Complement activation and complement receptors on follicular dendritic cells are critical for the function of a targeted adjuvant

Journal of Immunology

Volumn 187, Issue 7, 2011, Pages 3641-3652

  Mattsson, Johan ^a   Yrlid, Ulf ^a   Stensson, Anneli ^a   Schön, Karin ^a   Karlsson, Mikael C I ^b   Ravetch, Jeffrey V ^c   Lycke, Nils Y ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b KAROLINSKA INSTITUTE   (Sweden)

^c ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 HYDROXY 3 NITROPHENYLACETYLHAPTEN CHICKEN GAMMA GLOBULIN CONJUGATE; 4 HYDROXY 3 NITROPHENYLACETYLHAPTEN DEXTRAN CONJUGATE; 4 HYDROXY 3 NITROPHENYLACETYLHAPTEN FICOLL CONJUGATE; ANTIGEN; CHOLERA TOXIN A1 SUBUNIT D DIMER FUSION PROTEIN; CHOLERA TOXIN A1 SUBUNIT OVALBUMIN D DIMER FUSION PROTEIN; CHOLERA TOXIN A1R7K SUBUNIT D DIMER FUSION PROTEIN; COMPLEMENT RECEPTOR; IMMUNOLOGICAL ADJUVANT; RIBI; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; CD4+ T LYMPHOCYTE; COMPLEMENT ACTIVATION; CONTROLLED STUDY; DOSE RESPONSE; DRUG BINDING; DRUG MECHANISM; FOLLICULAR DENDRITIC CELL; GERMINAL CENTER; IMMUNE RESPONSE; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; CELL SEPARATION; CHOLERA TOXIN; COMPLEMENT ACTIVATION; DENDRITIC CELLS, FOLLICULAR; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GERMINAL CENTER; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTORS, COMPLEMENT; RECEPTORS, COMPLEMENT 3D; RECOMBINANT FUSION PROTEINS;

EID: 80053536456     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1101107     Document Type: Article

References (78)

1. O'Hagan, D. T., M. L. MacKichan, and M. Singh. 2001. Recent developments in adjuvants for vaccines against infectious diseases. Biomol. Eng. 18: 69-85. (Pubitemid 32889607)
2. Kool, M., T. Soullié, M. Van Nimwegen, M. A. Willart, F. Muskens, S. Jung, H. C. Hoogsteden, H. Hammad, and B. N. Lambrecht. 2008. Alum adjuvant boosts adaptive immunity by inducing uric acid and activating inflammatory dendritic cells. J. Exp. Med. 205: 869-882. (Pubitemid 351549884)
3. Lambrecht, B. N., M. Kool, M. A. Willart, and H. Hammad. 2009. Mechanism of action of clinically approved adjuvants. Curr. Opin. Immunol. 21: 23-29.
4. Higgins, S. C., and K. H. Mills. 2010. TLR, NLR Agonists, and Other Immune Modulators as Infectious Disease Vaccine Adjuvants. Curr. Infect. Dis. Rep. 12: 4-12.
5. De Gregorio, E., U. D'Oro, and A. Wack. 2009. Immunology of TLR-independent vaccine adjuvants. Curr. Opin. Immunol. 21: 339-345.
6. Pulendran, B., and R. Ahmed. 2006. Translating innate immunity into immunological memory: implications for vaccine development. Cell 124: 849-863. (Pubitemid 43261457)
7. Nest, G. O. G. v. 2007. Development of Vaccine Adjuvants: A Historical Perspective. In Vaccine adjuvants and delivery systems. M. Singh, ed. John Wiley &Sons, Hoboken, NJ, p. 1-32.
8. Fujihashi, K., T. Koga, F. W. Van Ginkel, Y. Hagiwara, and J. R. McGhee. 2002. A dilemma for mucosal vaccination: efficacy versus toxicity using enterotoxin-based adjuvants. Vaccine 20: 2431-2438. (Pubitemid 34615580)
9. Marciani, D. J. 2003. Vaccine adjuvants: role and mechanisms of action in vaccine immunogenicity. Drug Discov. Today 8: 934-943. (Pubitemid 37230013)
10. Ulmer, J. B., U. Valley, and R. Rappuoli. 2006. Vaccine manufacturing: challenges and solutions. Nat. Biotechnol. 24: 1377-1383. (Pubitemid 44722101)
11. Bendelac, A., and R. Medzhitov. 2002. Adjuvants of immunity: harnessing innate immunity to promote adaptive immunity. J. Exp. Med. 195: F19-F23. (Pubitemid 34461498)
12. Agren, L. C., L. Ekman, B. Löwenadler, and N. Y. Lycke. 1997. Genetically engineered nontoxic vaccine adjuvant that combines B cell targeting with immunomodulation by cholera toxin A1 subunit. J. Immunol. 158: 3936-3946. (Pubitemid 127488754)
13. Sundling, C., K. Schön, A. Mörner, M. N. Forsell, R. T. Wyatt, R. Thorstensson, G. B. Karlsson Hedestam, and N. Y. Lycke. 2008. CTA1-DD adjuvant promotes strong immunity against human immunodeficiency virus type 1 envelope glycoproteins following mucosal immunization. J. Gen. Virol. 89: 2954-2964.
