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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)- 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 differentiation of Th responses to hen egg lysozyme (HEL). In both BALB/c (Th2-biased) and B10.D2 (Th1-biased) mice, immunization with HEL in incomplete Freund's adjuvant (IFA) resulted in Th2-dominated immune responses characterized by HEL-specific secretion of IL-5 but not IFN-. In contrast, immunization with IFA-HEL plus CpG ODN switched the immune response to a Th1-dominated cytokine pattern, with high levels of HEL-specific IFN- secretion and decreased HEL-specific IL-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- or IgG2a, excepting lesser increases in B10.D2 (Th1-biased) mice. Thus, CpG ODN provide a signal to switch on Th1-dominated responses to coadministered antigen and are potential adjuvants for human vaccines to elicit protective Th1 immunity.

¹ Abbreviations used in this paper: HEL, hen egg lysozyme; ODN, oligodeoxynucleotides; PBST, PBS with Tween; S ODN, phosphorothioate-modified ODN; S-O ODN, ODN with partial phosphorothioate modification.

The first two authors contributed equally to this work.

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• Kline, J. N., Kitagaki, K., Businga, T. R., Jain, V. V. (2002). Treatment of established asthma in a murine model using CpG oligodeoxynucleotides. Am. J. Physiol. Lung Cell. Mol. Physiol. 283: L170-L179 [Abstract] [Full Text]  
• 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]  
• Dalpke, A. H., Schafer, M. K.-H., Frey, M., Zimmermann, S., Tebbe, J., Weihe, E., Heeg, K. (2002). Immunostimulatory CpG-DNA Activates Murine Microglia. J. Immunol. 168: 4854-4863 [Abstract] [Full Text]  
• 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]  
• Juffermans, N. P., Leemans, J. C., Florquin, S., Verbon, A., Kolk, A. H., Speelman, P., van Deventer, S. J. H., van der Poll, T. (2002). CpG Oligodeoxynucleotides Enhance Host Defense during Murine Tuberculosis. Infect. Immun. 70: 147-152 [Abstract] [Full Text]  
• 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]  

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