sacks S.H., and Zhou W. Dendritic cell synthesis of C3 is required for full T cell activation and development of a Th1 phenotype. J. Immunol. 176 (2006) 3330-3341
26. 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 (1974) 126-145
27. Perrin-Cocon L.A., Villiers C.L., Salamero J., Gabert F., and Marche P.N. B cell receptors and complement receptors target the antigen to distinct intracellular compartments. J. Immunol. 172 (2004) 3564-3572
28. Polla B.S., Gabert F., Peyrusse B.M., and Jacquier-Sarlin M.R. Increased proteolysis of diphtheria toxin by human monocytes after heat shock: a subsidiary role for heat-shock protein 70 in antigen processing. Immunology 120 (2007) 230-241
29. Puri J., and Factorovich Y. Selective inhibition of antigen presentation to cloned T cells by protease inhibitors. J. Immunol. 141 (1988) 3313-3317
30. Rey-Millet C.A., Chesne S., and Colomb M.G. Associated complement C3b. Towards an understanding of its intracellular modifications. Mol. Immunol. 30 (1993) 855-864
31. Rey-Millet C.A., Villiers C.L., Gabert F.M., Chesne S., and Colomb M.G. C3b covalently associated to tetanus toxin modulates TT processing and presentation by U937 cells. Mol. Immunol. 31 (1994) 1321-1327
32. Ruckrich T., Brandenburg J., Cansier A., Muller M., Stevanovic S., Schilling K., Wiederanders B., Beck A., Melms A., Reich M., Driessen C., and Kalbacher H. Specificity of human cathepsin S determined by processing of peptide substrates and MHC class II-associated invariant chain. Biol. Chem. 387 (2006) 1503-1511
33. Salacinski P.R.P., McLean C., Sykes J.E.C., Clement-Jones V.V., and Lowry P.J. Iodination of proteins, glycoproteins and peptides using a solid phase oxidising agent, 1,3,4,6-tetrachloro-3,6 diphenyl glycoluril (Iodogen). Anal. Biochem. 117 (1981) 136-146
34. Santoro L., Drouet C., Reboul A., Mach J.P., and Colomb M.G. Covalent binding of C3b to monoclonal antibodies selectively up-regulates heavy chain epitope recognition by T cells. Eur. J. Immunol. 24 (1994) 1620-1626
35. Savina A., Jancic C., Hugues S., Guermonprez P., Vargas P., Moura I.C., Lennon-Dumenil A.M., Seabra M.C., Raposo G., and Amigorena S. NOX2 controls phagosomal pH to regulate antigen processing during crosspresentation by dendritic cells. Cell 126 (2006) 205-218
36. Schulman E.S., Post T.J., Henson P.M., and Giclas P.C. Differential effects of the complement peptides, C5a and C5a des Arg on human basophil and lung mast cell histamine release. J. Clin. Invest. 81 (1988) 918-923
37. Serra V.A., Cretin F., Pepin E., Gabert F.M., and Marche P.N. Complement C3b fragment covalently linked to tetanus toxin increases lysosomal sodium dodecyl sulfate-stable HLA-DR dimer production. Eur. J. Immunol. 27 (1997) 2673-2679
38. Shi G.P., Villadangos J.A., Dranoff G., Small C., Gu L., Haley K.J., Riese R., Ploegh H.L., and Chapman H.A. Cathepsin S required for normal MHC class II peptide loading and germinal center development. Immunity 10 (1999) 197-206
39. Sim R.B., Twose T.M., Paterson D.S., and Sim E. The covalent-binding reaction of complement component C3. Biochem. J. 193 (1981) 115-127
40. Sundström G., and Nilsson K. Establishment and characterization of a human histiocytic cell-line (U937). Int. J. Cancer 17 (1976) 565-577
41. Tack B.D., and Prahl J.W. Third component of human complement: purification from plasma and physicochemical characterization. Biochemistry 15 (1976) 4513-4521
42. Takafuji S., Tadokoro K., Ito K., and Dahinden C.A. Degranulation from human eosinophils stimulated with C3a and C5a. Int. Arch. Allergy Immunol. 104 Suppl. 1 (1994) 27-29
43. Takahashi H., Cease K.B., and Berzofsky J.A. Identification of proteases that process distinct epitopes on the same protein. J. Immunol. 142 (1989) 2221-2229
44. Vidard L., Rock K.L., and Benacerraf B. The generation of immunogenic peptides can be selectively increased or decreased by proteolytic enzyme inhibitors. J. Immunol. 147 (1991) 1786-1791
45. Villiers C.L., and Villiers M.B. Modifications of the properties of C3 complement protein after proteolytic cleavage. Recent Res. Dev. Biochem. 4 (2003) 685-696
46. Villiers M.B., Villiers C.L., Wright J.F., Maison C.M., and Colomb M.G. Formation of covalent C3b-tetanus toxin complexes: a tool for the in vitro study of antigen presentation. Scand. J. Immunol. 34 (1991) 585-595
47. Villiers M.B., Gabert F.M., Jacquier M.R., Villiers C.L., and Colomb M.G. Involvement of the Zn-binding region of tetanus toxin in B and T recognition. Influence of Zn fixation. Mol. Immunol. 30 (1993) 129-136
48. Villiers M.B., Villiers C.L., Jacquier-Sarlin M.R., Gabert F.M., Journet A.M., and Colomb M.G. Covalent binding of C3b to tetanus toxin: influence on uptake/internalization of antigen by antigen-specific and non-specific B cells. Immunology 89 (1996) 348-355
49. Villiers M.B., Villiers C.L., Laharie A.M., and Marche P.N. Amplification of the antibody response by C3b complexed to antigen through an ester link. J. Immunol. 162 (1999) 3647-3652
50. Villiers M.B., Marche P.N., and Villiers C.L. Improvement of long-lasting response and antibody affinity by the complexation of antigen with complement C3b. Int. Immunol. 15 (2003) 91-95
51. Villiers M.B., Perrin-Cocon L., Marche P.N., and Villiers C.L. Complement receptors and B lymphocytes. Crit. Rev. Immunol. 24 (2004) 465-478
52. Wagner C., and Hansch G.M. Receptors for complement C3 on T-lymphocytes: relics of evolution or functional molecules?. Mol. Immunol. 43 (2006) 22-30
53. Wagner C., Ochmann C., Schoels M., Giese T., Stegmaier S., Richter R., Hug F., and Hansch G.M. The complement receptor 1, CR1 (CD35), mediates inhibitory signals in human T-lymphocytes. Mol. Immunol. 43 (2006) 643-651
54. Walport M.J. Complement. Second of two parts. N. Engl. J. Med. 344 (2001) 1140-1144
55. Weiss L., Fischer E., Haeffner-Cavaillon N., Jouvin M.H., Appay M.D., Bariety J., and Kazatchkine M. The human C3b receptor (CR1). Adv. Nephrol. Necker Hosp. 18 (1989) 249-269
56. Zhou W., Patel H., Li K., Peng Q., Villiers M.B., and Sacks S.H. Macrophages from C3-deficient mice have impaired potency to stimulate alloreactive T cells. Blood 107 (2006) 2461-2469