Therapeutic injection of C-class CpG ODN in draining lymph node area induces potent activation of immune cells and rejection of established breast cancer in mice

Clinical Immunology

Volumn 131, Issue 3, 2009, Pages 426-437

  Yang, Liang ^a   Sun, Luguo ^a   Wu, Xiuli ^a   Wang, Li ^a   Wei, Hongfei ^a   Wan, Min ^a   Zhang, Peiyin ^a   Yu, Yongli ^a   Wang, Liying ^a  

^a Basic Medical College   (China)

Author keywords

Breast cancer; CpG ODN; Draining lymph nodes; Immunity

Indexed keywords

CD19 ANTIGEN; CD69 ANTIGEN; CPG OLIGODEOXYNUCLEOTIDE; GLYCOPROTEIN P 15095; UNCLASSIFIED DRUG; YW 001; YW 002;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST CANCER; CANCER INHIBITION; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL ACTIVATION; CELL INFILTRATION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOTOXICITY; DOSE RESPONSE; DRUG EFFICACY; DRUG POTENCY; FEMALE; FLOW CYTOMETRY; GROWTH INHIBITION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOLOGICAL MEMORY; IMMUNOSTIMULATION; LYMPH NODE; MONOTHERAPY; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPLEEN; SURVIVAL; TREATMENT PLANNING; TUMOR DRAINING LYMPH NODE; TUMOR GROWTH;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; BREAST NEOPLASMS; CELL LINE; CERCOPITHECUS AETHIOPS; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; LEUKOCYTES, MONONUCLEAR; LYMPH NODES; MICE; MICE, INBRED BALB C; OLIGODEOXYRIBONUCLEOTIDES; SPLEEN; VERO CELLS;

EID: 67349183328     PISSN: 15216616     EISSN: 15217035     Source Type: Journal    
DOI: 10.1016/j.clim.2009.01.011     Document Type: Article

References (41)

