Combination of cyclophosphamide, rituximab, and intratumoral CpG oligodeoxynucleotide successfully eradicates established B cell Lymphoma

Journal of Immunotherapy

Volumn 35, Issue 7, 2012, Pages 534-543

  Betting, David J ^a   Hurvitz, Sara A ^a   Steward, Kristopher K ^a   Yamada, Reiko E ^a   Kafi, Kamran ^a   Van Rooijen, Nico ^b   Timmerman, John M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b VU UNIVERSITY AMSTERDAM   (Netherlands)

Author keywords

B cell lymphoma; CD20; CpG; rituximab; toll like receptor agonist

Indexed keywords

CD11B ANTIGEN; CD19 ANTIGEN; CD20 ANTIGEN; COMPLEMENT; CPG OLIGODEOXYNUCLEOTIDE; CYCLOPHOSPHAMIDE; RITUXIMAB; TRANSCRIPTION FACTOR FOXP3; TRASTUZUMAB;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B CELL LYMPHOMA; B LYMPHOCYTE; CANCER CELL; CANCER COMBINATION CHEMOTHERAPY; CANCER IMMUNOTHERAPY; CD4+ CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; FEMALE; LYMPHOID ORGAN; MACROPHAGE; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SUPPRESSOR CELL; T LYMPHOCYTE; TUMOR IMMUNITY;

EID: 85027925138     PISSN: 15249557     EISSN: 15374513     Source Type: Journal    
DOI: 10.1097/CJI.0b013e318261e679     Document Type: Article

References (59)

