Models of antigen receptor activation in the design of vaccines

Current Pharmaceutical Design

Volumn 15, Issue 28, 2009, Pages 3237-3248

  Molnár, Eszter ^a   Dopfer, Elaine Pashupati ^a   Deswal, Sumit ^a   Schamel, Wolfgang W A ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Autoimmunity; B cell; Clustering; Immune response; T cell; Tumor; Vaccine

Indexed keywords

B LYMPHOCYTE RECEPTOR; COMPLEMENT RECEPTOR; MONOVALENT CATION; T LYMPHOCYTE RECEPTOR; TETRAMER; VACCINE;

ANTIBODY COMBINING SITE; ANTIGEN BINDING; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; ANTIGEN RECOGNITION; ANTIGEN SPECIFICITY; ANTINEOPLASTIC ACTIVITY; AUTOIMMUNE DISEASE; AUTOIMMUNITY; B LYMPHOCYTE ACTIVATION; CANCER IMMUNOTHERAPY; CONFORMATIONAL TRANSITION; CROSS LINKING; DRUG DESIGN; DRUG RECEPTOR BINDING; DRUG TARGETING; HUMAN; IMMUNOGENICITY; IMMUNOLOGICAL TOLERANCE; IMMUNOMODULATION; INFECTION PREVENTION; MAJOR HISTOCOMPATIBILITY COMPLEX; OPSONIZATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; REVIEW; T LYMPHOCYTE ACTIVATION; VACCINE PRODUCTION;

ANIMALS; AUTOIMMUNITY; B-LYMPHOCYTES; DRUG DESIGN; HUMANS; MODELS, MOLECULAR; MOLECULAR CONFORMATION; RECEPTORS, ANTIGEN; T-LYMPHOCYTES; VACCINES;

EID: 70449389518     PISSN: 13816128     EISSN: None     Source Type: Journal    
DOI: 10.2174/138161209789105216     Document Type: Review

References (131)

1. Sigalov AB. Multichain immune recognition receptor signaling: different players, same game? Trends Immunol 2004; 25: 583-589
2. Reth M, Hombach J, Wienands J, Campbell KS, Chien N, Justement LB, et al. The B-cell antigen receptor complex. Immunol Today 1991; 12: 196-201.
3. Schamel WW, Risueno RM, Minguet S, Ortiz AR, Alarcon B. A conformation- and avidity-based proofreading mechanism for the TCR-CD3 complex. Trends Immunol 2006; 27: 176-182
4. Malissen B. An evolutionary and structural perspective on T cell antigen receptor function. Immunol Rev 2003; 191: 7-27. (Pubitemid 36398845)
5. Reth M. Antigen receptor tail clue. Nature 1989; 338: 383-384
6. Iwashima M, Irving BA, van Oers NS, Chan AC, Weiss A. Sequential interactions of the TCR with two distinct cytoplasmic tyrosine kinases. Science 1994; 263: 1136-1139
7. Rolli V, Gallwitz M, Wossning T, Flemming A, Schamel WW, Zurn C, et al. Amplification of B cell antigen receptor signaling by a Syk/ITAM positive feedback loop. Mol Cell 2002; 10: 1057-1069 (Pubitemid 36001972)
8. Moran MF, Koch CA, Anderson D, Ellis C, England L, Martin GS, et al. Src homology region 2 domains direct protein-protein interactions in signal transduction. Proc Natl Acad Sci USA 1990; 87: 8622-8626 (Pubitemid 20373144)
9. Van der Merwe PA. The TCR triggering puzzle. Immunity 2001; 14: 665-668
10. Germain RN. MHC-dependent antigen processing and peptide presentation: providing ligands for T lymphocyte activation. Cell 1994; 76: 287-299 (Pubitemid 24046691)
11. Ashwell JD, Klusner RD. Genetic and mutational analysis of the Tcell antigen receptor. Annu Rev Immunol 1990; 8: 139-167 (Pubitemid 20135624)
12. Gil D, Schamel WW, Montoya M, Sanchez-Madrid F, Alarcon B. Recruitment of Nck by CD3 epsilon reveals a ligand-induced conformational change essential for T cell receptor signaling and synapse formation. Cell 2002; 109: 901-912 (Pubitemid 34786004)
