Programming the magnitude and persistence of antibody responses with innate immunity

Nature

Volumn 470, Issue 7335, 2011, Pages 543-550

  Kasturi, Sudhir Pai ^a   Skountzou, Ioanna ^a,b   Albrecht, Randy A ^c   Koutsonanos, Dimitrios ^b   Hua, Tang ^a   Nakaya, Helder I ^a   Ravindran, Rajesh ^a   Stewart, Shelley ^d   Alam, Munir ^d   Kwissa, Marcin ^a   Villinger, Francois ^a,b   Murthy, Niren ^e   Steel, John ^c   Jacob, Joshy ^a,b   Hogan, Robert J ^f   García Sastre, Adolfo ^c   Compans, Richard ^a,b   Pulendran, Bali ^a,b  

^a EMORY UNIVERSITY   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^d DUKE UNIVERSITY MEDICAL CENTER   (United States)

^e GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^f UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMIQUIMOD; NEUTRALIZING ANTIBODY; OVALBUMIN; PHOSPHORYL LIPID A; POLYGLACTIN; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 7;

ANTIBODY; ANTIGEN; CELL ORGANELLE; IMMUNIZATION; INFLUENZA; LIGAND; MAGNITUDE; MOLECULAR ANALYSIS; PARTICULATE MATTER; PLASMA; RODENT; VACCINATION; VIRUS;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ANTIGEN SPECIFICITY; ARTICLE; B LYMPHOCYTE ACTIVATION; CELL ISOLATION; CONTROLLED STUDY; DENDRITIC CELL; FEMALE; INFLUENZA A (H1N1); INFLUENZA A (H5N1); INFLUENZA VIRUS A H1N1; INFLUENZA VIRUS A H5N1; INNATE IMMUNITY; MOUSE; NONHUMAN; PLASMA CELL; PRIORITY JOURNAL; SWINE; T LYMPHOCYTE;

ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; ANTIBODY FORMATION; DENDRITIC CELLS; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; IMMUNITY, INNATE; IMMUNOLOGIC MEMORY; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H5N1 SUBTYPE; INFLUENZA VACCINES; LACTIC ACID; LIGANDS; LYMPH NODES; LYMPHOCYTE ACTIVATION; MACACA MULATTA; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; NANOPARTICLES; PLASMA CELLS; POLYGLYCOLIC ACID; T-LYMPHOCYTES; TOLL-LIKE RECEPTORS;

AVES; MACACA MULATTA; MUS; SWINE INFLUENZA VIRUS;

EID: 79952173864     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature09737     Document Type: Article

References (56)

