Transient depletion of CD4+ T cells augments IL-21-based immunotherapy of disseminated neuroblastoma in syngeneic mice

International Journal of Cancer

Volumn 127, Issue 5, 2010, Pages 1141-1150

  Croce, Michela ^a   Corrias, Maria Valeria ^b   Orengo, Anna Maria ^a   Brizzolara, Antonella ^a   Carlini, Barbara ^b   Borghi, Martina ^a   Rigo, Valentina ^a   Pistoia, Vito ^b   Ferrini, Silvano ^a  

^a UNIVERSITY OF GENOA   (Italy)

^b G GASLINI INSTITUTE   (Italy)

Author keywords

IL 21; Immunotherapy; Monoclonal antibody; Neuroblastoma; Treg cells

Indexed keywords

ALPHA2A INTERFERON; BASILIXIMAB; CD4 ANTIGEN; CD8 ANTIGEN; CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 2; INTERLEUKIN 21; MESSENGER RNA; CANCER VACCINE; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, MOUSE; INTERLEUKIN 10; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN DERIVATIVE; MEMBRANE PROTEIN; MONOCLONAL ANTIBODY; PTGS1 PROTEIN, MOUSE; PTGS2 PROTEIN, MOUSE; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER IMMUNOTHERAPY; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; IMMUNE RESPONSE; MOUSE; NEUROBLASTOMA; NEUROBLASTOMA CELL; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SCID MOUSE; SPLEEN CELL; VACCINATION; A J MOUSE; ANIMAL; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; IMMUNOLOGY; IMMUNOTHERAPY; LYMPHOCYTE DEPLETION; METABOLISM; MOUSE MUTANT; NONOBESE DIABETIC MOUSE; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANIMALS; ANTIBODIES, MONOCLONAL; BLOTTING, WESTERN; CANCER VACCINES; CD4-POSITIVE T-LYMPHOCYTES; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; FEMALE; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; FORKHEAD TRANSCRIPTION FACTORS; IMMUNOTHERAPY; INTERFERON-GAMMA; INTERLEUKIN-10; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; INTERLEUKINS; LYMPHOCYTE DEPLETION; MEMBRANE PROTEINS; MICE; MICE, INBRED A; MICE, INBRED NOD; MICE, SCID; NEUROBLASTOMA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TRANSFORMING GROWTH FACTOR BETA;

EID: 77955479823     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.25140     Document Type: Article

References (39)