1. Verthelyi D., Ishii K.J., Gursel M., Takeshita F., and Klinman D.M. Human peripheral blood cells differentially recognize and respond to two distinct CpG motifs. J. Immunol. 166 (2001) 2372-2377
2. Marshall J.D., Fearon K., Abbate C., Subramanian S., Yee P., Gregorio J., Coffman R.L., and Van Nest G. Identification of a novel CpG DNA class and motif that optimally stimulate B cell and plasmacytoid dendritic cell functions. J. Leukoc. Biol. 73 (2003) 781-792
3. Vollmer J., Weeratna R., Payette P., Jurk M., Schetter C., Laucht M., Wader T., Tluk S., Liu M., Davis H.L., and Krieg A.M. Characterization of three CpG oligodeoxynucleotide classes with distinct immunostimulatory activities. Eur. J. Immunol. 34 (2004) 251-262
4. Krieg A.M. Therapeutic potential of Toll-like receptor 9 activation. Nat. Rev., Drug Discov. 5 (2006) 471-484
5. Krieg A.M. Development of TLR9 agonists for cancer therapy. J. Clin. Invest. 117 (2007) 1184-1194
6. Krieg A.M. Toll-like receptor 9 (TLR9) agonists in the treatment of cancer. Oncogene 27 (2008) 161-167
7. Carpentier A.F., Xie J., Mokhtari K., and Delattre J.Y. Successful treatment of intracranial gliomas in rat by oligodeoxynucleotides containing CpG motifs. Clin. Cancer Res. 6 (2000) 2469-2473
8. Lonsdorf A.S., Kuekrek H., Stern B.V., Boehm B.O., Lehmann P.V., and Tary-Lehmann M. Intratumor CpG-oligodeoxynucleotide injection induces protective antitumor T cell immunity. J. Immunol. 171 (2003) 3941-3946
9. Heckelsmiller K., Rall K., Beck S., Schlamp A., Seiderer J., Jahrsdorfer B., Krug A., Rothenfusser S., Endres S., and Hartmann G. 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. 169 (2002) 3892-3899
10. Sfondrini L., Besusso D., Rumio C., Rodolfo M., Menard S., and Balsari A. Prevention of spontaneous mammary adenocarcinoma in HER-2/neu transgenic mice by foreign DNA. FASEB J. 16 (2002) 1749-1754
11. Kawarada Y., Ganss R., Garbi N., Sacher T., Arnold B., and Hammerling G.J. NK- and CD8(+) T cell-mediated eradication of established tumors by peritumoral injection of CpG-containing oligodeoxynucleotides. J. Immunol. 167 (2001) 5247-5253
12. Carpentier A., Laigle-Donadey F., Zohar S., Capelle L., Behin A., Tibi A., Martin-Duverneuil N., Sanson M., Lacomblez L., Taillibert S., Puybasset L., Van Effenterre R., Delattre J.Y., and Carpentier A.F. Phase 1 trial of a CpG oligodeoxynucleotide for patients with recurrent glioblastoma. Neuro-Oncol. 8 (2006) 60-66
13. Pashenkov M., Goess G., Wagner C., Hormann M., Jandl T., Moser A., Britten C.M., Smolle J., Koller S., Mauch C., Tantcheva-Poor I., Grabbe S., Loquai C., Esser S., Franckson T., Schneeberger A., Haarmann C., Krieg A.M., Stingl G., and Wagner S.N. Phase II trial of a Toll-like receptor 9-activating oligonucleotide in patients with metastatic melanoma. J. Clin. Oncol. 24 (2006) 5716-5724
14. Thompson J.A., Kuzel T., Bukowski R., Masciari F., and Schmalbach T. Phase lb trial of a targeted TLR9 CpG immunomodulator (CPG 7909) in advanced renal cell carcinoma (RCC). J. Clin. Oncol. 22 (2004) 417S
15. Mellor A.L., Baban B., Chandler P.R., Manlapat A., Kahler D.J., and Munn D.H. Cutting edge: CpG oligonucleotides induce splenic CD19(+) dendritic cells to acquire potent indoleamine 2,3-dioxygenase-dependent T cell regulatory functions via IFN type 1 signaling. J. Immunol. 175 (2005) 5601-5605
16. Wingender G., Garbi N., Schumak B., Jungerkes F., Endl E., von Bulnoff D., Steitz J., Striegler J., Moldenhauer G., Tuting T., Heit A., Huster K.M., Takikawa O., Akira S., Busch D.H., Wagner H., Hammerling G.J., Knolle P.A., and Limmer A. Systemic application of CpG-rich DNA suppresses adaptive T cell immunity via induction of IDO. Eur. J. Immunol. 36 (2006) 12-20
17. Molenkamp B.G., van Leeuwen P.A.M., Meijer S., Sluijter B.J.R., Wijnands P.G.J.T., Baars A., van den Eertwegh A.J.M., Scheper R.J., and de Grujil T.D. Intradermal CpG-B activates both plasmacytoid and myeloid dendritic cells in the sentinel lymph node of melanoma patients. Clin. Cancer Res. 13 (2007) 2961-2969
18. Kim R., Emi M., Tanabe K., and Arihiro K. Immunobiology of the sentinel lymph node and its potential role for antitumour immunity. Lancet Oncol. 7 (2006) 1006-1016
19. Inoue M., Plautz G.E., and Shu S. Treatment of intracranial tumors by systemic transfer of superantigen-activated tumor-draining lymph node T cells. Cancer Res. 56 (1996) 4702-4708
20. Poindexter N.J., Sahin A., Hunt K.K., and Grimm E.A. Analysis of dendritic cells in tumor-free and tumor-containing sentinel lymph nodes from patients with breast cancer. Breast Cancer Res. 6 (2004) R408-R415