1. Pulendran, B. & Ahmed, R. Translating innate immunity into immunological memory: implications for vaccine development. Cell 124, 849-863 (2006). (Pubitemid 43261457)
2. Kawai, T. & Akira, S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nature Immunol. 11, 373-384 (2010).
3. Pulendran, B. Learning immunology from the yellow fever vaccine: innate immunity to systems vaccinology. Nature Rev. Immunol. 9, 741-747 (2009).
4. Querec, T. et al. Yellow fever vaccine YF-17D activates multiple dendritic cell subsets via TLR2, 7, 8, and 9 to stimulate polyvalent immunity. J. Exp. Med. 203, 413-424 (2006). (Pubitemid 43290850)
5. Querec, T. D. et al. Systems biology approach predicts immunogenicity of the yellow fever vaccine in humans. Nature Immunol. 10, 116-125 (2009).
6. Napolitani, G., Rinaldi, A., Bertoni, F., Sallusto, F. & Lanzavecchia, A. Selected Tolllike receptor agonist combinations synergistically trigger a T helper type 1-polarizing program in dendritic cells. Nature Immunol. 6, 769-776 (2005). (Pubitemid 43090462)
7. Peek, L. J., Middaugh, C. R.&Berkland, C. Nanotechnology in vaccine delivery. Adv. Drug Deliv. Rev. 60, 915-928 (2008).
8. Kazzaz, J. et al. Encapsulation of the immune potentiatorsMPL and RC529 in PLG microparticles enhances their potency. J. Control. Release 110, 566-573 (2006). (Pubitemid 43168189)
9. Singh, M., Chakrapani, A. & O'Hagan, D. Nanoparticles and microparticles as vaccine-delivery systems. Expert Rev. Vaccines 6, 797-808 (2007). (Pubitemid 47607854)
10. Young, J. A. & Collier, J. R. Attacking anthrax. Sci. Am. 286, 48-59 (2002). (Pubitemid 34563197)
11. Chen, G. L. & Subbarao, K. Live attenuated vaccines for pandemic influenza. Curr. Top. Microbiol. Immunol. 333, 109-132 (2009).
12. Hangartner, L., Zinkernagel, R. M. & Hengartner, H. Antiviral antibody responses: the two extremes of a wide spectrum. Nature Rev. Immunol. 6, 231-243 (2006). (Pubitemid 43290992)
13. Jung, S. et al. In vivodepletionofCD11c1dendritic cellsabrogates primingofCD81 T cells by exogenous cell-associated antigens. Immunity 17, 211-220 (2002). (Pubitemid 35245963)
14. Kissenpfennig, A. et al. Dynamics and function of Langerhans cells in vivo: dermal dendritic cells colonize lymph node areas distinct from slower migrating Langerhans cells. Immunity 22, 643-654 (2005). (Pubitemid 40719199)
15. Mata-Haro, V. et al. The vaccine adjuvantmonophosphoryl lipid A as a TRIF-biased agonist of TLR4. Science 316, 1628-1632 (2007). (Pubitemid 46982038)
16. Bernasconi, N. L., Traggiai, E. & Lanzavecchia, A. Maintenance of serological memory by polyclonal activation of human memory B cells. Science 298, 2199-2202 (2002). (Pubitemid 35471246)
17. Pasare, C.&Medzhitov, R. Control of B-cell responses by Toll-like receptors. Nature 438, 364-368 (2005). (Pubitemid 41643953)
18. Mitchison, N. A. T-cell-B-cell cooperation. Nature Rev. Immunol. 4, 308-312 (2004). (Pubitemid 38478666)
19. vanEssen, D.,Dullforce, P., Brocker, T.&Gray, D. Cellular interactions involved inTh cell memory. J. Immunol. 165, 3640-3646 (2000). (Pubitemid 32057268)
20. McHeyzer-Williams, L. J. & McHeyzer-Williams, M. G. Antigen-specific memory B cell development. Annu. Rev. Immunol. 23, 487-513 (2005). (Pubitemid 40563178)
21. Slifka, M. K., Antia, R., Whitmire, J. K. & Ahmed, R. Humoral immunity due to longlived plasma cells. Immunity 8, 363-372 (1998). (Pubitemid 28188896)
22. McHeyzer-Williams, M. G.,McLean, M. J., Lalor, P. A.&Nossal, G. J. Antigen-drivenB cell differentiation in vivo. J. Exp. Med. 178, 295-307 (1993). (Pubitemid 23173265)
23. Luckey, C. J. et al.Memory T andmemoryBcells share a transcriptional programof self-renewal with long-term hematopoietic stem cells. Proc. Natl Acad. Sci. USA 103, 3304-3309 (2006). (Pubitemid 43346465)
24. Wille-Reece, U. et al. HIV Gag protein conjugated to a Toll-like receptor 7/8 agonist improves the magnitude and quality of Th1 and CD81 T cell responses in nonhuman primates. Proc. Natl Acad. Sci. USA 102, 15190-15194 (2005). (Pubitemid 41513357)
25. Steel, J. et al. Live attenuated influenza viruses containing NS1 truncations as vaccine candidates against H5N1 highly pathogenic avian influenza. J. Virol. 83, 1742-1753 (2009).
26. Jurk, M. et al. Human TLR7 or TLR8 independently confer responsiveness to the antiviral compound R-848. Nature Immunol. 3, 499 (2002). (Pubitemid 34669818)
27. Dorner, M. et al. Plasma cell toll-like receptor (TLR) expression differs fromthat ofB cells, and plasma cell TLR triggering enhances immunoglobulin production. Immunology 128, 573-579 (2009).
28. Clark, T. W. et al. Trial of 2009 influenza A (H1N1) monovalent MF59-adjuvanted vaccine. N. Engl. J. Med. 361, 2424-2435 (2009).
29. Potter, C. W.&Oxford, J. S.Determinants ofimmunity to influenza infection inman. Br. Med. Bull. 35, 69-75 (1979). (Pubitemid 9096975)