13. Brezski RJ, Monroe JG. B-cell receptor. Adv Exp Med Biol 2008; 640: 12-21.
14. Klaus SJ, Berberich I, Shu G, Clark EA. CD40 and its ligand in the regulation of humoral immunity. Semin Immunol 1994; 6: 279-286 (Pubitemid 124001525)
15. Vos Q, Lees A, Wu ZQ, Snapper CM, Mond JJ. B-cell activation by T-cell-independent type 2 antigens as an integral part of the humoral immune response to pathogenic microorganisms. Immunol Rev 2000; 176: 154-170 (Pubitemid 30703327)
16. Swamy M, Minguet S, Siegers GM, Alarcon B, Schamel WW. A native antibody-based mobility-shift technique (NAMOS-assay) to determine the stoichiometry of multiprotein complexes. J Immunol Methods 2007; 324: 74-83. (Pubitemid 47001428)
17. Call ME, Pyrdol J, Wiedmann M, Wucherpfennig KW. The organizing principle in the formation of the T cell receptor-CD3 complex. Cell 2002; 111: 967-979 (Pubitemid 36044689)
18. Dopfer EP, Swamy M, Siegers GM, Molnar E, Yang J, Schamel WW. Segregation models. Adv Exp Med Biol 2008; 640: 74-81.
19. Dintzis HM, Dintzis RZ, Vogelstein B. Molecular determinants of immunogenicity: the immunon model of immune response. Proc Natl Acad Sci USA 1976; 73: 3671-3675
20. Bachmann MF, Rohrer UH, Kundig TM, Burki K, Hengartner H, Zinkernagel RM. The influence of antigen organization on B cell responsiveness. Science 1993; 262: 1448-1451 (Pubitemid 24035067)
21. Puffer EB, Pontrello JK, Hollenbeck JJ, Kink JA, Kiessling LL. Activating B cell signaling with defined multivalent ligands. ACS Chem Biol 2007; 2: 252-262
22. Minguet S, Dopfer EP, Pollmer C, Freudenberg MA, Galanos C, Reth M, et al. Enhanced B-cell activation mediated by TLR4 and BCR crosstalk. Eur J Immunol 2008; 38: 2475-2487
23. Kim YM, Pan JY, Korbel GA, Peperzak V, Boes M, Ploegh HL. Monovalent ligation of the B cell receptor induces receptor activation but fails to promote antigen presentation. Proc Natl Acad Sci USA 2006; 103: 3327-3332 (Pubitemid 43346469)
24. Chang TW, Kung PC, Gingras SP, Goldstein G. Does OKT3 monoclonal antibody react with an antigen-recognition structure on human T cells? Proc Natl Acad Sci USA 1981; 78: 1805-1808
25. Kaye J, Janeway CA, Jr. The alpha- and beta-subunits of a murine T cell antigen/Ia receptor have a molecular weight of 31,000 in the absence of N-linked glycosylation. J Immunol 1984; 133: 2291-2293 (Pubitemid 15205802)
26. Boniface JJ, Rabinowitz JD, Wulfing C, Hampl J, Reich Z, Altman JD, et al. Initiation of signal transduction through the T cell receptor requires the multivalent engagement of peptide/MHC ligands [corrected]. Immunity 1998; 9: 459-466 (Pubitemid 28499197)
27. Cochran JR, Cameron TO, Stern LJ. The relationship of MHC peptide binding and T cell activation probed using chemically defined MHC class II oligomers. Immunity 2000; 12: 241-250
28. Irvine DJ, Purbhoo MA, Krogsgaard M, Davis MM. Direct observation of ligand recognition by T cells. Nature 2002; 419: 845-849 (Pubitemid 35238571)
29. Krishna S, Benaroch P, Pillai S. Tetrameric cell-surface MHC class I molecules. Nature 1992; 357: 164-167
30. Schafer PH, Pierce SK, Jardetzky TS. The structure of MHC class II: a role for dimer of dimers. Semin Immunol 1995; 7: 389-398
31. Schamel WW, Reth M. Monomeric and oligomeric complexes of the B cell antigen receptor. Immunity 2000; 13: 5-14. (Pubitemid 30953947)
32. Fernandez-Miguel G, Alarcon B, Iglesias A, Bluethmann H, Alvarez-Mon M, Sanz E, et al. Multivalent structure of an alphabeta T cell receptor. Proc Natl Acad Sci USA 1999; 96: 1547-1552 (Pubitemid 129656235)
