Heterologous vaccination and checkpoint blockade synergize to induce antileukemia immunity

Journal of Immunology

Volumn 196, Issue 11, 2016, Pages 4793-4804

  Manlove, Luke S ^a   Schenkel, Jason M ^a,b   Manlove, Kezia R ^c   Pauken, Kristen E ^a,d   Williams, Richard T ^e,f   Vezys, Vaiva ^a,b   Farrar, Michael A ^a,b  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c PENNSYLVANIA STATE UNIVERSITY   (United States)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

^e AMGEN INC   (United States)

^f UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BCR ABL PROTEIN; CD40 LIGAND MONOCLONAL ANTIBODY; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4 ANTIBODY; GRANZYME B; INTERLEUKIN 10; INTERLEUKIN 17; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PEPTIDE; PROGRAMMED DEATH 1 RECEPTOR; PROGRAMMED DEATH 1 RECEPTOR ANTIBODY; RECEPTOR ANTIBODY; UNCLASSIFIED DRUG;

ACUTE LYMPHOBLASTIC LEUKEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN EXPRESSION; ARTICLE; CANCER CONTROL; CANCER IMMUNIZATION; CANCER IMMUNOTHERAPY; CELL CYCLE CHECKPOINT; CONTROLLED STUDY; HETEROLOGOUS VACCINATION; MOUSE; MURINE MODEL; MUTATIONAL LOAD; NONHUMAN; OVERALL SURVIVAL; PRINCIPAL COMPONENT ANALYSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE; TUMOR IMMUNITY; VACCINATION; ANIMAL; C57BL MOUSE; DISEASE MODEL; IMMUNOLOGY; KNOCKOUT MOUSE; PATHOLOGY; PHYSIOLOGY;

ANIMALS; CELL CYCLE CHECKPOINTS; DISEASE MODELS, ANIMAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PRECURSOR B-CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; VACCINATION;

EID: 84975119958     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1600130     Document Type: Article

References (56)

