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The Journal of Immunology, 2000, 164: 1617-1624.
Copyright © 2000 by The American Association of Immunologists

Delineation of a CpG Phosphorothioate Oligodeoxynucleotide for Activating Primate Immune Responses In Vitro and In Vivo1

Gunther Hartmann*,{dagger}, Risini D. Weeratna{ddagger}, Zuhair K. Ballas*, Paul Payette{ddagger}, Sue Blackwell*, Irma Suparto, Wendy L. Rasmussen§, Marianella Waldschmidt, Dondin Sajuthi, Robert H. Purcell||, Heather L. Davis{ddagger},# and Arthur M. Krieg2,*,#

* Department of Internal Medicine, University of Iowa, Iowa City, IA 52242; {dagger} CpG ImmunoPharmaceuticals GmbH, Hilden, Germany; {ddagger} Loeb Health Research Institute at the Ottawa Hospital, and Faculties of Health Sciences and Medicine, University of Ottawa, Ottawa, Canada; § Veterans Affairs Medical Center, Iowa City, IA 52246; Primate Research Center, Bogor Agricultural University, Bogor, Indonesia; || Hepatitis Viruses Section, Laboratory of Infectious Diseases, National Institute of Arthritis and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892; and # CpG ImmunoPharmaceuticals, Inc., Wellesley, MA 02481

Oligodeoxynucleotides (ODN) containing unmethylated CpG dinucleotides within specific sequence contexts (CpG motifs) are detected, like bacterial or viral DNA, as a danger signal by the vertebrate immune system. CpG ODN synthesized with a nuclease-resistant phosphorothioate backbone have been shown to be potent Th1-directed adjuvants in mice, but these motifs have been relatively inactive on primate leukocytes in vitro. Moreover, in vitro assays that predict in vivo adjuvant activity for primates have not been reported. In the present study we tested a panel of CpG ODN for their in vitro and in vivo immune effects in mice and identified in vitro activation of B and NK cells as excellent predictors of in vivo adjuvant activity. Therefore, we tested >250 phosphorothioate ODN for their capacity to stimulate proliferation and CD86 expression of human B cells and to induce lytic activity and CD69 expression of human NK cells. These studies revealed that the sequence, number, and spacing of individual CpG motifs contribute to the immunostimulatory activity of a CpG phosphorothioate ODN. An ODN with a TpC dinucleotide at the 5' end followed by three 6 mer CpG motifs (5'-GTCGTT-3') separated by TpT dinucleotides consistently showed the highest activity for human, chimpanzee, and rhesus monkey leukocytes. Chimpanzees or monkeys vaccinated once against hepatitis B with this CpG ODN adjuvant developed 15 times higher anti-hepatitis B Ab titers than those receiving vaccine alone. In conclusion, we report an optimal human CpG motif for phosphorothioate ODN that is a candidate human vaccine adjuvant.




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Infect. Immun.Home page
C. Nonnenmacher, A. Dalpke, S. Zimmermann, L. Flores-de-Jacoby, R. Mutters, and K. Heeg
DNA from Periodontopathogenic Bacteria Is Immunostimulatory for Mouse and Human Immune Cells
Infect. Immun., February 1, 2003; 71(2): 850 - 856.
[Abstract] [Full Text] [PDF]


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Cancer Res.Home page
A. D. Sandler, H. Chihara, G. Kobayashi, X. Zhu, M. A. Miller, D. L. Scott, and A. M. Krieg
CpG Oligonucleotides Enhance the Tumor Antigen-specific Immune Response of a Granulocyte Macrophage Colony-stimulating Factor-based Vaccine Strategy in Neuroblastoma
Cancer Res., January 15, 2003; 63(2): 394 - 399.
[Abstract] [Full Text] [PDF]


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J. Leukoc. Biol.Home page
R. Takauji, S. Iho, H. Takatsuka, S. Yamamoto, T. Takahashi, H. Kitagawa, H. Iwasaki, R. Iida, T. Yokochi, and T. Matsuki
CpG-DNA-induced IFN-{alpha} production involves p38 MAPK-dependent STAT1 phosphorylation in human plasmacytoid dendritic cell precursors
J. Leukoc. Biol., November 1, 2002; 72(5): 1011 - 1019.
[Abstract] [Full Text] [PDF]


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Nucleic Acids ResHome page
D. Yu, E. R. Kandimalla, L. Bhagat, J.-Y. Tang, Y. Cong, J. Tang, and S. Agrawal
'Immunomers'--novel 3'-3'-linked CpG oligodeoxyribonucleotides as potent immunomodulatory agents
Nucleic Acids Res., October 15, 2002; 30(20): 4460 - 4469.
[Abstract] [Full Text] [PDF]