33. Alarcon B, Swamy M, van Santen HM, Schamel WW. T-cell antigen-receptor stoichiometry: pre-clustering for sensitivity. EMBO Rep 2006; 7: 490-495 (Pubitemid 43904864)
34. Schamel WW, Arechaga I, Risueno RM, van Santen HM, Cabezas P, Risco C, et al. Coexistence of multivalent and monovalent TCRs explains high sensitivity and wide range of response. J Exp Med 2005; 202: 493-503. (Pubitemid 41186948)
35. Daeron M, Malbec O, Latour S, Espinosa E, Pina P, Fridman WH. Regulation of tyrosine-containing activation motif-dependent cell signalling by Fc gamma RII. Immunol Lett 1995; 44: 119-123
36. Jozsi M, Prechl J, Bajtay Z, Erdei A. Complement receptor type 1 (CD35) mediates inhibitory signals in human B lymphocytes. J Immunol 2002; 168: 2782-2788 (Pubitemid 34213256)
37. Li YY, Baccam M, Waters SB, Pessin JE, Bishop GA, Koretzky GA. CD40 ligation results in protein kinase C-independent activation of ERK and JNK in resting murine splenic B cells. J Immunol 1996; 157: 1440-1447 (Pubitemid 126449081)
38. Yanagi S, Sugawara H, Kurosaki M, Sabe H, Yamamura H, Kurosaki T. CD45 modulates phosphorylation of both autophosphorylation and negative regulatory tyrosines of Lyn in B cells. J Biol Chem 1996; 271: 30487-30492 (Pubitemid 26404055)
39. Eckl-Dorna J, Batista FD. BCR-mediated uptake of antigen linked to TLR9-ligand stimulates B-cell proliferation and antigen-specific plasma cell formation. Blood 2009.
40. Kiener PA, Mittler RS. CD45-protein tyrosine phosphatase crosslinking inhibits T cell receptor CD3-mediated activation in human T cells. J Immunol 1989; 143: 23-28
41. Turka LA, Ledbetter JA, Lee K, June CH, Thompson CB. CD28 is an inducible T cell surface antigen that transduces a proliferative signal in CD3+ mature thymocytes. J Immunol 1990; 144: 1646-1653 (Pubitemid 20093992)
42. Krummel MF, Sullivan TJ, Allison JP. Superantigen responses and co-stimulation: CD28 and CTLA-4 have opposing effects on T cell expansion in vitro and in vivo. Int Immunol 1996; 8: 519-523
43. Carter RH, Spycher MO, Ng YC, Hoffman R, Fearon DT. Synergistic interaction between complement receptor type 2 and membrane IgM on B lymphocytes. J Immunol 1988; 141: 457-463 (Pubitemid 18210244)
44. Tsokos GC, Lambris JD, Finkelman FD, Anastassiou ED, June CH. Monovalent ligands of complement receptor 2 inhibit whereas polyvalent ligands enhance anti-Ig-induced human B cell intracytoplasmic free calcium concentration. J Immunol 1990; 144: 1640-1645
45. Lee Y, Haas KM, Gor DO, Ding X, Karp DR, Greenspan NS, et al. Complement component C3d-antigen complexes can either augment or inhibit B lymphocyte activation and humoral immunity in mice depending on the degree of CD21/CD19 complex engagement. J Immunol 2005; 175: 8011-8023 (Pubitemid 41798363)
46. Lyubchenko T, dal Porto J, Cambier JC, Holers VM. Coligation of the B cell receptor with complement receptor type 2 (CR2/CD21) using its natural ligand C3dg: activation without engagement of an inhibitory signaling pathway. J Immunol 2005; 174: 3264-3272 (Pubitemid 40354029)
47. Cherukuri A, Cheng PC, Pierce SK. The role of the CD19/CD21 complex in B cell processing and presentation of complementtagged antigens. J Immunol 2001; 167: 163-172 (Pubitemid 32567774)
48. Sohn HW, Tolar P, Jin T, Pierce SK. Fluorescence resonance energy transfer in living cells reveals dynamic membrane changes in the initiation of B cell signaling. Proc Natl Acad Sci USA 2006; 103: 8143-8148 (Pubitemid 43801066)
49. Fingeroth JD, Heath ME, Ambrosino DM. Proliferation of resting B cells is modulated by CR2 and CR1. Immunol Lett 1989; 21: 291-301.
