CpG Oligodeoxynucleotides Act as Adjuvants that Switch on T Helper 1 (Th1) Immunity

doi:10.1084/jem.186.10.1623

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J. Exp. Med., Volume 186, Number 10, November 17, 1997 1623-1631

CpG Oligodeoxynucleotides Act as Adjuvants that Switch on T Helper 1 (Th1) Immunity

By Rose S. Chu,^* Oleg S. Targoni,^* Arthur M. Krieg, Paul V. Lehmann,^* and Clifford V. Harding^*

From the ^* Institute of Pathology, Case Western Reserve University, Cleveland, Ohio 44106; and Department of Internal Medicine, University of Iowa, Iowa City, Iowa 52242

Synthetic oligodeoxynucleotides (ODN) that contain unmethylated CpG motifs (CpG ODN) induce macrophages to secrete IL-12,which induces interferon (IFN)- $gamma$ secretion by natural killer (NK)cells. Since these cytokines can induce T helper 1 (Th1) differentiation,we examined the effects of coadministered CpG ODN on the differentiationof Th responses to hen egg lysozyme (HEL). In both BALB/c (Th2-biased)and B10.D2 (Th1-biased) mice, immunization with HEL in incompleteFreund's adjuvant (IFA) resulted in Th2-dominated immune responsescharacterized by HEL-specific secretion of IL-5 but not IFN- $gamma$ .In contrast, immunization with IFA-HEL plus CpG ODN switched theimmune response to a Th1-dominated cytokine pattern, with highlevels of HEL-specific IFN- $gamma$ secretion and decreased HEL-specificIL-5 production. IFA-HEL plus CpG ODN also induced anti-HEL IgG2a(a Th1-associated isotype), which was not induced by IFA-HEL alone.Control non-CpG ODN did not induce IFN- $gamma$ or IgG2a, excepting lesserincreases in B10.D2 (Th1-biased) mice. Thus, CpG ODN provide asignal to switch on Th1-dominated responses to coadministeredantigen and are potential adjuvants for human vaccines to elicitprotective Th1 immunity.

