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PMID: 15860583 Published · ppublish English Journal Article

Immunomodulatory oligonucleotides containing a cytosine-phosphate-2'-deoxy-7-deazaguanosine motif as potent toll-like receptor 9 agonists.

Kandimalla ER, Bhagat L, Li Y, Yu D, Wang D, Cong YP, Song SS, Tang JX, Sullivan T, Agrawal S

Abstract

Bacterial DNA and synthetic oligomers containing CpG dinucleotides activate the immune system through Toll-like receptor (TLR) 9. Here, we compare the immunostimulatory activity of three immunomers with different nucleotide sequences containing a synthetic cytosine-phosphate-2'-deoxy-7-deazaguanosine dinucleotide (CpR), called immunomodulatory oligonucleotides (IMOs), in mouse, human, and monkey systems. IMOs induced IL-12 and IFN-gamma secretion more than a control non-CpG IMO in mice. All three IMOs activated HEK293 cells expressing TLR9 but not TLR3, -7, or -8. IMOs induced human B-cell proliferation and enhanced expression of CD86 and CD69 surface markers on B cells. The three IMOs induced CD86 expression on human plasmacytoid dendritic cells, but only IMOs that contained a 5'-terminal TCR nucleotide sequence induced IFN-alpha secretion. A sequence that forms a duplex structure also was required for IFN-alpha induction in human peripheral blood mononuclear cell cultures. IMOs induced chemokine and cytokine gene expression in human peripheral blood mononuclear cells. In monkeys, all three IMOs induced transient changes in peripheral blood leukocytes and lymphocytes and activated B and T lymphocytes. All three IMOs induced IFN-alpha in vivo in monkeys; the IMO sequence that forms a stable secondary structure induced the highest levels of IFN-alpha. These studies are, to our knowledge, the first comprehensive studies to compare the activity of IMOs containing synthetic stimulatory CpR dinucleotides in mouse, monkey, and human systems. These results suggest that IMOs induce strong and rapid immunostimulation and that the CpR dinucleotide is recognized by TLR9, leading to immune-cell activation and cytokine secretion in vitro and in vivo.