21. Hartmann E., Wollenberg B., Rothenfusser S., Wagner M., Wellisch D., Mack B., Giese T., Gires O., Endres S., and Hartmann G. Identification and functional analysis of tumor-infiltrating plasmacytoid dendritic cells in head and neck cancer. Cancer Res. 63 (2003) 6478-6487
22. Liyanage U.K., Moore T.T., Joo H.G., Tanaka Y., Herrmann V., Doherty G., Drebin J.A., Strasberg S.M., Eberlein T.J., Goedegebuure P.S., and Linehan D.C. Prevalence of regulatory T cells is increased in peripheral blood and tumor microenvironment of patients with pancreas or breast adenocarcinoma. J. Immunol. 169 (2002) 2756-2761
23. Nathanson S.D. Insights into the mechanisms of lymph node metastasis. Cancer 98 (2003) 413-423
24. Munn D.H., and Mellor A.L. The tumor-draining lymph node as an immune-privileged site. Immunol. Rev. 213 (2006) 146-158
25. Molenkamp B.G., van Leeuwen P.A.M., van den Eertwegh A.J.M., Sluijter B.J.R., Scheper R.J., Meijer S., and de Gruijl T.D. Immunomodulation of the melanoma sentinel lymph node: a novel adjuvant therapeutic option. Immunobiology 211 (2006) 651-661
26. Bao M.S., Zhang Y., Wan M., Dai L., Hu X.P., Wu X.L., Wang L., Deng P., Wang J.Z., Chen J.Z., Liu Y.J., Yu Y.L., and Wang L.Y. Anti-SARS-CoV immunity induced by a novel CpG oligodeoxynucleotide. Clin. Immunol. 118 (2006) 180-187
27. Wang X.J., Bao M.S., Wan M., Wei H.F., Wang L., Yu H.T., Zhang X.S., Yu Y.L., and Wang L.Y. A CpG oligodeoxynucleotide acts as a potent adjuvant for inactivated rabies virus vaccine. Vaccine 26 (2008) 1893-1901
28. Carpentier A.F., Chen L., Maltonti F., and Delattre J.Y. Oligodeoxynucleotides containing CpG motifs can induce rejection of a neuroblastoma in mice. Cancer Res. 59 (1999) 5429-5432
29. Li D.P., Li H., Zhang P.Y., Wu X.L., Wei H.F., Wang L., Wan M., Deng P., Zhang Y., Wang J.Z., Liu Y.J., Yu Y.L., and Wang L.Y. Heat shock fusion protein induces both specific and nonspecific anti-tumor immunity. Eur. J. Immunol. 36 (2006) 1324-1336
30. Ballas Z.K., Krieg A.M., Warren T., Rasmussen W., Davis H.L., Waldschmidt M., and Weiner G.J. Divergent therapeutic and immunologic effects of oligodeoxynucleotides with distinct CpG motifs. J. Immunol. 167 (2001) 4878-4886
31. Maurer T., Heit A., Hochrein H., Ampenberger F., O'Keeffe M., Bauer S., Lipford G.B., Vabulas R.M., and Wagner H. CpG-DNA aided cross-presentation of soluble antigens by dendritic cells. Eur. J. Immunol. 32 (2002) 2356-2364
32. Heit A., Huster K.M., Schmitz F., Schiemann M., Busch D.H., and Wagner H. CpG-DNA aided cross-priming by cross-presenting B cells. J. Immunol. 172 (2004) 1501-1507
33. van Ojik H.H., Bevaart L., Dahle C.E., Bakker A., Jansen M.J.H., van Vugt M.J., van de Winkel J.G.J.V., and Weiner G.J. CpG-A and B oligodeoxynucleotides enhance the efficacy of antibody therapy by activating different effector cell populations. Cancer Res. 63 (2003) 5595-5600
34. Cong Z., Wan M., Wu X.L., Wang L., Hu X.P., Yang F.L., Bao M.S., Zhang X.S., Chen J.Z., Wang L.Y., and Yu Y.L. A CpG oligodeoxynucleotide inducing anti-coxsackie B3 virus activity in human peripheral blood mononuclear cells. FEMS Immunol. Med. Microbiol. 51 (2007) 26-34
35. Jonasch E., and Haluska F.G. Interferon in oncological practice: review of interferon biology, clinical applications, and toxicities. Oncologist 6 (2001) 34-55
36. Krug A., Rothenfusser S., Selinger S., Bock C., Kerkmann M., Battiany J., Sarris A., Giese T., Speiser D., Endres S., and Hartmann G. CpG-A oligonucleotides induce a monocyte-derived dendritic cell-like phenotype that preferentially activates CD8 T cells. J. Immunol. 170 (2003) 3468-3477
37. Nakano H., Yanagita M., and Gunn M.D. CD11c(+)B220(+)Gr-1(+) cells in mouse lymph nodes and spleen display characteristics of plasmacytoid dendritic cells. J. Exp. Med. 194 (2001) 1171-1178
38. Colonna M., Trinchieri G., and Liu Y.J. Plasmacytoid dendritic cells in immunity. Nat. Immunol. 5 (2004) 1219-1226
39. Le Bon A., Etchart N., Rossmann C., Ashton M., Hou S., Gewert D., Borrow P., and Tough D.F. Cross-priming of CD8(+) T cells stimulated by virus-induced type I interferon. Nat. Immunol. 4 (2003) 1009-1015
40. Kuchtey J., Chefalo P.J., Gray R.C., Ramachandra L., and Harding C.V. Enhancement of dendritic cell antigen cross-presentation by CpG DNA involves type IIFN and stabilization of class I MHC mRNA. J. Immunol. 175 (2005) 2244-2251
41. Sun S.Q., Zhang X.H., Tough D.F., and Sprent J. Type I interferon-mediated stimulation of T cells by CgG DNA. J. Exp. Med. 188 (1998) 2335-2342