1. Maris JM, Hogarty MD, Bagatell R, Cohn SL. Neuroblastoma. Lancet 2007;369: 2106-20.
2. De Bernardi B, Nicolas B, Boni L, Indolfi P, Carli M, Cordero Di Montezemolo L, Donfrancesco A, Pession A, Provenzi M, Di Cataldo A, Rizzo A, Tonini GP, et al. Disseminated neuroblastoma in children older than one year at diagnosis: comparable results with three consecutive high-dose protocols adopted by the Italian Co-operative Group for Neuroblastoma. J Clin Oncol 2003;21:1592-601.
3. Wysocki PJ, Karczewska-Dzionk A, Mackiewicz-Wysocka M, Mackiewicz A. Human cancer gene therapy with cytokine gene-modified cells. Expert Opin Biol Ther 2004;4:1595-607.
4. Parmiani G, Pilla L, Castelli C, Rivoltini L. Vaccination of patients with solid tumours. Ann Oncol 2003;6:817-24.
5. Vieweg J, Su Z, Dahm P, Kusmartsev S. Reversal of tumor-mediated immunosuppression. Clin Cancer Res 2007; 13:727s-732s
6. Nagaraj S, Gabrilovich DI. Tumor escape mechanism governed by myeloid-derived suppressor cells. Cancer Res 2008;68: 2561-3.
7. Jordan MS, Boesteanu A, Reed AJ, Petrone AL, Holenbeck AE, Lerman MA, Naji A, Caton AJ. Thymic selection of CD4+CD25+ regulatory T cells induced by an agonist self-peptide. Nat Immunol 2001;2:301-6.
8. Hori S, Nomura T, Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Science 2003; 299:1057-61.
9. Sakaguchi S. Naturally arising CD4+ regulatory T cells for immunologic self-tolerance and negative control of immune responses. Annu Rev Immunol 2004;22: 531-62.
10. Chen W, Jin W, Hardegen N, Lei KJ, Li L, Marinos N, McGrady G, Wah SM. Conversion of peripheral CD4+CD25-naive T cells to CD4+CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. J Exp Med 2003;198:1875-86.
11. Valzasina B, Piconese S, Guiducci C, Colombo MP. Tumor-induced expansion of regulatory T cells by conversion of CD4+CD25-lymphocytes is thymus and proliferation independent. Cancer Res 2006; 66:4488-95.
12. Liu VC, Wong LY, Jang T, Shah AH, Park I, Yang X, Zhang Q, Lonning S, Teicher BA, Lee C. Tumor evasion of the immune system by converting CD4+CD25-T cells into CD4+CD25+ T regulatory cells: role of tumor-derived TGF-beta. J Immunol 2007;178:2883-92.
13. Sharma S, Yang SC, Zhu L, Reckamp K, Gardner B, Baratelli F, Huang M, Batra RK, Dubinett SM. Tumor cyclooxygenase- 2/prostaglandin E2-dependent promotion of FOXP3 expression and CD4+ CD25+ T regulatory cell activities in lung cancer. Cancer Res 2005;65:5211-20.
14. Colombo MP, Piconese S. Regulatory-T-cell inhibition versus depletion: the right choice in cancer immunotherapy. Nat Rev Cancer 2007;7:880-7.
15. Refaeli Y, Van Parijs L, London CA, Tschopp J, Abbas AK. Biochemical mechanisms of IL-2-regulated Fas-mediated T cell apoptosis. Immunity 1998; 8:615-23.
16. Bayer AL, Yu A, Adeegbe D, Malek TR. Essential role for interleukin-2 for CD4(+)CD25(+) T regulatory cell development during the neonatal period. J Exp Med 2005;201:769-77.
17. Parrish-Novak J, Dillon SR, Nelson A, Hammond A, Sprecher C, Gross JA, Johnston J, Madden K, Xu W, West J, Schrader S, Burkhead S, et al. Interleukin- 21 and its receptor are involved in NK cell expansion and regulation of lymphocyte function. Nature 2000;408:57-63.
18. Comes A, Rosso O, Orengo AM, DiCarlo E, Sorrentino C, Meazza R, Piazza T, Valzasina B, Nanni P, Colombo MP, Ferrini S. CD25+ regulatory T cell depletion augments immunotherapy of micrometastases by an IL-21-secreting cellular vaccine. J Immunol 2006;176: 1750-8.
19. Wang G, Tschoi M, Spolski R, Lou Y, Ozaki K, Feng C, Kim G, Leonard WJ, Hwu P. In vivo antitumor activity of interleukin 21 mediated by natural killer cells. Cancer Res 2003;63:9016-22.
20. Moroz A, Eppolito C, Li Q, Tao J, Clegg CH, Shrikant PA. IL-21 enhances and sustains CD8+ T cell responses to achieve durable tumor immunity: comparative evaluation of IL-2. IL-15, and. IL-21. J Immunol 2004;173:900-9.
21. Croce M, Meazza R, Orengo AM, Fabbi M, Borghi M, Ribatti D, Nico B, Carlini B, Pistoia V, Corrias MV, Ferrini S. Immunotherapy of neuroblastoma by an interleukin-21-secreting cell vaccine involves survivin as antigen. Cancer Immunol Immunother 2008;57:1625-34.