50. Hippen KL, Buhl AM, D'Ambrosio D, Nakamura K, Persin C, Cambier JC. Fc gammaRIIB1 inhibition of BCR-mediated phosphoinositide hydrolysis and Ca2+ mobilization is integrated by CD19 dephosphorylation. Immunity 1997; 7: 49-58. (Pubitemid 27357264)
51. Poe JC, Hasegawa M, Tedder TF. CD19, CD21, and CD22: multifaceted response regulators of B lymphocyte signal transduction. Int Rev Immunol 2001; 20: 739-762
52. Pasare C, Medzhitov R. Control of B-cell responses by Toll-like receptors. Nature 2005; 438: 364-368 (Pubitemid 41643953)
53. Wang JH, Meijers R, Xiong Y, Liu JH, Sakihama T, Zhang R, et al. Crystal structure of the human CD4 N-terminal two-domain fragment complexed to a class II MHC molecule. Proc Natl Acad Sci USA 2001; 98: 10799-10804 (Pubitemid 32878700)
54. Garboczi DN, Ghosh P, Utz U, Fan QR, Biddison WE, Wiley DC. Structure of the complex between human T-cell receptor, viral peptide and HLA-A2. Nature 1996; 384: 134-141 (Pubitemid 26386462)
55. Garcia KC, Degano M, Stanfield RL, Brunmark A, Jackson MR, Peterson PA, et al. An alphabeta T cell receptor structure at 2.5 A and its orientation in the TCR-MHC complex. Science 1996; 274: 209-219 (Pubitemid 26353190)
56. Kim PW, Sun ZY, Blacklow SC, Wagner G, Eck MJ. A zinc clasp structure tethers Lck to T cell coreceptors CD4 and CD8. Science 2003; 301: 1725-1728 (Pubitemid 37174366)
57. Madrenas J, Chau LA, Smith J, Bluestone JA, Germain RN. The efficiency of CD4 recruitment to ligand-engaged TCR controls the agonist/partial agonist properties of peptide-MHC molecule ligands. J Exp Med 1997; 185: 219-229 (Pubitemid 27078279)
58. Suzuki S, Kupsch J, Eichmann K, Saizawa MK. Biochemical evidence of the physical association of the majority of CD3 delta chains with the accessory/co-receptor molecules CD4 and CD8 on nonactivated T lymphocytes. Eur J Immunol 1992; 22: 2475-2479
59. Risueno RM, Gil D, Fernandez E, Sanchez-Madrid F, Alarcon B. Ligand-induced conformational change in the T-cell receptor associated with productive immune synapses. Blood 2005; 106:601-608 (Pubitemid 40981257)
60. Gil D, Schrum AG, Alarcon B, Palmer E. T cell receptor engagement by peptide-MHC ligands induces a conformational change in the CD3 complex of thymocytes. J Exp Med 2005; 201: 517-522 (Pubitemid 40289542)
61. Risueno RM, Schamel WW, Alarcon B. T cell receptor engagement triggers its CD3epsilon and CD3zeta subunits to adopt a compact, locked conformation. PLoS ONE 2008; 3: e1747. (Pubitemid 351903214)
62. Minguet S, Swamy M, Alarcon B, Luescher IF, Schamel WW. Full activation of the T cell receptor requires both clustering and conformational changes at CD3. Immunity 2007; 26: 43-54. (Pubitemid 46109342)
63. Reth M, Wienands J, Schamel WW. An unsolved problem of the clonal selection theory and the model of an oligomeric B-cell antigen receptor. Immunol Rev 2000; 176: 10-18 (Pubitemid 30703316)
64. Reth M. Oligomeric antigen receptors: a new view on signaling for the selection of lymphocytes. Trends Immunol 2001; 22: 356-360 (Pubitemid 32673640)
65. Sigalov AB. Signaling chain homooligomerization (SCHOOL) model. Adv Exp Med Biol 2008; 640: 121-163
66. McKeithan TW. Kinetic proofreading in T-cell receptor signal transduction. Proc Natl Acad Sci USA 1995; 92: 5042-5046
67. Valitutti S, Muller S, Cella M, Padovan E, Lanzavecchia A. Serial triggering of many T-cell receptors by a few peptide-MHC complexes. Nature 1995; 375: 148-151