MeSH Terms
Animals Antigens, CD/biosynthesis Antigens, Differentiation, T-Lymphocyte/biosynthesis B-Lymphocytes/cytology,metabolism B7-2 Antigen Base Sequence Cell Line Cell Proliferation Chemokines/metabolism CpG Islands Cytokines/chemistry,metabolism DNA-Binding Proteins/agonists Dendritic Cells/cytology Deoxyguanosine/analogs & derivatives,chemistry Dose-Response Relationship, Drug Enzyme-Linked Immunosorbent Assay Female Flow Cytometry Gene Expression Regulation Haplorhini Humans Interferon-gamma/metabolism Interleukin-12/metabolism Lectins, C-Type Leukocytes, Mononuclear/metabolism Lymphocytes/metabolism Membrane Glycoproteins/biosynthesis,metabolism Mice Mice, Inbred C57BL Molecular Sequence Data Nucleotides/chemistry Oligonucleotides/chemistry Protein Binding RNA, Messenger/metabolism Receptors, Cell Surface/agonists,metabolism Time Factors Toll-Like Receptor 3 Toll-Like Receptor 9 Toll-Like Receptors Up-Regulation
Chemicals
Antigens, CD Antigens, Differentiation, T-Lymphocyte B7-2 Antigen CD69 antigen CD86 protein, human Cd86 protein, mouse Chemokines Cytokines DNA-Binding Proteins Lectins, C-Type Membrane Glycoproteins Nucleotides Oligonucleotides RNA, Messenger Receptors, Cell Surface TLR3 protein, human TLR9 protein, human Tlr9 protein, mouse Toll-Like Receptor 3 Toll-Like Receptor 9 Toll-Like Receptors Interleukin-12 7-deaza-2'-deoxyguanosine Interferon-gamma Deoxyguanosine
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Kandimalla Ekambar R
Hybridon, Inc., 345 Vassar Street, Cambridge, MA 02139, USA.
Bhagat Lakshmi
Li Yukui
Yu Dong
Wang Daqing
Cong Yan-Ping
Song Sam S
Tang Jimmy X
Sullivan Tim
Agrawal Sudhir
References (37)
37 references, click to expand
  1. Site of chemical modifications in CpG containing phosphorothioate oligodeoxynucleotide modulates its immunostimulatory activity.
    Bioorg Med Chem Lett. 1999 Dec 20;9(24):3453-8 PMID: 10617090
  2. CpG oligonucleotides with modified termini and nicked dumbbell structure show enhanced immunostimulatory activity.
    J Med Chem. 2003 Nov 6;46(23):5031-44 PMID: 14584953
  3. A Toll-like receptor recognizes bacterial DNA.
    Nature. 2000 Dec 7;408(6813):740-5 PMID: 11130078
  4. Accessible 5'-end of CpG-containing phosphorothioate oligodeoxynucleotides is essential for immunostimulatory activity.
    Bioorg Med Chem Lett. 2000 Dec 4;10(23):2585-8 PMID: 11128629
  5. Human peripheral blood cells differentially recognize and respond to two distinct CPG motifs.
    J Immunol. 2001 Feb 15;166(4):2372-7 PMID: 11160295
  6. Modulation of immunostimulatory activity of CpG oligonucleotides by site-specific deletion of nucleobases.
    Bioorg Med Chem Lett. 2001 Sep 3;11(17):2263-7 PMID: 11527711
  7. Immunostimulatory activity of CpG oligonucleotides containing non-ionic methylphosphonate linkages.
    Bioorg Med Chem. 2001 Nov;9(11):2803-8 PMID: 11597460
  8. Immunostimulatory properties of phosphorothioate CpG DNA containing both 3'-5'- and 2'-5'-internucleotide linkages.
    Nucleic Acids Res. 2002 Apr 1;30(7):1613-9 PMID: 11917022
  9. Antisense and/or immunostimulatory oligonucleotide therapeutics.
    Curr Cancer Drug Targets. 2001 Nov;1(3):197-209 PMID: 12188879
  10. Potent CpG oligonucleotides containing phosphodiester linkages: in vitro and in vivo immunostimulatory properties.
    Biochem Biophys Res Commun. 2002 Sep 13;297(1):83-90 PMID: 12220512
  11. Conjugation of ligands at the 5'-end of CpG DNA affects immunostimulatory activity.
    Bioconjug Chem. 2002 Sep-Oct;13(5):966-74 PMID: 12236778
  12. Design, synthesis, and immunostimulatory properties of CpG DNAs containing alkyl-linker substitutions: role of nucleosides in the flanking sequences.
    J Med Chem. 2002 Sep 26;45(20):4540-8 PMID: 12238933
  13. 'Immunomers'--novel 3'-3'-linked CpG oligodeoxyribonucleotides as potent immunomodulatory agents.
    Nucleic Acids Res. 2002 Oct 15;30(20):4460-9 PMID: 12384593
  14. A dinucleotide motif in oligonucleotides shows potent immunomodulatory activity and overrides species-specific recognition observed with CpG motif.
    Proc Natl Acad Sci U S A. 2003 Nov 25;100(24):14303-8 PMID: 14610275
  15. Novel immunomodulatory oligonucleotides prevent development of allergic airway inflammation and airway hyperresponsiveness in asthma.