22. Daga A, Orengo AM, Gangemi RM, Marubbi D, Perera M, Comes A, Ferrini S, Corte G. Glioma immunotherapy by IL-21 gene-modified cells or by recombinant IL-21 involves antibody responses. Int J Cancer 2007;121:1756-63.
23. Smyth MJ, Teng MW, Sharkey J, Westwood JA, Haynes NM, Yagita H, Takeda K, Sivakumar PV, Kershaw MH. Interleukin 21 enhances antibody-mediated tumor rejection. Cancer Res 2008;68: 3019-25.
24. Thompson JA, Curti BD, Redman BG, Bhatia S, Weber JS, Agarwala SS, Sievers EL, Hughes SD, DeVries TA, Hausman DF. Phase I study of recombinant interleukin-21 in patients with metastatic melanoma and renal cell carcinoma. J Clin Oncol 2008;26:2034-9.
25. Davis ID, Skrumsager BK, Cebon J, Nicholaou T, Barlow JW, Moller NP, Skak K, Lundsgaard D, Frederiksen KS, Thygesen P, McArthur GA. An open-label, two-arm, phase I trial of recombinant human interleukin-21 in patients with metastatic melanoma. Clin Cancer Res 2007;13:3630-6.
26. Croce M, Meazza R, Orengo AM, Radic' L, De Giovanni B, Gambini C, Carlini B, Pistoia V, Mortara L, Accolla RS, Corrias MV, Ferrini S. Sequential immunogene therapy with interleukin-12- and interleukin-15-engineered neuroblastoma cells cures metastatic disease in syngeneic mice. Clin Cancer Res 2005;11: 735-42.
27. Lowenthal JW, Corthesy P, Tougne C, Lees R, MacDonald HR, Nabholz M. High and low affinity IL 2 receptors: analysis by IL 2 dissociation rate and reactivity with monoclonal anti-receptor antibody PC61. J Immunol 1985;135:3988-94.
28. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using realtime quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001;25: 402-8.
29. Roncarolo MG, Gregori S, Battaglia M, Bacchetta R, Fleischhauer K, Levings MK. Interleukin-10-secreting type 1 regulatory T cells in rodents and humans. Immunol Rev 2006;212:28-50.
30. Wei L, Laurence A, Elias KM, O'Shea JJ. IL-21 is produced by Th17 cells and drives IL-17 production in a STAT3-dependent manner. J Biol Chem 2007;282: 34605-10.
31. Di Carlo E, Comes A, Orengo AM, Rosso O, Meazza R, Musiani P, Colombo MP, Ferrini S. IL-21 induces tumor rejection by specific CTL and IFN-gamma-dependent CXC chemokines in syngeneic mice. J Immunol 2004;172:1540-7.
32. Couper KN, Blount DG, de Souza JB, Suffia I, Belkaid Y, Riley EM. Incomplete depletion and rapid regeneration of Foxp3+ regulatory T cells following anti-CD25 treatment in malaria-infected mice. J Immunol 2007;178: 4136-46.
33. Zelenay S, Demengeot J. Comment on cutting edge: anti-CD25 monoclonal antibody injection results in the functional inactivation, not depletion, of CD4+CD25+ T regulatory cells. J Immunol 2006;177:2036-7.
34. Terabe M, Berzofsky JA. The role of NKT cells in tumor immunity. Adv Cancer Res 2008;101:277-348.
35. Nagai H, Hara I, Horikawa T, Oka M, Kamidono S, Ichihashi M. Elimination of CD4(+) T cells enhances anti-tumor effect of locally secreted interleukin-12 on B16 mouse melanoma and induces vitiligo-like coat color alteration. J Invest Dermatol 2000;115:1059-64.
36. Heinzel FP, Rerko RM. Cure of progressive murine leishmaniasis: interleukin 4 dominance is abolished by transient CD4(+) T cell depletion and T helper cell type 1-selective cytokine therapy. J Exp Med 1999;189:1895-906.
37. Gattinoni L, Finkelstein SE, Klebanoff CA, Antony PA, Palmer DC, Spiess PJ, Hwang LN, Yu Z, Wrzesinski C, Heimann DM, Surh CD, Rosenberg SA, et al. Removal of homeostatic cytokine sinks by lymphodepletion enhances the efficacy of adoptively transferred tumor-specific CD8+ T cells. J Exp Med 2005; 202:907-12.
38. Jing W, Gershan JA, Johnson BD. Depletion of CD4 T cells enhances immunotherapy for neuroblastoma after syngeneic HSCT but compromises development of anti-tumor immune memory. Blood 2009; 113:4449-57.
39. Smyth MJ, Hayakawa Y, Cretney E, Zerafa N, Sivakumar P, Yagita H, Takeda K. IL-21 enhances tumor-specific CTL induction by anti-DR5 antibody therapy. J Immunol 2006;176:6347-55.