1. Cheson BD, Leonard JP.Monoclonal antibody therapy for B cell non-Hodgkin's lymphoma. N Engl J Med. 2008;359:613-626.
2. Sousou T, Friedberg J. Rituximab in indolent lymphomas. Semin Hematol. 2010;47:133-142.
3. Zwick C, Murawski N, Pfreundschuh M. Rituximab in highgrade lymphoma. Semin Hematol. 2010;47:148-155.
4. Maloney DG. Immunotherapy for non-Hodgkin's lymphoma: monoclonal antibodies and vaccines. J Clin Oncol. 2005;23: 6421-6428. (Pubitemid 46218853)
5. Weiner GJ. Rituximab: mechanism of action. Semin Hematol. 2010;47:115-123.
6. Clynes RA, Towers TL, Presta LG, et al. Inhibitory Fc receptors modulate in vivo cytotoxicity against tumor targets. Nat Med. 2000;6:443-446. (Pubitemid 30208162)
7. Cartron G, Dacheux L, Salles G, et al. Therapeutic activity of humanized anti-CD20 monoclonal antibody and polymorphism in IgG Fc receptor FcgammaRIIIa gene. Blood. 2002;99:754-758. (Pubitemid 34525533)
8. Weng WK, Levy R. Two immunoglobulin G fragment C receptor polymorphisms independently predict response to rituximab in patients with follicular lymphoma. J Clin Oncol. 2003;21:3940-3947. (Pubitemid 46606207)
9. Selenko N, Maidic O, Draxier S, et al. CD20 antibody (C2B8)-induced apoptosis of lymphoma cells promotes phagocytosis by dendritic cells and cross-priming of CD8+ cytotoxic T cells. Leukemia. 2001;15:1619-1626. (Pubitemid 32994682)
10. Dhodapkar KM, Dhodapkar MV. Recruiting dendritic cells to improve antibody therapy of cancer. Proc Natl Acad Sci USA. 2005;102:6243-6244. (Pubitemid 40617428)
11. Franki SN, Steward KK, Betting DJ, et al. Dendritic cells loaded with apoptotic antibody-coated tumor cells provide protective immunity against B cell lymphoma in vivo. Blood. 2008;111:1504-1511. (Pubitemid 351213439)
12. Hilchey SP, Hyrien O, Mosmann TR, et al. Rituximab immunotherapy results in the induction of a lymphoma idiotype-specific T cell response in patients with follicular lymphoma: support for a "vaccinal effect" of rituximab. Blood. 2009;113:3809-3812.
13. Davis TA, Maloney DG, Grillo-Lopez AJ, et al. Combination immunotherapy of relapsed or refractory low-grade or follicular non-Hodgkin's lymphoma with rituximab and interferon-alpha-2a. Clin Cancer Res. 2000;6:2644-2652. (Pubitemid 30482099)
14. Ansell SM, Witzig TE, Kurtin PJ, et al. Phase 1 study of interleukin-12 in combination with rituximab in patients with B cell non-Hodgkin lymphoma. Blood. 2002;99:67-74.
15. Kimby E. Beyond immunochemotherapy: combinations of rituximab with cytokines interferon-alpha2a and granulocyte colony stimulating factor [corrected]. Semin Oncol. 2002;29:7-10. (Pubitemid 34594978)
16. Friedberg JW, Neuberg D, Gribben JG, et al. Combination immunotherapy with rituximab and interleukin 2 in patients with relapsed or refractory follicular non-Hodgkin's lymphoma. Br J Haematol. 2002;117:828-834. (Pubitemid 34639243)
17. Gluck WL, Hurst D, Yuen A, et al. Phase I studies of interleukin (IL)-2 and rituximab in B cell non-Hodgkin's lymphoma: IL-2 mediated natural killer cell expansion correlations with clinical response. Clin Cancer Res. 2004;10: 2253-2264. (Pubitemid 38445682)
18. Cartron G, Watier H, Golay J, et al. From the bench to the bedside: ways to improve rituximab efficacy. Blood. 2004;104:2635-2642. (Pubitemid 39434941)
19. Kanzler H, Barrat FJ, Hessel EM, et al. Therapeutic targeting of innate immunity with Toll-like receptor agonists and antagonists. Nat Med. 2007;13:552-559. (Pubitemid 46830615)
20. Krieg AM. Development of TLR9 agonists for cancer therapy. J Clin Invest. 2007;117:1184-1194. (Pubitemid 46718403)
21. Krieg AM. Toll-like receptor 9 (TLR9) agonists in the treatment of cancer. Oncogene. 2008;27:161-167.
22. Link BK, Ballas ZK, Weisdorf D, et al. Oligodeoxynucleotide CpG 7909 delivered as intravenous infusion demonstrates immunologic modulation in patients with previously treated non-Hodgkin lymphoma. J Immunother. 2006;29:558-568. (Pubitemid 44395280)