14. Eriksson, A. M., K. M. Schön, and N. Y. Lycke. 2004. The cholera toxin-derived CTA1-DD vaccine adjuvant administered intranasally does not cause inflammation or accumulate in the nervous tissues. J. Immunol. 173: 3310-3319. (Pubitemid 39142040)
15. Eriksson, A., and N. Lycke. 2003. The CTA1-DD vaccine adjuvant binds to human B cells and potentiates their T cell stimulating ability. Vaccine 22: 185-193. (Pubitemid 37419992)
16. Eliasson, D. G., K. El Bakkouri, K. Schön, A. Ramne, E. Festjens, B. Löwenadler, W. Fiers, X. Saelens, and N. Lycke. 2008. CTA1-M2e-DD: a novel mucosal adjuvant targeted influenza vaccine. Vaccine 26: 1243-1252.
17. Agren, L., E. Sverremark, L. Ekman, K. Schön, B. Löwenadler, C. Fernandez, and N. Lycke. 2000. The ADP-ribosylating CTA1-DD adjuvant enhances T cell-dependent and independent responses by direct action on B cells involving antiapoptotic Bcl-2- and germinal center-promoting effects. J. Immunol. 164: 6276-6286. (Pubitemid 30408808)
18. Berek, C., A. Berger, and M. Apel. 1991. Maturation of the immune response in germinal centers. Cell 67: 1121-1129. (Pubitemid 121001525)
19. Bemark, M., P. Bergqvist, A. Stensson, A. Holmberg, J. Mattsson, and N. Y. Lycke. 2011. A unique role of the cholera toxin A1-DD adjuvant for long-term plasma and memory B cell development. J. Immunol. 186: 1399-1410.
20. Lycke, N., and M. Bemark. 2010. Mucosal adjuvants and long-term memory development with special focus on CTA1-DD and other ADP-ribosylating toxins. Mucosal Immunol. 3: 556-566.
21. Yoshida, K., T. K. Van den Berg, and C. D. Dijkstra. 1993. Two different mechanisms of immune-complex trapping in the mouse spleen during immune responses. Adv. Exp. Med. Biol. 329: 377-382. (Pubitemid 23199654)
22. Tew, J. G., and T. E. Mandel. 1979. Prolonged antigen half-life in the lymphoid follicles of specifically immunized mice. Immunology 37: 69-76. (Pubitemid 9249289)
23. Aydar, Y., S. Sukumar, A. K. Szakal, and J. G. Tew. 2005. The influence of immune complex-bearing follicular dendritic cells on the IgM response, Ig class switching, and production of high affinity IgG. J. Immunol. 174: 5358-5366. (Pubitemid 40593174)
24. Brockman, M. A., A. Verschoor, J. Zhu, M. C. Carroll, and D. M. Knipe. 2006. Optimal long-term humoral responses to replication-defective herpes simplex virus require CD21/CD35 complement receptor expression on stromal cells. J. Virol. 80: 7111-7117. (Pubitemid 44025207)
25. Kosco-Vilbois, M. H. 2003. Are follicular dendritic cells really good for nothing? Nat. Rev. Immunol. 3: 764-769. (Pubitemid 41070817)
26. Allen, C. D., and J. G. Cyster. 2008. Follicular dendritic cell networks of primary follicles and germinal centers: phenotype and function. Semin. Immunol. 20: 14-25.
27. Nishikawa, Y., M. Hikida, M. Magari, N. Kanayama, M. Mori, H. Kitamura, T. Kurosaki, and H. Ohmori. 2006. Establishment of lymphotoxin beta receptor signaling-dependent cell lines with follicular dendritic cell phenotypes from mouse lymph nodes. J. Immunol. 177: 5204-5214. (Pubitemid 44527593)
28. Gorelik, L., K. Gilbride, M. Dobles, S. L. Kalled, D. Zandman, and M. L. Scott. 2003. Normal B cell homeostasis requires B cell activation factor production by radiation-resistant cells. J. Exp. Med. 198: 937-945. (Pubitemid 37152930)
29. Dempsey, P. W., M. E. Allison, S. Akkaraju, C. C. Goodnow, and D. T. Fearon. 1996. C3d of complement as a molecular adjuvant: bridging innate and acquired immunity. Science 271: 348-350.