68. Kalergis AM, Boucheron N, Doucey MA, Palmieri E, Goyarts EC, Vegh Z, et al. Efficient T cell activation requires an optimal dwelltime of interaction between the TCR and the pMHC complex. Nat Immunol 2001; 2: 229-234 (Pubitemid 33705999)
69. Blander JM, Medzhitov R. Toll-dependent selection of microbial antigens for presentation by dendritic cells. Nature 2006; 440: 808-812
70. Carroll MC. The role of complement in B cell activation and tolerance. Adv Immunol 2000; 74: 61-88.
71. O'Hagan DT, Valiante NM. Recent advances in the discovery and delivery of vaccine adjuvants. Nat Rev Drug Discov 2003; 2: 727-735 (Pubitemid 37361788)
72. Cella M, Sallusto F, Lanzavecchia A. Origin, maturation and antigen presenting function of dendritic cells. Curr Opin Immunol 1997; 9: 10-16 (Pubitemid 27095893)
73. Benko S, Magyarics Z, Szabo A, Rajnavolgyi E. Dendritic cell subtypes as primary targets of vaccines: the emerging role and cross-talk of pattern recognition receptors. Biol Chem 2008; 389: 469-485 (Pubitemid 351874188)
74. Proudfoot O, Apostolopoulos V, Pietersz GA. Receptor-mediated delivery of antigens to dendritic cells: anticancer applications. Mol Pharm 2007; 4: 58-72. (Pubitemid 46302129)
75. Jiang W, Lederman MM, Harding CV, Rodriguez B, Mohner RJ, Sieg SF. TLR9 stimulation drives naive B cells to proliferate and to attain enhanced antigen presenting function. Eur J Immunol 2007; 37: 2205-2213 (Pubitemid 47250213)
76. Ferguson AR, Youd ME, Corley RB. Marginal zone B cells transport and deposit IgM-containing immune complexes onto follicular dendritic cells. Int Immunol 2004; 16: 1411-1422
77. Egan MA, Chong SY, Hagen M, Megati S, Schadeck EB, Piacente P, et al. A comparative evaluation of nasal and parenteral vaccine adjuvants to elicit systemic and mucosal HIV-1 peptide-specific humoral immune responses in cynomolgus macaques. Vaccine 2004; 22: 3774-3788 (Pubitemid 39099655)
78. Huleatt JW, Nakaar V, Desai P, Huang Y, Hewitt D, Jacobs A, et al. Potent immunogenicity and efficacy of a universal influenza vaccine candidate comprising a recombinant fusion protein linking influenza M2e to the TLR5 ligand flagellin. Vaccine 2008; 26:201-214 (Pubitemid 50008089)
79. Dempsey PW, Allison ME, Akkaraju S, Goodnow CC, Fearon DT. C3d of complement as a molecular adjuvant: bridging innate and acquired immunity. Science 1996; 271: 348-350 (Pubitemid 3021509)
80. Baiu DC, Prechl J, Tchorbanov A, Molina HD, Erdei A, Sulica A, et al. Modulation of the humoral immune response by antibodymediated antigen targeting to complement receptors and Fc receptors. J Immunol 1999; 162: 3125-3130 (Pubitemid 29313556)
81. Mahat RI, Monera OD, Smith LC, Rolland A. Peptide-based gene delivery. Curr Opin Mol Ther 1999; 1: 226-243
82. Ma H, Diamond SL. Nonviral gene therapy and its delivery systems. Curr Pharm Biotechnol 2001; 2: 1-17. (Pubitemid 32416443)
83. Basarkar A, Singh J. Nanoparticulate systems for polynucleotide delivery. Int J Nanomedicine 2007; 2: 353-360
84. Karmali PP, Chaudhuri A. Cationic liposomes as non-viral carriers of gene medicines: resolved issues, open questions, and future promises. Med Res Rev 2007; 27: 696-722. (Pubitemid 47282449)
85. Tang CK, Sheng KC, Esparon SE, Proudfoot O, Apostolopoulos V, Pietersz GA. Molecular basis of improved immunogenicity in DNA vaccination mediated by a mannan based carrier. Biomaterials 2008.