23. Friedberg JW, Kim H, McCauley M, et al. Combination immunotherapy with a CpG oligonucleotide (1018 ISS) and rituximab in patients with non-Hodgkin lymphoma: increased interferon-alpha/beta-inducible gene expression, without significant toxicity. Blood. 2005;105:489-495. (Pubitemid 40070726)
24. Leonard JP, Link BK, Emmanouilides C, et al. Phase I trial of toll-like receptor 9 agonist PF-3512676 with and following rituximab in patients with recurrent indolent and aggressive non Hodgkin's lymphoma. Clin Cancer Res. 2007;13:6168-6174. (Pubitemid 350075077)
25. Heckelsmiller K, Rall K, Beck S, et al. 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;169:3892-3899.
26. Sharma S, Karakousis CP, Takita H, et al. Intra-tumoral injection of CpG results in the inhibition of tumor growth in murine Colon-26 and B-16 tumors. Biotechnol Lett. 2003;25:149-153. (Pubitemid 36189361)
27. Lonsdorf AS, Kuekrek H, Stern BV, et al. Intratumor CpGoligodeoxynucleotide injection induces protective antitumor T cell immunity. J Immunol. 2003;171:3941-3946. (Pubitemid 37238666)
28. Furumoto K, Soares L, Engleman EG, et al. Induction of potent antitumor immunity by in situ targeting of intratumoral DCs. J Clin Invest. 2004;113:774-783. (Pubitemid 38544171)
29. Sharma S, Dominguez AL, Hoelzinger DB, et al. CpG-ODN but not other TLR-ligands restore the antitumor responses in old mice: the implications for vaccinations in the aged. Cancer Immunol Immunother. 2008;57:549-561. (Pubitemid 351170538)
30. Li J, Song W, Czerwinski DK, et al. Lymphoma immunotherapy with CpG oligodeoxynucleotides requires TLR9 either in the host or in the tumor itself. J Immunol. 2007;179:2493-2500.
31. Varghese B, Widman A, Do J, et al. Generation of CD8+ T cell-mediated immunity against idiotype-negative lymphoma escapees. Blood. 2009;114:4477-4485.
32. Brody JD, Ai WZ, Czerwinski DK, et al. In situ vaccination with a TLR9 agonist induces systemic lymphoma regression: a phase I/II study. J Clin Oncol. 2010;28:4324-4332.
33. Betting DJ, Yamada RE, Kafi K, et al. Intratumoral but not systemic delivery of CpG oligodeoxynucleotide augments the efficacy of anti-CD20 monoclonal antibody therapy against B cell lymphoma. J Immunother. 2009;32:622-631.
34. Coiffier B, Lepage E, Briere J, et al. CHOP chemotherapy plus rituximab compared with CHOP alone in elderly patients with diffuse large-B cell lymphoma. N Engl J Med. 2002;346: 235-242. (Pubitemid 34438862)
35. Marcus R, Imrie K, Solal-Celigny P, et al. Phase III study of R-CVP compared with cyclophosphamide, vincristine, and prednisone alone in patients with previously untreated advanced follicular lymphoma. J Clin Oncol. 2008;26:4579-4586.
36. Lutsiak ME, Semnani RT, De Pascalis R, et al. Inhibition of CD4(+)25+ T regulatory cell function implicated in enhanced immune response by low-dose cyclophosphamide. Blood. 2005;105:2862-2868. (Pubitemid 40446280)
37. Bracci L, Moschella F, Sestili P, et al. Cyclophosphamide enhances the antitumor efficacy of adoptively transferred immune cells through the induction of cytokine expression, B cell and T cell homeostatic proliferation, and specific tumor infiltration. Clin Cancer Res. 2007;13:644-653. (Pubitemid 46225372)
38. Salem ML, Kadima AN, El-Naggar SA, et al. Defining the ability of cyclophosphamide preconditioning to enhance the antigen-specific CD8+ T cell response to peptide vaccination: creation of a beneficial host microenvironment involving type I IFNs and myeloid cells. J Immunother. 2007;30:40-53. (Pubitemid 46052202)
39. Berraondo P, Nouze C, Preville X, et al. Eradication of large tumors in mice by a tritherapy targeting the innate, adaptive, and regulatory components of the immune system. Cancer Res. 2007;67:8847-8855. (Pubitemid 47437461)