30. Carroll, M. C. 2004. The complement system in regulation of adaptive immunity. Nat. Immunol. 5: 981-986. (Pubitemid 41057714)
31. Whipple, E. C., R. S. Shanahan, A. H. Ditto, R. P. Taylor, and M. A. Lindorfer. 2004. Analyses of the in vivo trafficking of stoichiometric doses of an anticomplement receptor 1/2 monoclonal antibody infused intravenously in mice. J. Immunol. 173: 2297-2306. (Pubitemid 39063085)
32. Youd, M. E., A. R. Ferguson, and R. B. Corley. 2002. Synergistic roles of IgM and complement in antigen trapping and follicular localization. Eur. J. Immunol. 32: 2328-2337. (Pubitemid 34965896)
33. Kurtz, C. B., E. O'Toole, S. M. Christensen, and J. H. Weis. 1990. 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. J. Immunol. 144: 3581-3591. (Pubitemid 20146398)
34. Dunkelberger, J. R., and W. C. Song. 2010. Complement and its role in innate and adaptive immune responses. Cell Res. 20: 34-50.
35. Cumano, A., and K. Rajewsky. 1986. Clonal recruitment and somatic mutation in the generation of immunological memory to the hapten NP. EMBO J. 5: 2459-2468.
36. Rasband, W. S. 2009. ImageJ. National Institutes of Health, Bethesda, MD. Available at: http://rsb.info.nih.gov/ij/.
37. Van Rooijen, N., and A. Sanders. 1994. Liposome mediated depletion of macrophages: mechanism of action, preparation of liposomes and applications. J. Immunol. Methods 174: 83-93.
38. Akhiani, A. A., A. Stensson, K. Schön, and N. Lycke. 2006. The nontoxic CTA1-DD adjuvant enhances protective immunity against Helicobacter pylori infection following mucosal immunization. Scand. J. Immunol. 63: 97-105.
39. Lycke, N., and K. Schön. 2001. The B cell targeted adjuvant, CTA1-DD, exhibits potent mucosal immunoenhancing activity despite pre-existing anti-toxin immunity. Vaccine 19: 2542-2548. (Pubitemid 32234270)
40. Agren, L. C., L. Ekman, B. Löwenadler, J. G. Nedrud, and N. Y. Lycke. 1999. Adjuvanticity of the cholera toxin A1-based gene fusion protein, CTA1-DD, is critically dependent on the ADP-ribosyltransferase and Ig-binding activity. J. Immunol. 162: 2432-2440. (Pubitemid 29288873)
41. Kranich, J., N. J. Krautler, E. Heinen, M. Polymenidou, C. Bridel, A. Schildknecht, C. Huber, M. H. Kosco-Vilbois, R. Zinkernagel, G. Miele, and A. Aguzzi. 2008. Follicular dendritic cells control engulfment of apoptotic bodies by secreting Mfge8. J. Exp. Med. 205: 1293-1302. (Pubitemid 351831487)
42. Fu, Y. X., G. Huang, M. Matsumoto, H. Molina, and D. D. Chaplin. 1997. Independent signals regulate development of primary and secondary follicle structure in spleen and mesenteric lymph node. Proc. Natl. Acad. Sci. USA 94: 5739-5743. (Pubitemid 27241840)
43. Roozendaal, R., T. R. Mempel, L. A. Pitcher, S. F. Gonzalez, A. Verschoor, R. E. Mebius, U. H. Von Andrian, and M. C. Carroll. 2009. Conduits mediate transport of low-molecular-weight antigen to lymph node follicles. Immunity 30: 264-276.