1. Gleissner, B., N. Gökbuget, C. R. Bartram, B. Janssen, H. Rieder, J. W. Janssen, C. Fonatsch, A. Heyll, D. Voliotis, J. Beck, et al; German Multicenter Trials of Adult Acute Lymphoblastic Leukemia Study Group. 2002. Leading prognostic relevance of the BCR-ABL translocation in adult acute B-lineage lymphoblastic leukemia: a prospective study of the German Multicenter Trial Group and confirmed polymerase chain reaction analysis. Blood 99: 1536-1543.
2. +) acute lymphoblastic leukemia. Blood 116: 2070-2077.
3. Hodi, F. S., S. J. O'Day, D. F. McDermott, R. W. Weber, J. A. Sosman, J. B. Haanen, R. Gonzalez, C. Robert, D. Schadendorf, J. C. Hassel, et al. 2010. Improved survival with ipilimumab in patients with metastatic melanoma. N. Engl. J. Med. 363: 711-723.
4. Topalian, S. L., F. S. Hodi, J. R. Brahmer, S. N. Gettinger, D. C. Smith, D. F. McDermott, J. D. Powderly, R. D. Carvajal, J. A. Sosman, M. B. Atkins, et al. 2012. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N. Engl. J. Med. 366: 2443-2454.
5. Alexandrov, L. B., S. Nik-Zainal, D. C. Wedge, S. A. Aparicio, S. Behjati, A. V. Biankin, G. R. Bignell, N. Bolli, A. Borg, A. L. Børresen-Dale, et al; Australian Pancreatic Cancer Genome Initiative; ICGC Breast Cancer Consortium; ICGC MMML-Seq Consortium; ICGC PedBrain. 2013. Signatures of mutational processes in human cancer. Nature 500: 415-421.
6. Manlove, L. S., K. E. Berquam-Vrieze, K. E. Pauken, R. T. Williams, M. K. Jenkins, and M. A. Farrar. 2015. Adaptive immunity to leukemia is inhibited by cross-reactive induced regulatory T cells. J. Immunol. 195: 4028-4037.
7. Williams, R. T., M. F. Roussel, and C. J. Sherr. 2006. Arf gene loss enhances oncogenicity and limits imatinib response in mouse models of Bcr-Abl-induced acute lymphoblastic leukemia. Proc. Natl. Acad. Sci. USA 103: 6688-6693.
8. +, Arf-null lymphoblastic leukemia. Genes Dev. 21: 2283-2287.
9. Manlove, L. S., K. E. Berquam-Vrieze, K. E. Pauken, R. T. Williams, M. K. Jenkins, and M. A. Farrar. 2015. Adaptive immunity to leukemia is inhibited by cross-reactive induced regulatory T cells. J. Immunol. 195: 4028-4037.
10. + acute lymphoblastic leukemia during long-term imatinib mesylate treatment. Blood 115: 1512-1518.
11. Kamijo, T., F. Zindy, M. F. Roussel, D. E. Quelle, J. R. Downing, R. A. Ashmun, G. Grosveld, and C. J. Sherr. 1997. Tumor suppression at the mouse INK4a locus mediated by the alternative reading frame product p19ARF. Cell 91: 649-659.
12. Hogquist, K. A., S. C. Jameson, W. R. Heath, J. L. Howard, M. J. Bevan, and F. R. Carbone. 1994. T cell receptor antagonist peptides induce positive selection. Cell 76: 17-27.
13. Brundage, R. A., G. A. Smith, A. Camilli, J. A. Theriot, and D. A. Portnoy. 1993. Expression and phosphorylation of the Listeria monocytogenes ActA protein in mammalian cells. Proc. Natl. Acad. Sci. USA 90: 11890-11894.
14. Orr, M. T., N. N. Orgun, C. B. Wilson, and S. S. Way. 2007. Cutting edge: recombinant Listeria monocytogenes expressing a single immune-dominant peptide confers protective immunity to herpes simplex virus-1 infection. J. Immunol. 178: 4731-4735.
15. + T cells during Listeria monocytogenes infection. J. Immunol. 182: 3032-3038.
16. Pear, W. S., J. P. Miller, L. Xu, J. C. Pui, B. Soffer, R. C. Quackenbush, A. M. Pendergast, R. Bronson, J. C. Aster, M. L. Scott, and D. Baltimore. 1998. Efficient and rapid induction of a chronic myelogenous leukemia-like myeloproliferative disease in mice receiving P210 bcr/abl-transduced bone marrow. Blood 92: 3780-3792.
17. Moon, J. J., H. H. Chu, J. Hataye, A. J. Pagán, M. Pepper, J. B. McLachlan, T. Zell, and M. K. Jenkins. 2009. Tracking epitope-specific T cells. Nat. Protoc. 4: 565-581.
18. R Core Team. 2012. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
