Toll-like receptor ligand links innate and adaptive immune responses by the production of heat-shock proteins

Journal of Leukocyte Biology

Volumn 73, Issue 5, 2003, Pages 574-583

  Kumaraguru, Udayasankar ^a   Pack, Christopher D ^a   Rouse, Barry T ^a  

^a UNIVERSITY OF TENNESSEE   (United States)

Author keywords

Chaperone; Cross priming; DC; Hsp70; M

Indexed keywords

ADJUVANT; ANTIGEN; CD8 ANTIGEN; CYTOKINE; DNA; EPITOPE; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 70; LIGAND; TOLL LIKE RECEPTOR; CELL SURFACE RECEPTOR; CPG OLIGONUCLEOTIDE; CPG-OLIGONUCLEOTIDE; EGG PROTEIN; GLYCOPROTEIN B, TYPE 1 HERPES SIMPLEX VIRUS; IMMUNOLOGICAL ADJUVANT; LIPOPOLYSACCHARIDE; MEMBRANE PROTEIN; MEPACRINE; OLIGODEOXYRIBONUCLEOTIDE; OVA 8; OVA-8; OVALBUMIN; VIRUS ENVELOPE PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN PRESENTING CELL; ARTICLE; CELL STIMULATION; CONTROLLED STUDY; CPG ISLAND; DENDRITIC CELL; DRUG EFFECT; EXPOSURE; FEMALE; IMMUNE RESPONSE; IMMUNOGENICITY; IN VIVO STUDY; LYMPHOCYTE CULTURE; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; T LYMPHOCYTE; UPREGULATION; ANIMAL; ANTIGEN PRESENTATION; BAGG ALBINO MOUSE; BIOSYNTHESIS; C57BL MOUSE; CD8+ T LYMPHOCYTE; CELL CULTURE; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; IMMUNOLOGY; INNATE IMMUNITY; PHYSIOLOGY;

ANIMALIA;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; ANTIGEN PRESENTATION; CD8-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; CPG ISLANDS; DENDRITIC CELLS; EGG PROTEINS; FEMALE; GENE EXPRESSION REGULATION; HSP70 HEAT-SHOCK PROTEINS; IMMUNITY, NATURAL; LIPOPOLYSACCHARIDES; MACROPHAGES; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; OLIGODEOXYRIBONUCLEOTIDES; OVALBUMIN; QUINACRINE; RECEPTORS, CELL SURFACE; TOLL-LIKE RECEPTORS; TRANSFECTION; VIRAL ENVELOPE PROTEINS;

EID: 0038500959     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0902470     Document Type: Article

References (52)