44. Seiler, P., P. Aichele, B. Odermatt, H. Hengartner, R. M. Zinkernagel, and R. A. Schwendener. 1997. Crucial role of marginal zone macrophages and marginal zone metallophils in the clearance of lymphocytic choriomeningitis virus infection. Eur. J. Immunol. 27: 2626-2633. (Pubitemid 27453853)
45. Karlsson, M. C., R. Guinamard, S. Bolland, M. Sankala, R. M. Steinman, and J. V. Ravetch. 2003. Macrophages control the retention and trafficking of B lymphocytes in the splenic marginal zone. J. Exp. Med. 198: 333-340. (Pubitemid 36987858)
46. Cinamon, G., M. Matloubian, M. J. Lesneski, Y. Xu, C. Low, T. Lu, R. L. Proia, and J. G. Cyster. 2004. Sphingosine 1-phosphate receptor 1 promotes B cell localization in the splenic marginal zone. Nat. Immunol. 5: 713-720. (Pubitemid 39023303)
47. Vora, K. A., E. Nichols, G. Porter, Y. Cui, C. A. Keohane, R. Hajdu, J. Hale, W. Neway, D. Zaller, and S. Mandala. 2005. Sphingosine 1-phosphate receptor agonist FTY720-phosphate causes marginal zone B cell displacement. J. Leukoc. Biol. 78: 471-480. (Pubitemid 41061319)
48. Fischer, M. B., M. Ma, S. Goerg, X. Zhou, J. Xia, O. Finco, S. Han, G. Kelsoe, R. G. Howard, T. L. Rothstein, et al. 1996. Regulation of the B cell response to T-dependent antigens by classical pathway complement. J. Immunol. 157: 549-556. (Pubitemid 26231355)
49. Evans, J. T., C. W. Cluff, D. A. Johnson, M. J. Lacy, D. H. Persing, and J. R. Baldridge. 2003. Enhancement of antigen-specific immunity via the TLR4 ligands MPL adjuvant and Ribi.529. Expert Rev. Vaccines 2: 219-229. (Pubitemid 36559927)
50. Kopf, M., B. Abel, A. Gallimore, M. Carroll, and M. F. Bachmann. 2002. Complement component C3 promotes T-cell priming and lung migration to control acute influenza virus infection. Nat. Med. 8: 373-378. (Pubitemid 34407032)
51. Zhou, W., H. Patel, K. Li, Q. Peng, M. B. Villiers, and S. H. Sacks. 2006. Macrophages from C3-deficient mice have impaired potency to stimulate alloreactive T cells. Blood 107: 2461-2469. (Pubitemid 43345568)
52. Hasselberg, A., L. Ekman, L. F. Yrlid, K. Schön, and N. Y. Lycke. 2010. ADP-ribosylation controls the outcome of tolerance or enhanced priming following mucosal immunization. J. Immunol. 184: 2776-2784.
53. Kozono, Y., R. Abe, H. Kozono, R. G. Kelly, T. Azuma, and V. M. Holers. 1998. Cross-linking CD21/CD35 or CD19 increases both B7-1 and B7-2 expression on murine splenic B cells. J. Immunol. 160: 1565-1572. (Pubitemid 28106439)
54. Mongini, P. K., and J. K. Inman. 2001. Cytokine dependency of human B cell cycle progression elicited by ligands which coengage BCR and the CD21/CD19/CD81 costimulatory complex. Cell. Immunol. 207: 127-140. (Pubitemid 32225454)
55. Aichele, P., J. Zinke, L. Grode, R. A. Schwendener, S. H. Kaufmann, and P. Seiler. 2003. Macrophages of the splenic marginal zone are essential for trapping of blood-borne particulate antigen but dispensable for induction of specific T cell responses. J. Immunol. 171: 1148-1155. (Pubitemid 36900042)
56. Koppel, E. A., M. Litjens, V. C. Van den Berg, Y. Van Kooyk, and T. B. Geijtenbeek. 2008. Interaction of SIGNR1 expressed by marginal zone macrophages with marginal zone B cells is essential to early IgM responses against Streptococcus pneumoniae. Mol. Immunol. 45: 2881-2887.
57. Kraal, G., H. Ter Hart, C. Meelhuizen, G. Venneker, and E. Claassen. 1989. Marginal zone macrophages and their role in the immune response against T-independent type 2 antigens: modulation of the cells with specific antibody. Eur. J. Immunol. 19: 675-680. (Pubitemid 19152935)
58. Claassen, E., N. Kors, and N. Van Rooijen. 1986. Influence of carriers on the development and localization of anti-2,4,6-trinitrophenyl (TNP) antibody-forming cells in the murine spleen. II. Suppressed antibody response to TNP-Ficoll after elimination of marginal zone cells. Eur. J. Immunol. 16: 492-497. (Pubitemid 16103045)
59. Oehen, S., B. Odermatt, U. Karrer, H. Hengartner, R. Zinkernagel, and C. López-Macías. 2002. Marginal zone macrophages and immune responses against viruses. J. Immunol. 169: 1453-1458. (Pubitemid 34809190)
60. Cinamon, G., M. A. Zachariah, O. M. Lam, F. W. Foss, Jr., and J. G. Cyster. 2008. Follicular shuttling of marginal zone B cells facilitates antigen transport. Nat. Immunol. 9: 54-62. (Pubitemid 350286204)
61. Swanson, C. L., T. J. Wilson, P. Strauch, M. Colonna, R. Pelanda, and R. M. Torres. 2010. Type I IFN enhances follicular B cell contribution to the T cell-independent antibody response. J. Exp. Med. 207: 1485-1500.