86. Burgdorf S, Kautz A, Bohnert V, Knolle PA, Kurts C. Distinct pathways of antigen uptake and intracellular routing in CD4 and CD8 T cell activation. Science 2007; 316: 612-616 (Pubitemid 46683149)
87. He LZ, Crocker A, Lee J, Mendoza-Ramirez J, Wang XT, Vitale LA, et al. Antigenic targeting of the human mannose receptor induces tumor immunity. J Immunol 2007; 178: 6259-6267 (Pubitemid 46717409)
88. Espuelas S, Thumann C, Heurtault B, Schuber F, Frisch B. Influence of ligand valency on the targeting of immature human dendritic cells by mannosylated liposomes. Bioconjug Chem 2008; 19(12): 2385-2393
89. Chua BY, Eriksson EM, Brown LE, Zeng W, Gowans EJ, Torresi J, et al. A self-adjuvanting lipopeptide-based vaccine candidate for the treatment of hepatitis C virus infection. Vaccine 2008; 26: 4866-4875
90. Villiers MB, Marche PN, Villiers CL. Improvement of long-lasting response and antibody affinity by the complexation of antigen with complement C3b. Int Immunol 2003; 15: 91-95
91. Manca F. Galactose receptors and presentation of HIV envelope glycoprotein to specific human T cells. J Immunol 1992; 148: 2278-2282
92. LaTemple DC, Abrams JT, Zhang SY, Galili U. Increased immunogenicity of tumor vaccines complexed with anti-Gal: studies in knockout mice for alpha1,3galactosyltransferase. Cancer Res 1999; 59: 3417-3423 (Pubitemid 29334502)
93. Abdel-Motal UM, Guay HM, Wigglesworth K, Welsh RM, Galili U. Immunogenicity of influenza virus vaccine is increased by antigal- mediated targeting to antigen-presenting cells. J Virol 2007; 81: 9131-9141 (Pubitemid 47311456)
94. Casten LA, Kaumaya P, Pierce SK. Enhanced T cell responses to antigenic peptides targeted to B cell surface Ig, Ia, or class I molecules. J Exp Med 1988; 168: 171-180 (Pubitemid 18195142)
95. Carayanniotis G, Skea DL, Luscher MA, Barber BH. Adjuvantindependent immunization by immunotargeting antigens to MHC and non-MHC determinants in vivo. Mol Immunol 1991; 28: 261-267
96. Whipple EC, Shanahan RS, Ditto AH, Taylor RP, Lindorfer MA. Analyses of the in vivo trafficking of stoichiometric doses of an anti-complement receptor 1/2 monoclonal antibody infused intravenously in mice. J Immunol 2004; 173: 2297-2306
97. Fearon DT, Carter RH. The CD19/CR2/TAPA-1 complex of B lymphocytes: linking natural to acquired immunity. Annu Rev Immunol 1995; 13: 127-149
98. Molina H, Holers VM, Li B, Fung Y, Mariathasan S, Goellner J, et al. Markedly impaired humoral immune response in mice deficient in complement receptors 1 and 2. Proc Natl Acad Sci USA 1996; 93: 3357-3361 (Pubitemid 26125624)
99. Ahearn JM, Fischer MB, Croix D, Goerg S, Ma M, Xia J, 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. Immunity 1996; 4: 251-262 (Pubitemid 26131008)
100. Wu X, Jiang N, Fang YF, Xu C, Mao D, Singh J, et al. Impaired affinity maturation in Cr2-/- mice is rescued by adjuvants without improvement in germinal center development. J Immunol 2000; 165: 3119-3127 (Pubitemid 30728164)
101. Barrington RA, Zhang M, Zhong X, Jonsson H, Holodick N, Cherukuri A, et al. CD21/CD19 coreceptor signaling promotes B cell survival during primary immune responses. J Immunol 2005; 175: 2859-2867 (Pubitemid 41170503)