1. Gurunalhan, S., Wu, C. Y., Freidag, B. L., Seder, R. A. (2000) DNA vaccines: a key for inducing long-term cellular immunity. Curr. Opin. Immunol. 12, 442-447.
2. Gurunathan, S., Klinman, D. M., Seder, R. A. (2000) DNA vaccines: immunology, application, and optimization. Annu. Rev. Immunol. 18, 927-974.
3. Paliard, X., Doe, B., Selby, M. J., Hartog, K., Lee, A. Y., Burke, R. L., Walker, C. M. (2001) Induction of herpes simplex virus gB-specific cytotoxic T lymphocytes in TAP1-deficient mice by genetic immunization but not HSV infection. Virology 282, 56-64.
4. Fu, T. M., Ulmer, J. B., Caulfield, M. J., Deck, R. R., Friedman, A., Wang, S., Liu, X., Donnelly, J. J., Liu, M. A. (1997) Priming of cytotoxic T lymphocytes by DNA vaccines: requirement for professional antigen presenting cells and evidence for antigen transfer from myocytes. Mol. Med. 3, 362-371.
5. Klinman, D. M., Yamshchikov, G., Ishigatsubo, Y. (1997) Contribution of CpG motifs to the immunogenicity of DNA vaccines. J. Immunol. 158, 3635-3639.
6. Klinman, D. M., Yi, A. K., Beaucage, S. L., Conover, J., Krieg, A. M. (1996) CpG motifs present in bacteria DNA rapidly induce lymphocytes to secrete interleukin 6, interleukin 12, and interferon gamma. Proc. Natl. Acad. Sci. USA 93, 2879-2883.
7. Krieg, A. M., Yi, A. K., Matson, S., Wahlschmidt, T. J., Bishop, G. A., Teasdale, R., Koretzky, G. A., Klinman, D. M. (1995) CpG motifs in bacterial DNA trigger direct B cell activation. Nature 374, 546-549.
8. Krieg, A. M. (2000) The role of CpG motifs in innate immunity. Curr. Opin. Immunol. 12, 35-43.
9. Krieg, A. M. (2000) Immune effects and mechanisms of action of CpG motifs. Vaccine 19, 618-622.
10. Krieg, A. M. (2002) CpG motifs in bacterial DNA and their immune effects. Annu. Rev. Immunol. 20, 709-760.
11. Cho, H. J., Takabayashi, K., Cheng, P. M., Nguyen, M. D., Corr, M., Tuck, S., Raz, E. (2000) Immunostimulatory DNA-based vaccines induce cytotoxic lymphocyte activity by a T-helper cell-independent mechanism. Nat. Biotechnol. 18, 509-514.
12. Wild, J., Grusby, M. J., Schirmbeek, R., Reimann, J. (1999) Priming MHC-I-restricted cytotoxic T lymphocyte responses to exogenous hepatitis B surface antigen is CD4+ T cell dependent. J. Immunol. 163, 1880-1887.
13. Homer, A. A., Datta, S. K., Takabayashi, K., Belyakov, I. M., Hayashi, T., Cinman, N., Nguyen, M. D., Van Uden, J. H., Berzofsky, J. A., Richman, D. D., Raz, E. (2001) Immunostimulatory DNA-based vaccines elicit multifaceted immune responses against HIV at systemic and mucosal sites. J. Immunol. 167, 1584-1591.
14. Gierynska, M., Kumaraguru, U., Gierynska, M., Kumaraguru, U., Eo, S. K., Lee, S., Krieg, A., Rouse, B. T. (2002) Induction of CD8 T cell-specific systemic and mucosal immunity against herpes simplex virus with CpG-peptide complexes. J. Virol. 76, 6568-6576.
15. Sparwasser, T., Koch, E. S., Vabulas, R. M., Heeg, K., Lipford, G. B., Ellwart, J. W., Wagner, H. (1998) Bacterial DNA and immunostimulatory CpG oligonucleotides trigger maturation and activation of murine dendritic cells. Eur. J. Immunol. 28, 2045-2054.
16. Jakob, T., Walker, P. S., Krieg, A. M., Udey, M. C., Vogel, J. C. (1998) Activation of cutaneous dendritic cells by CpG-containing oligodeoxynucleotides: a role for dendritic cells in the augmentation of Th1 responses by immunostimulatory DNA. J. Immunol. 161, 3042-3049.
17. Askew, D., Chu, R. S., Krieg, A. M., Harding, C. V. (2000) CpG DNA induces maturation of dendritic cells with distinct effects on nascent and recycling MHC-II antigen-processing mechanisms. J. Immunol. 165, 6889-6895.