40. Liu JY, Wu Y, Zhang XS, et al. Single administration of low dose cyclophosphamide augments the antitumor effect of dendritic cell vaccine. Cancer Immunol Immunother. 2007;56: 1597-1604. (Pubitemid 47094389)
41. Matsushita N, Pilon-Thomas SA, Martin LM, et al. Comparative methodologies of regulatory T cell depletion in a murine melanoma model. J Immunol Methods. 2008;333:167-179.
42. Schiavoni G, Sistigu A, Valentini M, et al. Cyclophosphamide synergizes with type I interferons through systemic dendritic cell reactivation and induction of immunogenic tumor apoptosis. Cancer Res. 2011;71:768-778.
43. Bergman Y, Haimovich J. Characterization of a carcinogeninduced murine B lymphocyte cell line of C3H/eB origin. Eur J Immunol. 1977;7:413-417. (Pubitemid 8149366)
44. Golay J, Cittera E, Di Gaetano N, et al. The role of complement in the therapeutic activity of rituximab in a murine B lymphoma model homing in lymph nodes. Haematologica. 2006;91:176-183.
45. Van Rooijen N, Sanders A. Liposome mediated depletion of macrophages: mechanism of action, preparation of liposomes and applications. J Immunol Methods. 1994;174:83-93.
46. Timmerman JM, Levy R. Linkage of foreign carrier protein to a self-tumor antigen enhances the immunogenicity of a pulsed dendritic cell vaccine. J Immunol. 2000;164:4797-4803. (Pubitemid 30238082)
47. Timmerman JM, Caspar CB, Lambert SL, et al. Idiotypeencoding recombinant adenoviruses provide protective immunity against murine B cell lymphomas. Blood. 2001;97:1370-1377. (Pubitemid 32183761)
48. Betting DJ, Kafi K, Abdollahi-Fard A, et al. Sulfhydryl-based tumor antigen-carrier protein conjugates stimulate superior anti-tumor immunity against B cell lymphomas. J Immunol. 2008;181:4131-4140.
49. Minard-Colin V, Xiu Y, Poe JC, et al. Lymphoma depletion during CD20 immunotherapy in mice is mediated by macrophage FcgammaRI, FcgammaRIII, and FcgammaRIV. Blood. 2008;112:1205-1213.
50. Miller G, Bleier JI, Antonescu C, et al. Natural killer cell depletion confounds the antitumor mechanism of endogenous IL-12 overexpression. Int J Cancer. 2004;110:395-402. (Pubitemid 38649891)
51. Neeson P, Paterson Y. A new multi-parameter flow cytometric assay for monitoring lymphoma growth and spread in a preclinical murine model for human lymphoma. Cytometry A. 2004;60:8-20. (Pubitemid 38859197)
52. Uchida J, Hamaguchi Y, Oliver JA, et al. The innate mononuclear phagocyte network depletes B lymphocytes through Fc receptor-dependent mechanisms during Anti-CD20 antibody immunotherapy. J Exp Med. 2004;199: 1659-1669. (Pubitemid 38821999)
53. Gong Q, Ou Q, Ye S, et al. Importance of cellular microenvironment and circulatory dynamics in B cell immunotherapy. J Immunol. 2005;174:817-826. (Pubitemid 40094277)
54. Cameron RB, Spiess PJ, Rosenberg SA. Synergistic antitumor activity of tumor-infiltrating lymphocytes, interleukin 2, and local tumor irradiation. Studies on the mechanism of action. J Exp Med. 1990;171:249-263. (Pubitemid 20040613)
55. Serafini P, Borrello I, Bronte V. Myeloid suppressor cells in cancer: recruitment, phenotype, properties, and mechanisms of immune suppression. Semin Cancer Biol. 2006;16:53-65. (Pubitemid 43139709)
56. Serafini P, Mgebroff S, Noonan K, et al. Myeloid-derived suppressor cells promote cross-tolerance in B cell lymphoma by expanding regulatory T cells. Cancer Res. 2008;68:5439-5449.
57. Morecki S, Gelfand Y, Yacovlev E, et al. CpG-induced myeloid CD11b+Gr-1+ cells efficiently suppress T cellmediated immunoreactivity and graft-versus-host disease in a murine model of allogeneic cell therapy. Biol Blood Marrow Transplant. 2008;14:973-984.
58. Honeychurch J, Glennie MJ, Illidge TM. Cyclophosphamide inhibition of anti-CD40 monoclonal antibody-based therapy of B cell lymphoma is dependent on CD11b+ cells. Cancer Res. 2005;65:7493-7501. (Pubitemid 41161285)
59. Ugel S, Delpozzo F, Desantis G, et al. Therapeutic targeting of myeloid-derived suppressor cells. Curr Opin Pharmacol. 2009; 9:470-481.