102. Molnar E, Erdei A, Prechl J. Novel roles for murine complement receptors type 1 and 2 I. Regulation of B cell survival and proliferation by CR1/2. Immunol Lett 2008; 116: 156-162
103. Villiers MB, Villiers CL, Laharie AM, Marche PN. Amplification of the antibody response by C3b complexed to antigen through an ester link. J Immunol 1999; 162: 3647-3652
104. Pozdnyakova O, Guttormsen HK, Lalani FN, Carroll MC, Kasper DL. Impaired antibody response to group B streptococcal type III capsular polysaccharide in C3- and complement receptor 2-deficient mice. J Immunol 2003; 170: 84-90. (Pubitemid 36026126)
105. Fernandez C, Moller G. Immune response against two epitopes on the same thymus-independent polysaccharide carrier. 1. Role of epitope density in carrier-dependent immunity and tolerance. Immunology 1977; 33: 59-68.
106. Jennings GT, Bachmann MF. The coming of age of virus-like particle vaccines. Biol Chem 2008; 389: 521-536
107. Anolik JH, Barnard J, Cappione A, Pugh-Bernard AE, Felgar RE, Looney RJ, et al. Rituximab improves peripheral B cell abnormalities in human systemic lupus erythematosus. Arthritis Rheum 2004; 50: 3580-3590 (Pubitemid 39488683)
108. Dorner T, Kaufmann J, Wegener WA, Teoh N, Goldenberg DM, Burmester GR. Initial clinical trial of epratuzumab (humanized anti-CD22 antibody) for immunotherapy of systemic lupus erythematosus. Arthritis Res Ther 2006; 8: R74.
109. Caramaschi P, Biasi D, Colombatti M, Pieropan S, Martinelli N, Carletto A, et al. Anti-TNFalpha therapy in rheumatoid arthritis and autoimmunity. Rheumatol Int 2006; 26: 209-214 (Pubitemid 41830977)
110. Atzeni F, Turiel M, Capsoni F, Doria A, Meroni P, Sarzi-Puttini P. Autoimmunity and anti-TNF-alpha agents. Ann N Y Acad Sci 2005; 1051: 559-569
111. Prodeus AP, Goerg S, Shen LM, Pozdnyakova OO, Chu L, Alicot EM, et al. A critical role for complement in maintenance of selftolerance. Immunity 1998; 9: 721-731 (Pubitemid 28557600)
112. Prechl J, Molnar E, Szekeres Z, Isaak A, Papp K, Balogh P, et al. Murine CR1/2 targeted antigenized single-chain antibody fragments induce transient low affinity antibodies and negatively influence an ongoing immune response. Adv Exp Med Biol 2007; 598: 214-225
113. Reichardt P, Dornbach B, Rong S, Beissert S, Gueler F, Loser K, et al. Naive B cells generate regulatory T cells in the presence of a mature immunologic synapse. Blood 2007; 110: 1519-1529 (Pubitemid 47443968)
114. Voynova E, Tchorbanov A, Prechl J, Nikolova M, Baleva M, Erdei A, et al. An antibody-based construct carrying DNA-mimotope and targeting CR1(CD35) selectively suppresses human autoreactive Blymphocytes. Immunol Lett 2008; 116: 168-173
115. Angyal A, Prechl J, Sarmay G. Possible therapeutic applications of single-chain antibodies in systemic autoimmune diseases. Expert Opin Biol Ther 2007; 7: 691-704. (Pubitemid 46707191)
116. Nakamura A, Kubo T, Takai T. Fc receptor targeting in the treatment of allergy, autoimmune diseases and cancer. Adv Exp Med Biol 2008; 640: 220-233
117. Segal DM, Weiner GJ, Weiner LM. Bispecific antibodies in cancer therapy. Curr Opin Immunol 1999; 11: 558-562