18. Kumaraguru, U., Rouse, R. J., Nair, S. K., Bruce, B. D., Rouse, B. T. (2000) Involvement of an ATP-dependent peptide chaperone in cross-presentation after DNA immunization. J. Immunol. 165, 750-759.
19. Cho, H. J., Hayashi, T., Datta, S. K., Takabayashi, K., Van Uden, J. H., Horner, A., Corr, M., Raz, E. (2002) IFN-alphabeta promote priming of antigen-specific CD8(+) and CD4(+) T lymphocytes by immunostimulatory DNA-based vaccines. J. Immunol. 168, 4907-4913.
20. Srivastava, P. K. (2002) Interaction of heat shock proteins with peptides and antigen presenting cells: chaperoning of the innate and adaptive immune responses. Annu. Rev. Immunol. 20, 395-425.
21. Hogquist, K. A., Jameson, S. C., Heath, W. R., Howard, J. L., Bevan, M. J., Carbone, F. R. (1994) T cell receptor antagonist peptides induce positive selection. Cell 76, 17-27.
22. Rouse, R. J., Nair, S. K., Lydy, S. L., Bowen, J. C., Rouse, B. T. (1994) Induction in vitro of primary cytotoxic T-lymphocyte responses with DNA encoding herpes simplex virus proteins. J. Virol. 68, 5685-5689.
23. Moore, M. W., Carbone, F. R., Bevan, M. J. (1988) Introduction of soluble protein into the class I pathway of antigen processing and presentation. Cell 54, 777-785.
24. Craig, E. A., Kramer, J., Shilling, J., Werner-Washburne, M., Holmes, S., Kosic-Smithers, J., Nicolet, C. M. (1989) SSC1, an essential member of the yeast HSP70 multigene family, encodes a mitochondrial protein. Mol. Cell. Biol. 9, 3000-3008.
25. Nair, S., Zhou, F., Reddy, R., Huang, L., Rouse, B. T. (1992) Soluble proteins delivered to dendritic cells via pH-sensitive liposomes induce primary cytotoxic T lymphocyte responses in vitro, J. Exp. Med. 175, 609-612.
26. Eastcott, J. W., Holmberg, C. J., Dewhirst, F. E., Esch, T. R., Smith, D. J., Taubman, M. A. (2001) Oligonucleotide containing CpG motifs enhances immune response to mucosally or systemically administered tetanus toxoid. Vaccine 19, 1636-1642.
27. Mueller, S. N., Jones, C. M., Smith, C. M., Heath, W. R., Carbone, F. R. (2002) Rapid cytotoxic T lymphocyte activation occurs in the draining lymph nodes after cutaneous herpes simplex virus infection as a result of early antigen presentation and not the presence of virus. J. Exp. Med. 195, 651-656.
28. Peng, P., Menoret, A., Srivastava, P. K. (1997) Purification of immunogenic heat shock protein 70-peptide complexes by ADP-affinity chromatography, J. Immunol. Methods 204, 13-21.
29. Van Rooijen, N., Sanders, A. (1994) Liposome mediated depletion of macrophages: mechanism of action, preparation of liposomes and applications. J. Immunol. Methods 174, 83-93.
30. Brewer, J. M., Alexander, J. (1997) Cytokines and the mechanism of action of vaccine adjuvants. Cytokines Cell. Mol. Ther. 3, 233-246.
31. Suto, R., Srivastava, P. K. (1995) A mechanism for the specific immunogenicity of heat shock protein-chaperoned peptides. Science 269, 1585-1588.
32. Macfarlane, D. E., Manzel, L. (1998) Antagonism of immunostimulatory CpG-oligodeoxynucleotides by quinacrine, chloroquine, structurally related compounds. J. Immunol 160, 1122-1131.
33. Wagner, H. (1999) Bacterial CpG DNA activates immune cells to signal infectious danger. Adv. Immunol 73, 329-368.
34. Miconnet, I., Koenig, S., Speiser, D., Krieg, A., Guillaume, P., Cerottini, J. C., Romero, P. (2002) CpG are efficient adjuvants for specific CTL induction against tumor antigen-derived peptide. J. Immunol. 168, 1212-1218.
35. Ronaghy, A., Prakken, B. J., Takabavasin, K., Firestein, G. S., Boyle, D., Zvailfler, N. J., Roord, S. T., Albani, S., Carson, D. A., Raz, E. (2002) Immunostimulatory DNA sequences influence the course of adjuvant arthritis. J. Immunol. 168, 51-56.