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J. Virol.Home page
A. R. M. Olbrich, S. Schimmer, K. Heeg, K. Schepers, T. N. M. Schumacher, and U. Dittmer
Effective Postexposure Treatment of Retrovirus-Induced Disease with Immunostimulatory DNA Containing CpG Motifs
J. Virol., October 11, 2002; 76(22): 11397 - 11404.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
K. Heckelsmiller, K. Rall, S. Beck, A. Schlamp, J. Seiderer, B. Jahrsdorfer, A. Krug, S. Rothenfusser, S. Endres, and G. Hartmann
Peritumoral CpG DNA Elicits a Coordinated Response of CD8 T Cells and Innate Effectors to Cure Established Tumors in a Murine Colon Carcinoma Model
J. Immunol., October 1, 2002; 169(7): 3892 - 3899.
[Abstract] [Full Text] [PDF]


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J. Virol.Home page
E. M. A. van Rooij, H. L. Glansbeek, L. A. T. Hilgers, E. G. te Lintelo, Y. E. de Visser, W. J. A. Boersma, B. L. Haagmans, and A. T. J. Bianchi
Protective Antiviral Immune Responses to Pseudorabies Virus Induced by DNA Vaccination Using Dimethyldioctadecylammonium Bromide as an Adjuvant
J. Virol., September 11, 2002; 76(20): 10540 - 10545.
[Abstract] [Full Text] [PDF]


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J. Leukoc. Biol.Home page
B. Jahrsdorfer, R. Jox, L. Muhlenhoff, K. Tschoep, A. Krug, S. Rothenfusser, G. Meinhardt, B. Emmerich, S. Endres, and G. Hartmann
Modulation of malignant B cell activation and apoptosis by bcl-2 antisense ODN and immunostimulatory CpG ODN
J. Leukoc. Biol., July 1, 2002; 72(1): 83 - 92.
[Abstract] [Full Text] [PDF]


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J. Virol.Home page
M. Gierynska, U. Kumaraguru, S.-K. Eo, S. Lee, A. Krieg, and B. T. Rouse
Induction of CD8 T-Cell-Specific Systemic and Mucosal Immunity against Herpes Simplex Virus with CpG-Peptide Complexes
J. Virol., June 5, 2002; 76(13): 6568 - 6576.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
V. Hornung, S. Rothenfusser, S. Britsch, A. Krug, B. Jahrsdorfer, T. Giese, S. Endres, and G. Hartmann
Quantitative Expression of Toll-Like Receptor 1-10 mRNA in Cellular Subsets of Human Peripheral Blood Mononuclear Cells and Sensitivity to CpG Oligodeoxynucleotides
J. Immunol., May 1, 2002; 168(9): 4531 - 4537.
[Abstract] [Full Text] [PDF]


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Nucleic Acids ResHome page
D. Yu, E. R. Kandimalla, Q. Zhao, Y. Cong, and S. Agrawal
Immunostimulatory properties of phosphorothioate CpG DNA containing both 3'-5'- and 2'-5'-internucleotide linkages
Nucleic Acids Res., April 1, 2002; 30(7): 1613 - 1619.
[Abstract] [Full Text] [PDF]


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J. Leukoc. Biol.Home page
T.-H. Chuang, J. Lee, L. Kline, J. C. Mathison, and R. J. Ulevitch
Toll-like receptor 9 mediates CpG-DNA signaling
J. Leukoc. Biol., March 1, 2002; 71(3): 538 - 544.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
D. Verthelyi, R. T. Kenney, R. A. Seder, A. A. Gam, B. Friedag, and D. M. Klinman
CpG Oligodeoxynucleotides as Vaccine Adjuvants in Primates
J. Immunol., February 15, 2002; 168(4): 1659 - 1663.
[Abstract] [Full Text] [PDF]


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BloodHome page
T. Decker, S. Hipp, R. J. Kreitman, I. Pastan, C. Peschel, and T. Licht
Sensitization of B-cell chronic lymphocytic leukemia cells to recombinant immunotoxin by immunostimulatory phosphorothioate oligodeoxynucleotides
Blood, February 15, 2002; 99(4): 1320 - 1326.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
Z. K. Ballas, A. M. Krieg, T. Warren, W. Rasmussen, H. L. Davis, M. Waldschmidt, and G. J. Weiner
Divergent Therapeutic and Immunologic Effects of Oligodeoxynucleotides with Distinct CpG Motifs
J. Immunol., November 1, 2001; 167(9): 4878 - 4886.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
F. Takeshita, C. A. Leifer, I. Gursel, K. J. Ishii, S. Takeshita, M. Gursel, and D. M. Klinman
Cutting Edge: Role of Toll-Like Receptor 9 in CpG DNA-Induced Activation of Human Cells
J. Immunol., October 1, 2001; 167(7): 3555 - 3558.
[Abstract] [Full Text] [PDF]