    Int Immunopharmacol. 2004 Jan;4(1):127-38 PMID: 14975367
  16. Immunopharmacological and antitumor effects of second-generation immunomodulatory oligonucleotides containing synthetic CpR motifs.
    Int J Oncol. 2004 Apr;24(4):901-8 PMID: 15010828
  17. Immunotherapeutic uses of CpG oligodeoxynucleotides.
    Nat Rev Immunol. 2004 Apr;4(4):249-58 PMID: 15057783
  18. Antitumor activity of deoxyribonucleic acid fraction from Mycobacterium bovis BCG. I. Isolation, physicochemical characterization, and antitumor activity.
    J Natl Cancer Inst. 1984 Apr;72(4):955-62 PMID: 6200641
  19. In vitro augmentation of natural killer cell activity and production of interferon-alpha/beta and -gamma with deoxyribonucleic acid fraction from Mycobacterium bovis BCG.
    Jpn J Cancer Res. 1988 Jul;79(7):866-73 PMID: 2459094
  20. Acute hematologic effects of interferon alpha, interferon gamma, tumor necrosis factor alpha and interleukin 2.
    Ann Hematol. 1991 Feb;62(1):25-31 PMID: 1903309
  21. Stimulation of in vitro murine lymphocyte proliferation by bacterial DNA.
    J Immunol. 1991 Sep 15;147(6):1759-64 PMID: 1890302
  22. CpG motifs in bacterial DNA trigger direct B-cell activation.
    Nature. 1995 Apr 6;374(6522):546-9 PMID: 7700380
  23. Effect of different chemically modified oligodeoxynucleotides on immune stimulation.
    Biochem Pharmacol. 1996 Jan 26;51(2):173-82 PMID: 8615886
  24. CpG motifs present in bacteria DNA rapidly induce lymphocytes to secrete interleukin 6, interleukin 12, and interferon gamma.
    Proc Natl Acad Sci U S A. 1996 Apr 2;93(7):2879-83 PMID: 8610135
  25. Immunostimulatory DNA sequences necessary for effective intradermal gene immunization.
    Science. 1996 Jul 19;273(5273):352-4 PMID: 8662521
  26. Macrophages ingest and are activated by bacterial DNA.
    J Immunol. 1996 Sep 1;157(5):2116-22 PMID: 8757335
  27. Pattern and kinetics of cytokine production following administration of phosphorothioate oligonucleotides in mice.
    Antisense Nucleic Acid Drug Dev. 1997 Oct;7(5):495-502 PMID: 9361908
  28. Rapid induction of mitogen-activated protein kinases by immune stimulatory CpG DNA.
    J Immunol. 1998 Nov 1;161(9):4493-7 PMID: 9794373
  29. Effect of chemical modifications of cytosine and guanine in a CpG-motif of oligonucleotides: structure-immunostimulatory activity relationships.
    Bioorg Med Chem. 2001 Mar;9(3):807-13 PMID: 11310616
  30. Interleukin 12 immunotherapy after autologous stem cell transplantation for hematological malignancies.
    Clin Cancer Res. 2002 Nov;8(11):3383-93 PMID: 12429625
  31. Requirement of nucleobase proximal to CpG dinucleotide for immunostimulatory activity of synthetic CpG DNA.
    Bioorg Med Chem. 2003 Feb 6;11(3):459-64 PMID: 12517441
  32. CpG penta- and hexadeoxyribonucleotides as potent immunomodulatory agents.
    Biochem Biophys Res Commun. 2003 Jan 24;300(4):853-61 PMID: 12559951
  33. Divergent synthetic nucleotide motif recognition pattern: design and development of potent immunomodulatory oligodeoxyribonucleotide agents with distinct cytokine induction profiles.
    Nucleic Acids Res. 2003 May 1;31(9):2393-400 PMID: 12711684
  34. Identification of a novel CpG DNA class and motif that optimally stimulate B cell and plasmacytoid dendritic cell functions.
    J Leukoc Biol. 2003 Jun;73(6):781-92 PMID: 12773511
  35. Rational design of new CpG oligonucleotides that combine B cell activation with high IFN-alpha induction in plasmacytoid dendritic cells.
    Eur J Immunol. 2003 Jun;33(6):1633-41 PMID: 12778481
  36. Novel chimeric immunomodulatory compounds containing short CpG oligodeoxyribonucleotides have differential activities in human cells.
    Nucleic Acids Res. 2003 Sep 1;31(17):5122-33 PMID: 12930963
  37. Immunostimulatory activity of CpG containing phosphorothioate oligodeoxynucleotide is modulated by modification of a single deoxynucleoside.
    Bioorg Med Chem Lett. 2000 May 15;10(10):1051-4 PMID: 10843214
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2005-05-10
Epub
2005-00-28
Pages
6925-30
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC1100782
Subset
IM
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