30. Bachmann, M. F., Odermatt, B., Hengartner, H. & Zinkernagel, R. M. Induction of long-lived germinal centers associated with persisting antigen after viral infection. J. Exp. Med. 183, 2259-2269 (1996). (Pubitemid 26158917)
31. Sah, H. A new strategy to determine the actual protein content of poly(lactide-coglycolide) microspheres. J. Pharm. Sci. 86, 1315-1318 (1997). (Pubitemid 27486108)
32. Henri, S. et al. CD2071 CD1031 dermal dendritic cells cross-present keratinocytederived antigens irrespective of the presence of Langerhans cells. J. Exp. Med. 207, 189-206 (2010).
33. den Haan, J. M., Kraal, G. & Bevan, M. J. Cutting edge: lipopolysaccharide induces IL-10-producing regulatoryCD41T cells that suppress theCD81T cell response. J. Immunol. 178, 5429-5433 (2007). (Pubitemid 46674336)
34. Zhu, Q. et al. Immunization by vaccine-coated microneedle arrays protects against lethal influenza virus challenge. Proc. Natl Acad. Sci. USA 106, 7968-7973 (2009).
35. Staats, H. F. et al. In vitro and in vivo characterization of anthrax anti-protective antigen and anti-lethal factor monoclonal antibodies after passive transfer in a mouse lethal toxin challenge model to define correlates of immunity. Infect. Immun. 75, 5443-5452 (2007). (Pubitemid 350033633)
36. Compans, R. W. Hemagglutination-inhibition: rapid assay for neuraminic acidcontaining viruses. J. Virol. 14, 1307-1309 (1974).
37. Enioutina, E. Y., Visic, D. & Daynes, R. A. The induction of systemic and mucosal immune responses to antigen-adjuvant compositions administered into the skin: alterations in the migratory properties of dendritic cells appears to be important for stimulating mucosal immunity. Vaccine 18, 2753-2767 (2000). (Pubitemid 30211584)
38. Reed, L. J.&Muench, H.Asimplemethodof estimatingfifty percentendpoints.Am. J. Hyg. 27, 493-497 (1938).
39. Badr, G. et al. Type I interferon(IFN-a/b) rescues B-lymphocytes fromapoptosis via PI3Kd/Akt, Rho-A, NFkB and Bcl-2/Bcl(XL). Cell. Immunol. 263, 31-40 (2010).
40. Bekeredjian-Ding, I. B. et al. Plasmacytoid dendritic cells control TLR7 sensitivity of naive B cells via type I IFN. J. Immunol. 174, 4043-4050 (2005).
41. Thibault, D. L. et al. IRF9 and STAT1 are required for IgG autoantibody production and B cell expression of TLR7 in mice. J. Clin. Invest. 118, 1417-1426 (2008). (Pubitemid 351500435)
42. Tovey, M. G., Lallemand, C.&Thyphronitis, G. Adjuvant activity of type I interferons. Biol. Chem. 389, 541-545 (2008). (Pubitemid 351874185)
43. Swanson, C. L. et al. Type I IFN enhances follicular B cell contribution to the T cellindependent antibody response. J. Exp. Med. 207, 1485-1500 (2010).
44. Liu, H. et al. Functional studies of BCL11A: characterization of the conserved BCL11A-XL splice variant and its interaction with BCL6 in nuclear paraspeckles of germinal center B cells. Mol. Cancer 5, 18 (2006).
45. Smith, K. G. et al. bcl-2 transgene expression inhibits apoptosis in the germinal center and reveals differences in the selection ofmemoryBcells and bonemarrow antibody-forming cells. J. Exp. Med. 191, 475-484 (2000).
46. Aiba, Y. et al. Preferential localization of IgG memory B cells adjacent to contracted germinal centers. Proc. Natl Acad. Sci. USA 107, 12192-12197 (2010).
47. Zhou, G. & Ono, S. J. Induction of BCL-6 gene expression by interferon-c and identification of an IRE in exon I. Exp. Mol. Pathol. 78, 25-35 (2005). (Pubitemid 41373313)
48. Mitsdoerffer, M. et al. Proinflammatory T helper type 17 cells are effective B-cell helpers. Proc. Natl Acad. Sci. USA 107, 14292-14297 (2010).
49. Chin, A. I. et al. TANKpotentiates tumor necrosis factor receptor-associated factormediated c-Jun N-terminal kinase/stress-activated protein kinase activation through the germinal center kinase pathway. Mol. Cell. Biol. 19, 6665-6672 (1999). (Pubitemid 29441850)
50. Basso, K. & Dalla-Favera, R. BCL6:master regulator of the germinal center reaction and key oncogene inBcell lymphomagenesis.Adv. Immunol.105, 193-210 (2010).
51. Kano, G. et al. Ikaros dominant negative isoform (Ik6) induces IL-3-independent survival of murine pro-B lymphocytes by activating JAK-STAT and up-regulating Bcl-xl levels. Leuk. Lymphoma 49, 965-973 (2008). (Pubitemid 351942752)
52. Ke, N., Godzik, A.&Reed, J. C. Bcl-B, a novel Bcl-2 familymember that differentially binds and regulates Bax and Bak. J. Biol. Chem. 276, 12481-12484 (2001).
53. Airoldi, I. et al. Expression and function of IL-12 and IL-18 receptors on human tonsillar B cells. J. Immunol. 165, 6880-6888 (2000). (Pubitemid 32001157)
54. Airoldi, I. et al. Heterogeneous expression of interleukin-18 and its receptor in B-cell lymphoproliferative disorders deriving from naive, germinal center, and memory B lymphocytes. Clin. Cancer Res. 10, 144-154 (2004). (Pubitemid 38114173)
55. Hikida, M. et al. PLC-c2 is essential for formation and maintenance of memory B cells. J. Exp. Med. 206, 681-689 (2009).
56. Nera, K. P. & Lassila, O. Pax5-a critical inhibitor of plasma cell fate. Scand. J. Immunol. 64, 190-199 (2006). (Pubitemid 44215107)