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J. Pharmacol. Exp. Ther.Home page
B. Mui, S. G. Raney, S. C. Semple, and M. J. Hope
Immune Stimulation by a CpG-Containing Oligodeoxynucleotide Is Enhanced When Encapsulated and Delivered in Lipid Particles
J. Pharmacol. Exp. Ther., September 1, 2001; 298(3): 1185 - 1192.
[Abstract] [Full Text] [PDF]


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Cancer Res.Home page
M. Schnurr, P. Galambos, C. Scholz, F. Then, M. Dauer, S. Endres, and A. Eigler
Tumor Cell Lysate-pulsed Human Dendritic Cells Induce a T-Cell Response against Pancreatic Carcinoma Cells: an in Vitro Model for the Assessment of Tumor Vaccines
Cancer Res., September 1, 2001; 61(17): 6445 - 6450.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
B. E. Britigan, T. S. Lewis, M. Waldschmidt, M. L. McCormick, and A. M. Krieg
Lactoferrin Binds CpG-Containing Oligonucleotides and Inhibits Their Immunostimulatory Effects on Human B Cells
J. Immunol., September 1, 2001; 167(5): 2921 - 2928.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
C. Neufert, R. K. Pai, E. H. Noss, M. Berger, W. H. Boom, and C. V. Harding
Mycobacterium tuberculosis 19-kDa Lipoprotein Promotes Neutrophil Activation
J. Immunol., August 1, 2001; 167(3): 1542 - 1549.
[Abstract] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
S. Bauer, C. J. Kirschning, H. Hacker, V. Redecke, S. Hausmann, S. Akira, H. Wagner, and G. B. Lipford
Human TLR9 confers responsiveness to bacterial DNA via species-specific CpG motif recognition
PNAS, July 19, 2001; (2001) 161293498.
[Abstract] [Full Text] [PDF]


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Infect. Immun.Home page
T. D. Crabtree, L. Jin, D. P. Raymond, S. J. Pelletier, C. W. Houlgrave, T. G. Gleason, T. L. Pruett, and R. G. Sawyer
Preexposure of Murine Macrophages to CpG Oligonucleotide Results in a Biphasic Tumor Necrosis Factor Alpha Response to Subsequent Lipopolysaccharide Challenge
Infect. Immun., April 1, 2001; 69(4): 2123 - 2129.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
N. Kadowaki, S. Antonenko, and Y.-J. Liu
Distinct CpG DNA and Polyinosinic-Polycytidylic Acid Double-Stranded RNA, Respectively, Stimulate CD11c- Type 2 Dendritic Cell Precursors and CD11c+ Dendritic Cells to Produce Type I IFN
J. Immunol., February 15, 2001; 166(4): 2291 - 2295.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
D. Verthelyi, K. J. Ishii, M. Gursel, F. Takeshita, and D. M. Klinman
Human Peripheral Blood Cells Differentially Recognize and Respond to Two Distinct CpG Motifs
J. Immunol., February 15, 2001; 166(4): 2372 - 2377.
[Abstract] [Full Text] [PDF]


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J. Leukoc. Biol.Home page
B. Jahrsdörfer, G. Hartmann, E. Racila, W. Jackson, L. Mühlenhoff, G. Meinhardt, S. Endres, B. K. Link, A. M. Krieg, and G. J. Weiner
CpG DNA increases primary malignant B cell expression of costimulatory molecules and target antigens
J. Leukoc. Biol., January 1, 2001; 69(1): 81 - 88.
[Abstract] [Full Text]


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J. Leukoc. Biol.Home page
G. J. Weiner
The immunobiology and clinical potential of immunostimulatory CpG oligodeoxynucleotides
J. Leukoc. Biol., October 1, 2000; 68(4): 455 - 463.
[Abstract] [Full Text]


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J. Immunol.Home page
S. W. Lee, M. K. Song, K. H. Baek, Y. Park, J. K. Kim, C. H. Lee, H.-K. Cheong, C. Cheong, and Y. C. Sung
Effects of a Hexameric Deoxyriboguanosine Run Conjugation into CpG Oligodeoxynucleotides on Their Immunostimulatory Potentials
J. Immunol., October 1, 2000; 165(7): 3631 - 3639.
[Abstract] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
S. Bauer, C. J. Kirschning, H. Hacker, V. Redecke, S. Hausmann, S. Akira, H. Wagner, and G. B. Lipford
Human TLR9 confers responsiveness to bacterial DNA via species-specific CpG motif recognition
PNAS, July 31, 2001; 98(16): 9237 - 9242.
[Abstract] [Full Text] [PDF]




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