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Rhee, E. G., Mendez, S., Shah, J. A., Wu, C.-y., Kirman, J. R., Turon, T. N., Davey, D. F., Davis, H., Klinman, D. M., Coler, R. N., Sacks, D. L., Seder, R. A. (2002). Vaccination with Heat-killed Leishmania Antigen or Recombinant Leishmanial Protein and CpG Oligodeoxynucleotides Induces Long-Term Memory CD4+and CD8+T Cell Responses and Protection Against Leishmania major Infection. JEM 195: 1565-1573 [Abstract] [Full Text]
Stern, B. V., Boehm, B. O., Tary-Lehmann, M. (2002). Vaccination with Tumor Peptide in CpG Adjuvant Protects Via IFN-{gamma}-Dependent CD4 Cell Immunity. J. Immunol. 168: 6099-6105 [Abstract] [Full Text]
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 [Abstract] [Full Text]
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Riedl, P., Stober, D., Oehninger, C., Melber, K., Reimann, J., Schirmbeck, R. (2002). Priming Th1 Immunity to Viral Core Particles Is Facilitated by Trace Amounts of RNA Bound to Its Arginine-Rich Domain. J. Immunol. 168: 4951-4959 [Abstract] [Full Text]
He, Y., Vemulapalli, R., Schurig, G. G. (2002). Recombinant Ochrobactrum anthropi Expressing Brucella abortus Cu,Zn Superoxide Dismutase Protects Mice against B. abortus Infection Only after Switching of Immune Responses to Th1 Type. Infect. Immun. 70: 2535-2543 [Abstract] [Full Text]
Nagayama, Y., Kita-Furuyama, M., Ando, T., Nakao, K., Mizuguchi, H., Hayakawa, T., Eguchi, K., Niwa, M. (2002). A Novel Murine Model of Graves' Hyperthyroidism with Intramuscular Injection of Adenovirus Expressing the Thyrotropin Receptor. J. Immunol. 168: 2789-2794 [Abstract] [Full Text]
Vasselon, T., Detmers, P. A. (2002). Toll Receptors: a Central Element in Innate Immune Responses. Infect. Immun. 70: 1033-1041 [Full Text]
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 [Abstract] [Full Text]
Nau, R., Eiffert, H. (2002). Modulation of Release of Proinflammatory Bacterial Compounds by Antibacterials: Potential Impact on Course of Inflammation and Outcome in Sepsis and Meningitis. Clin. Microbiol. Rev. 15: 95-110 [Abstract] [Full Text]
Renz, H., Herz, U. (2002). The bidirectional capacity of bacterial antigens to modulate allergy and asthma. Eur Respir J 19: 158-171 [Abstract] [Full Text]
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Ronaghy, A., Prakken, B. J., Takabayashi, K., Firestein, G. S., Boyle, D., Zvailfler, N. J., Roord, S. T. A., Albani, S., Carson, D. A., Raz, E. (2002). Immunostimulatory DNA Sequences Influence the Course of Adjuvant Arthritis. J. Immunol. 168: 51-56 [Abstract] [Full Text]
Billiau, A., Matthys, P. (2001). Modes of action of Freund's adjuvants in experimental models of autoimmune diseases. J. Leukoc. Biol. 70: 849-860 [Abstract] [Full Text]
Ballas, Z. K., Krieg, A. M., Warren, T., Rasmussen, W., Davis, H. L., Waldschmidt, M., Weiner, G. J. (2001). Divergent Therapeutic and Immunologic Effects of Oligodeoxynucleotides with Distinct CpG Motifs. J. Immunol. 167: 4878-4886 [Abstract] [Full Text]
Kawarada, Y., Ganss, R., Garbi, N., Sacher, T., Arnold, B., Hammerling, G. J. (2001). NK- and CD8+ T Cell-Mediated Eradication of Established Tumors by Peritumoral Injection of CpG-Containing Oligodeoxynucleotides. J. Immunol. 167: 5247-5253 [Abstract] [Full Text]
Gursel, I., Gursel, M., Ishii, K. J., Klinman, D. M. (2001). Sterically Stabilized Cationic Liposomes Improve the Uptake and Immunostimulatory Activity of CpG Oligonucleotides. J. Immunol. 167: 3324-3328 [Abstract] [Full Text]
Baek, K. H., Ha, S. J., Sung, Y. C. (2001). A Novel Function of Phosphorothioate Oligodeoxynucleotides as Chemoattractants for Primary Macrophages. J. Immunol. 167: 2847-2854 [Abstract] [Full Text]
Britigan, B. E., Lewis, T. S., Waldschmidt, M., McCormick, M. L., Krieg, A. M. (2001). Lactoferrin Binds CpG-Containing Oligonucleotides and Inhibits Their Immunostimulatory Effects on Human B Cells. J. Immunol. 167: 2921-2928 [Abstract] [Full Text]
Blazar, B. R., Krieg, A. M., Taylor, P. A. (2001). Synthetic unmethylated cytosine-phosphate-guanosine oligodeoxynucleotides are potent stimulators of antileukemia responses in naive and bone marrow transplant recipients. Blood 98: 1217-1225 [Abstract] [Full Text]
Al-Mariri, A., Tibor, A., Mertens, P., De Bolle, X., Michel, P., Godefroid, J., Walravens, K., Letesson, J.-J. (2001). Protection of BALB/c Mice against Brucella abortus 544 Challenge by Vaccination with Bacterioferritin or P39 Recombinant Proteins with CpG Oligodeoxynucleotides as Adjuvant. Infect. Immun. 69: 4816-4822 [Abstract] [Full Text]
Chen, Y., Zhang, J., Moore, S. A., Ballas, Z. K., Portanova, J. P., Krieg, A. M., Berg, D. J. (2001). CpG DNA induces cyclooxygenase-2 expression and prostaglandin production. Int Immunol 13: 1013-1020 [Abstract] [Full Text]
Bauer, S., Kirschning, C. J., Hacker, H., Redecke, V., Hausmann, S., Akira, S., Wagner, H., Lipford, G. B. (2001). Human TLR9 confers responsiveness to bacterial DNA via species-specific CpG motif recognition. Proc. Natl. Acad. Sci. USA 10.1073/pnas.161293498v1 [Abstract] [Full Text]
Malanchere-Bres, E., Payette, P. J., Mancini, M., Tiollais, P., Davis, H. L., Michel, M.-L. (2001). CpG Oligodeoxynucleotides with Hepatitis B Surface Antigen (HBsAg) for Vaccination in HBsAg-Transgenic Mice. J. Virol. 75: 6482-6491 [Abstract] [Full Text]