Home LiteratureArticle Details
PMID: 22231700 Published · ppublish English Journal Article Research Support, N.I.H., Intramural

Intratumoral injection of CpG oligonucleotides induces the differentiation and reduces the immunosuppressive activity of myeloid-derived suppressor cells.

Journal of immunology (Baltimore, Md. : 1950) ·Vol. 188 ·No. 4 ·2012-02-15 ·Pages 1592-9

Shirota Y, Shirota H, Klinman DM

Abstract

Immunostimulatory CpG oligonucleotides (ODN) activate cells that express TLR9 and have been shown to improve the host's response to tumor Ags. Unfortunately, the immunosuppressive microenvironment that surrounds many cancers inhibits Ag-specific cellular responses and thus interferes with CpG-mediated immunotherapy. Myeloid-derived suppressor cells (MDSC) represent an important constituent of this immunosuppressive milieu. Large numbers of MDSC are present in and near tumor sites where they inhibit the activity of Ag-specific T and NK cells. Current studies indicate that the delivery of CpG ODN directly into the tumor bed reduces the immunosuppressive activity of monocytic (CD11b(+), Ly6G(-), Ly6C(high)) MDSC. Monocytic MDSC express TLR9 and respond to CpG stimulation by 1) losing their ability to suppress T cell function, 2) producing Th1 cytokines, and 3) differentiating into macrophages with tumoricidal capability. These findings provide insight into a novel mechanism by which CpG ODN contribute to tumor regression, and they support intratumoral injection as the optimal route for their delivery.