36. Chu, R. S., Targoni, O. S., Krieg, A. M., Lehmann, P. V., Harding, C. V. (1997) CpG oligodeoxynucleotides act as adjuvants that switch on T helper I (Th1) immunity. J. Exp. Med. 186, 1623-1631.
37. McCluskie, M. J., Weeratna, R. D., Davis, H. L. (2001) The potential of oligodeoxynucleotides as mucosal and parenteral adjuvants. Vaccine 19, 2657-2660.
38. McCluskie, M. J., Weeratna, R. D., Davis, H. L. (2000) Intranasal immunization of mice with CpG DNA induces strong systemic and mucosal responses that are influenced by other mucosal adjuvants and antigen distribution. Mol. Med. 6, 867-877.
39. Warren, T. L., Bhatia, S. K., Acosta, A. M., Dahle, C. E., Ratliff, T. L., Krieg, A. M., Wiener, G. J. (2000) APC stimulated by CpG oligodeoxynucleotide enhance activation of MHC class I-restricted T cells. J. Immunol. 165, 6244-6251.
40. Chu, R. S., Askew, D., Harding, C. V. (2000) CpG DNA switches on Th1 immunity and modulates antigen-presenting cell function. Curr. Top. Microbiol. Immunol. 247, 199-210.
41. Klinman, D. M., Yamshchikov, G., Ishigatsubo, Y. (1997) Contribution of CpG motifs to the immunogenicity of DNA vaccines. J. Immunol. 158, 3635-3639.
42. Chu, R. S., Askew, D., Noss, E. H. Tobian, A., Krieg, A. M., Harding, C. V. (1999) CpG oligodeoxynucleotides down-regulate macrophage class 11 MHC antigen processing. J. Immunol. 163, 1188-1191.
43. Wagner Hemmi, H., Takeuchi, O., Kawai, T., Kaisho, T., Sato, S., Sanjo, H., Matsumoto, M., Hoshino, K., Wagner, H., Takeda, K., Akira, S. (2000) A Toll-like receptor recognizes bacterial DNA. Nature 408, 740-745.
44. Takeshita, F., Leifer, C. A., Gursel, I., Ishii, K. J., Takeshita, S., Gursel, M., Klinman, D. M. (2001) Role of Toll-like receptor 9 in CpG DNA-induced activation of human cells. J. Immunol. 167, 3555-3558.
45. Doe, B., Selby, M., Barnett, S., Baenziger, J., Walker, C. M. (1996) Induction of cytotoxic T lymphocytes by intramuscular immunization with plasmid DNA is facilitated by, bone marrow-derived cells. Proc. Natl. Acad. Sci. USA 93, 8578-8583.
46. Maurer, T., Heit, A., Hochreiu, H., Ampenberger, F., O'Keeffe, M., Bauer, S., Lipford, G. B., Vabulas, R. M., Wagner, H. (2002) CpG-DNA aided cross-presentation of soluble antigens by dendritic cells. Eur. J. Immunol. 32, 2356-2364.
47. Asea, A., Rehli, M., Kabingu, E., Boch, J. A., Bare, O., Auron, P. E., Stevenson, M. A., Calderwood, S. K. (2002) Novel signal transduction pathway used by extracellular HSP70: role of toll-like receptor (TLR) 2 and TLR4. J. Biol. Chem. 277, 15028-15034.
48. Basu, S., Binder, R. J., Ramalingam, T., Srivastava, P. K. (2001) CD91 is a common receptor for heat shock proteins gp96, hsp90, hsp70, and calreticulin. Immunity 14, 303-313.
49. Binder, R. J., Han, D. K., Srivastava, P. K. (2000) CD91: a receptor for heat shock protein gp96. Nat. Immunol, 1, 151-155.
50. Binder, R. J., Anderson, K. M., Basu, S., Srivastava, P. K. (2000) Heat shock protein gp96 induces maturation and migration of CD11c+ cells in vivo. J. Immunol. 165, 6029-6035,
51. Vabulas, R. M., Braedel, S., Hilf, N., Singh-Jasuja, H., Herter, S, Ahmad-Nejad, P., Kirschning, C. J., Da Costa, C., Rammensee, H. G., Wagner, H., Schild, H. (2002) The endoplasmic reticulum-resident heat shock protein Gp96 activates dendritic cells via the Toll-like receptor 214 pathway. J. Biol. Chem, 277, 20847-20853.
52. Stan, A. C., Casares, S., Brumeanu, T. D., Klinman, D. M., Bona, C. A. (2001) CpG motifs of DNA vaccines induce the expression of chemokines and MHC class II molecules on myocytes. Eur. J. Immunol, 31, 301-310.