62. Vos, Q., A. Lees, Z. Q. Wu, C. M. Snapper, and J. J. Mond. 2000. B-cell activation by T-cell-independent type 2 antigens as an integral part of the humoral immune response to pathogenic microorganisms. Immunol. Rev. 176: 154-170.
63. Hsu, M. C., K. M. Toellner, C. G. Vinuesa, and I. C. Maclennan. 2006. B cell clones that sustain long-term plasmablast growth in T-independent extrafollicular antibody responses. Proc. Natl. Acad. Sci. USA 103: 5905-5910.
64. Mongini, P. K., D. L. Longo, and W. E. Paul. 1984. T cell regulation of immunoglobulin class expression in the B cell response to TNP-Ficoll: characterization of the T cell responsible for preferential enhancement of the IgG2a response. J. Immunol. 132: 1647-1653. (Pubitemid 14171425)
65. Wang, D., S. M. Wells, A. M. Stall, and E. A. Kabat. 1994. Reaction of germinal centers in the T-cell-independent response to the bacterial polysaccharide alpha (1->6)dextran. Proc. Natl. Acad. Sci. USA 91: 2502-2506. (Pubitemid 24139375)
66. Sverremark, E., and C. Fernandez. 1998. Germinal center formation following immunization with the polysaccharide dextran B512 is substantially increased by cholera toxin. Int. Immunol. 10: 851-859. (Pubitemid 28325601)
67. Palm, N. W., and R. Medzhitov. 2009. Immunostimulatory activity of haptenated proteins. Proc. Natl. Acad. Sci. USA 106: 4782-4787.
68. Sverremark, E., and C. Fernandez. 1998. Role of T cells and germinal center formation in the generation of immune responses to the thymus-independent carbohydrate dextran B512. J. Immunol. 161: 4646-4651. (Pubitemid 28492038)
69. Ahearn, J. M., M. B. Fischer, D. Croix, S. Goerg, M. Ma, J. Xia, X. Zhou, R. G. Howard, T. L. Rothstein, and M. C. Carroll. 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)
70. -/- mice is rescued by adjuvants without improvement in germinal center development. J. Immunol. 165: 3119-3127.
71. Allen, C. D., T. Okada, and J. G. Cyster. 2007. Germinal-center organization and cellular dynamics. Immunity 27: 190-202. (Pubitemid 47284923)
72. Suzuki, K., M. Maruya, S. Kawamoto, K. Sitnik, H. Kitamura, W. W. Agace, and S. Fagarasan. 2010. The sensing of environmental stimuli by follicular dendritic cells promotes immunoglobulin A generation in the gut. Immunity 33: 71-83.
73. Garin, A., M. Meyer-Hermann, M. Contie, M. T. Figge, V. Buatois, M. Gunzer, K. M. Toellner, G. Elson, and M. H. Kosco-Vilbois. 2010. Toll-like receptor 4 signaling by follicular dendritic cells is pivotal for germinal center onset and affinity maturation. Immunity 33: 84-95.
74. El Shikh, M. E., R. M. El Sayed, Y. Wu, A. K. Szakal, and J. G. Tew. 2007. TLR4 on follicular dendritic cells: an activation pathway that promotes accessory activity. J. Immunol. 179: 4444-4450.
75. Good-Jacobson, K. L., C. G. Szumilas, L. Chen, A. H. Sharpe, M. M. Tomayko, and M. J. Shlomchik. 2010. PD-1 regulates germinal center B cell survival and the formation and affinity of long-lived plasma cells. Nat. Immunol. 11: 535-542.
76. Tangye, S. G., and D. M. Tarlinton. 2009. Memory B cells: effectors of long-lived immune responses. Eur. J. Immunol. 39: 2065-2075.
77. Zotos, D., J. M. Coquet, Y. Zhang, A. Light, K. D'Costa, A. Kallies, L. M. Corcoran, D. I. Godfrey, K. M. Toellner, M. J. Smyth, et al. 2010. IL-21 regulates germinal center B cell differentiation and proliferation through a B cell-intrinsic mechanism. J. Exp. Med. 207: 365-378.
78. O'Connor, B. P., M. Cascalho, and R. J. Noelle. 2002. Short-lived and long-lived bone marrow plasma cells are derived from a novel precursor population. J. Exp. Med. 195: 737-745. (Pubitemid 34259718)