MeSH Terms
Animals Cell Differentiation Cytokines/biosynthesis Dendritic Cells/immunology Immune Tolerance Immunity, Innate/drug effects Injections, Intralesional Killer Cells, Natural/immunology Macrophages/drug effects,immunology,metabolism Mice Mice, Inbred BALB C Mice, Inbred C57BL Myeloid Cells/immunology Neoplasms/immunology Oligodeoxyribonucleotides/administration & dosage,immunology T-Lymphocytes/metabolism T-Lymphocytes, Cytotoxic/immunology Toll-Like Receptor 9/biosynthesis Tumor Microenvironment/immunology
Chemicals
CPG-oligonucleotide Cytokines Oligodeoxyribonucleotides Toll-Like Receptor 9
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Shirota Yuko
Cancer and Inflammation Program, National Cancer Institute, Frederick, MD 21702, USA.
Shirota Hidekazu
Klinman Dennis M
References (40)
40 references, click to expand
  1. CPG-7909 (PF-3512676, ProMune): toll-like receptor-9 agonist in cancer therapy.
    Expert Opin Biol Ther. 2007 Aug;7(8):1257-66 PMID: 17696823
  2. Myeloid-derived suppressor cells prevent type 1 diabetes in murine models.
    J Immunol. 2010 Nov 15;185(10):5828-34 PMID: 20956337
  3. Phosphodiesterase-5 inhibition augments endogenous antitumor immunity by reducing myeloid-derived suppressor cell function.
    J Exp Med. 2006 Nov 27;203(12):2691-702 PMID: 17101732
  4. Regulation of immune responses by L-arginine metabolism.
    Nat Rev Immunol. 2005 Aug;5(8):641-54 PMID: 16056256
  5. Immunotherapeutic uses of CpG oligodeoxynucleotides.
    Nat Rev Immunol. 2004 Apr;4(4):249-58 PMID: 15057783
  6. NK- and CD8(+) T cell-mediated eradication of established tumors by peritumoral injection of CpG-containing oligodeoxynucleotides.
    J Immunol. 2001 Nov 1;167(9):5247-53 PMID: 11673539
  7. Hierarchy of immunosuppressive strength among myeloid-derived suppressor cell subsets is determined by GM-CSF.
    Eur J Immunol. 2010 Jan;40(1):22-35 PMID: 19941314
  8. CpG blocks immunosuppression by myeloid-derived suppressor cells in tumor-bearing mice.
    Clin Cancer Res. 2011 Apr 1;17(7):1765-75 PMID: 21233400
  9. Myeloid-derived suppressor cells: linking inflammation and cancer.
    J Immunol. 2009 Apr 15;182(8):4499-506 PMID: 19342621
  10. CpG oligodeoxynucleotides as TLR9 agonists: therapeutic applications in cancer.
    BioDrugs. 2009;23(6):361-75 PMID: 19894778
  11. Immune-mediated tumor regression induced by CpG-containing oligodeoxynucleotides.
    Clin Cancer Res. 2003 Jul;9(7):2693-700 PMID: 12855649
  12. Reversal of tumor-induced dendritic cell paralysis by CpG immunostimulatory oligonucleotide and anti-interleukin 10 receptor antibody.
    J Exp Med. 2002 Aug 19;196(4):541-9 PMID: 12186845
  13. A Toll-like receptor recognizes bacterial DNA.
    Nature. 2000 Dec 7;408(6813):740-5 PMID: 11130078
  14. Potential of transfected muscle cells to contribute to DNA vaccine immunogenicity.
    J Immunol. 2007 Jul 1;179(1):329-36 PMID: 17579053
  15. Antitumor activity mediated by CpG: the route of administration is critical.
    J Immunother. 2011 Apr;34(3):279-88 PMID: 21389870
  16. Arginine regulation by myeloid derived suppressor cells and tolerance in cancer: mechanisms and therapeutic perspectives.
    Immunol Rev. 2008 Apr;222:180-91 PMID: 18364002
  17. Myeloid-derived suppressor cells as regulators of the immune system.
    Nat Rev Immunol. 2009 Mar;9(3):162-74 PMID: 19197294
  18. Gemcitabine directly inhibits myeloid derived suppressor cells in BALB/c mice bearing 4T1 mammary carcinoma and augments expansion of T cells from tumor-bearing mice.
    Int Immunopharmacol. 2009 Jul;9(7-8):900-9 PMID: 19336265
  19. A potential role of macrophage activation in the treatment of cancer.
    Crit Rev Oncol Hematol. 2002 Nov;44(2):143-61 PMID: 12413632
  20. Phase 1 evaluation of intralesionally injected TLR9-agonist PF-3512676 in patients with basal cell carcinoma or metastatic melanoma.
    J Immunother. 2008 Jun;31(5):520-7 PMID: 18463532
  21. Local administration of PF-3512676 CpG-B instigates tumor-specific CD8+ T-cell reactivity in melanoma patients.
    Clin Cancer Res. 2008 Jul 15;14(14):4532-42 PMID: 18628468
  22. Cancer related inflammation: the macrophage connection.
    Cancer Lett. 2008 Aug 28;267(2):204-15 PMID: 18448242
  23. Sunitinib mediates reversal of myeloid-derived suppressor cell accumulation in renal cell carcinoma patients.
    Clin Cancer Res. 2009 Mar 15;15(6):2148-57 PMID: 19276286
  24. Immunotherapeutic applications of CpG oligodeoxynucleotide TLR9 agonists.
    Adv Drug Deliv Rev. 2009 Mar 28;61(3):195-204 PMID: 19211030
  25. Increased circulating myeloid-derived suppressor cells correlate with clinical cancer stage, metastatic tumor burden, and doxorubicin-cyclophosphamide chemotherapy.
    Cancer Immunol Immunother. 2009 Jan;58(1):49-59 PMID: 18446337
  26. Mechanism of all-trans retinoic acid effect on tumor-associated myeloid-derived suppressor cells.
    Cancer Res. 2007 Nov 15;67(22):11021-8 PMID: 18006848
  27. CpG-conjugated apoptotic tumor cells elicit potent tumor-specific immunity.
    Cancer Immunol Immunother. 2011 May;60(5):659-69 PMID: 21318638
  28. Targeting the mechanisms of tumoral immune tolerance with small-molecule inhibitors.
    Nat Rev Cancer. 2006 Aug;6(8):613-25 PMID: 16862192
  29. 5-Fluorouracil selectively kills tumor-associated myeloid-derived suppressor cells resulting in enhanced T cell-dependent antitumor immunity.
    Cancer Res. 2010 Apr 15;70(8):3052-61 PMID: 20388795
  30. Therapeutic targeting of myeloid-derived suppressor cells.
    Curr Opin Pharmacol. 2009 Aug;9(4):470-81 PMID: 19616475
  31. 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. 2002 Oct 1;169(7):3892-9 PMID: 12244187
  32. Therapeutic applications of synthetic CpG oligodeoxynucleotides as TLR9 agonists for immune modulation.
    BioDrugs. 2007;21(6):387-401 PMID: 18020622
  33. In situ vaccination with a TLR9 agonist induces systemic lymphoma regression: a phase I/II study.
    J Clin Oncol. 2010 Oct 1;28(28):4324-32 PMID: 20697067
  34. TLR ligands in the local treatment of established intracerebral murine gliomas.
    J Immunol. 2008 Nov 15;181(10):6720-9 PMID: 18981089
  35. Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm.
    Nat Immunol. 2010 Oct;11(10):889-96 PMID: 20856220
  36. The role of myeloid cells in the promotion of tumour angiogenesis.
    Nat Rev Cancer. 2008 Aug;8(8):618-31 PMID: 18633355
  37. Cancer despite immunosurveillance: immunoselection and immunosubversion.
    Nat Rev Immunol. 2006 Oct;6(10):715-27 PMID: 16977338
  38. Randomized phase 2/3 trial of CpG oligodeoxynucleotide PF-3512676 alone or with dacarbazine for patients with unresectable stage III and IV melanoma.
    Cancer. 2009 Sep 1;115(17):3944-54 PMID: 19536884
  39. Cancer-expanded myeloid-derived suppressor cells induce anergy of NK cells through membrane-bound TGF-beta 1.
    J Immunol. 2009 Jan 1;182(1):240-9 PMID: 19109155
  40. CpG motifs in bacterial DNA trigger direct B-cell activation.
    Nature. 1995 Apr 6;374(6522):546-9 PMID: 7700380
Article Info
Journal
Journal of immunology (Baltimore, Md. : 1950)
Abbr.
J Immunol
ISSN
1550-6606
Published
2012-02-15
Epub
2012-00-09
Pages
1592-9
Language
English
Region
United States
NLM ID
2985117R
PMCID
PMC3273593
Subset
IM
Grants
Intramural NIH HHS · ZIA BC010852-04 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com