118. Muller D, Kontermann RE. Recombinant bispecific antibodies for cellular cancer immunotherapy. Curr Opin Mol Ther 2007; 9: 319-326 (Pubitemid 47255664)
119. Kipriyanov SM, Moldenhauer G, Strauss G, Little M. Bispecific CD3 x CD19 diabody for T cell-mediated lysis of malignant human B cells. Int J Cancer 1998; 77: 763-772 (Pubitemid 28341395)
120. Cochlovius B, Kipriyanov SM, Stassar MJ, Schuhmacher J, Benner A, Moldenhauer G, et al. Cure of Burkitt's lymphoma in severe combined immunodeficiency mice by T cells, tetravalent CD3 x CD19 tandem diabody, and CD28 costimulation. Cancer Res 2000; 60: 4336-4341 (Pubitemid 32103606)
121. Asano R, Sone Y, Makabe K, Tsumoto K, Hayashi H, Katayose Y, et al. Humanization of the bispecific epidermal growth factor receptor x CD3 diabody and its efficacy as a potential clinical reagent. Clin Cancer Res 2006; 12: 4036-4042 (Pubitemid 44078091)
122. Gao Y, Xiong D, Yang M, Liu H, Peng H, Shao X, et al. Efficient inhibition of multidrug-resistant human tumors with a recombinant bispecific anti-P-glycoprotein x anti-CD3 diabody. Leukemia 2004; 18: 513-520 (Pubitemid 38425866)
123. Takemura S, Kudo T, Asano R, Suzuki M, Tsumoto K, Sakurai N, et al. A mutated superantigen SEA D227A fusion diabody specific to MUC1 and CD3 in targeted cancer immunotherapy for bile duct carcinoma. Cancer Immunol Immunother 2002; 51: 33-44. (Pubitemid 34158521)
124. Buhler P, Wolf P, Gierschner D, Schaber I, Katzenwadel A, Schultze-Seemann W, et al. A bispecific diabody directed against prostate-specific membrane antigen and CD3 induces T-cell mediated lysis of prostate cancer cells. Cancer Immunol Immunother 2008; 57: 43-52. (Pubitemid 350043647)
125. Schraven B, Kalinke U. CD28 superagonists: what makes the difference in humans? Immunity 2008; 28: 591-595
126. Reusch U, Le Gall F, Hensel M, Moldenhauer G, Ho AD, Little M, et al. Effect of tetravalent bispecific CD19xCD3 recombinant antibody construct and CD28 costimulation on lysis of malignant B cells from patients with chronic lymphocytic leukemia by autologous T cells. Int J Cancer 2004; 112: 509-518 (Pubitemid 39390618)
127. Sakita I, Horig H, Sun R, Wang F, Nathenson SG. In vivo CTL immunity can be elicited by in vitro reconstituted MHC/peptide complex. J Immunol Methods 1996; 192: 105-115
128. Maile R, Wang B, Schooler W, Meyer A, Collins EJ, Frelinger JA. Antigen-specific modulation of an immune response by in vivo administration of soluble MHC class I tetramers. J Immunol 2001; 167: 3708-3714
129. Lomax AR, Calder PC. Probiotics, immune function, infection and inflammation: a review of the evidence from studies conducted in humans. Curr Pharm Des 2009; 15(13): 1428-1518
130. Magrone T, Tafaro A, Jirillo F, Amati L, Jirillo E, Covelli V. Elicitation of immune responsiveness against antigenic challenge in age-related diseases: effects of red wine polyphenols. Curr Pharm Des 2008; 14(26): 2749-2757
131. Rovere-Querini P, Brunelli S, Clementi E, Manfredi AA. Cell death: tipping the balance of autoimmunity and tissue repair. Curr Pharm Des 2008; 14(3): 269-277