19. Zhang, M., Z, Yao, S, Dubois, W. Ju, J. R. Muller, and T. A. Waldmann., 2009. Interleukin-15 combined with an anti-CD40 antibody provides enhanced therapeutic efficacy for murine models of colon cancer. Proc. Natl. Acad. Sci. USA 106 7513-7513.
20. Braumuller, H., T. Wieder, E. Brenner, S. Aßmann, M. Hahn, M. Alkhaled, K. Schilbach, F. Essmann, M. Kneilling, C. Griessinger, et al. 2013. T-helper-1-cell cytokines drive cancer into senescence. Nature 494: 361-365.
21. Barber, D. L., E. J. Wherry, D. Masopust, B. Zhu, J. P. Allison, A. H. Sharpe, G. J. Freeman, and R. Ahmed. 2006. Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 439: 682-687.
22. Perez, V. L., L. Van Parijs, A. Biuckians, X. X. Zheng, T. B. Strom, and A. K. Abbas. 1997. Induction of peripheral T cell tolerance in vivo requires CTLA-4 engagement. Immunity 6: 411-417.
23. Krummel, M. F., and J. P. Allison. 1996. CTLA-4 engagement inhibits IL-2 accumulation and cell cycle progression upon activation of resting T cells. J. Exp. Med. 183: 2533-2540.
24. Krummel, M. F., and J. P. Allison. 1995. CD28 and CTLA-4 have opposing effects on the response of T cells to stimulation. J. Exp. Med. 182: 459-465.
25. Mumm, J. B., J. Emmerich, X. Zhang, I. Chan, L. Wu, S. Mauze, S. Blaisdell, B. Basham, J. Dai, J. Grein, et al. 2011. IL-10 elicits IFNg-dependent tumor immune surveillance. Cancer Cell 20: 781-796.
26. Curran, M. A., T. L. Geiger, W. Montalvo, M. Kim, S. L. Reiner, A. Al-Shamkhani, J. C. Sun, and J. P. Allison. 2013. Systemic 4-1BB activation induces a novel T cell phenotype driven by high expression of Eomesodermin. J. Exp. Med. 210: 743-755.
27. Rose, N. F., P. A. Marx, A. Luckay, D. F. Nixon, W. J. Moretto, S. M. Donahoe, D. Montefiori, A. Roberts, L. Buonocore, and J. K. Rose. 2001. An effective AIDS vaccine based on live attenuated vesicular stomatitis virus recombinants. Cell 106: 539-549.
28. Muranski, P., Z. A. Borman, S. P. Kerkar, C. A. Klebanoff, Y. Ji, L. Sanchez-Perez, M. Sukumar, R. N. Reger, Z. Yu, S. J. Kern, et al. 2011. Th17 cells are long lived and retain a stem cell-like molecular signature. Immunity 35: 972-985.
29. Kantarjian, H. M., R. S. Walters, M. J. Keating, T. L. Smith, S. O'Brien, E. H. Estey, Y. O. Huh, J. Spinolo, K. Dicke, B. Barlogie, et al. 1990. Results of the vincristine, doxorubicin, and dexamethasone regimen in adults with standard-and high-risk acute lymphocytic leukemia. J. Clin. Oncol. 8: 994-1004.
30. Daver, N., D. Thomas, F. Ravandi, J. Cortes, R. Garris, E. Jabbour, G. Garcia-Manero, G. Borthakur, T. Kadia, M. Rytting, et al. 2015. Final report of a phase II study of imatinib mesylate with hyper-CVAD for the front-line treatment of adult patients with Philadelphia chromosome-positive acute lymphoblastic leukemia. Haematologica 100: 653-661.
31. Sawyers, C. L., A. Hochhaus, E. Feldman, J. M. Goldman, C. B. Miller, O. G. Ottmann, C. A. Schiffer, M. Talpaz, F. Guilhot, M. W. Deininger, et al. 2002. Imatinib induces hematologic and cytogenetic responses in patients with chronic myelogenous leukemia in myeloid blast crisis: results of a phase II study. Blood 99: 3530-3539.
32. Wolchok, J. D., A. Hoos, S. O'Day, J. S. Weber, O. Hamid, C. Lebbé, M. Maio, M. Binder, O. Bohnsack, G. Nichol, et al. 2009. Guidelines for the evaluation of immune therapy activity in solid tumors: immune-related response criteria. Clin. Cancer Res. 15: 7412-7420.
33. Brahmer, J. R., S. S. Tykodi, L. Q. Chow, W. J. Hwu, S. L. Topalian, P. Hwu, C. G. Drake, L. H. Camacho, J. Kauh, K. Odunsi, et al. 2012. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N. Engl. J. Med. 366: 2455-2465.
34. Kochenderfer, J. N., Z. Yu, D. Frasheri, N. P. Restifo, and S. A. Rosenberg. 2010. Adoptive transfer of syngeneic T cells transduced with a chimeric antigen receptor that recognizes murine CD19 can eradicate lymphoma and normal B cells. Blood 116: 3875-3886.
35. Snyder, A., V. Makarov, T. Merghoub, J. Yuan, J. M. Zaretsky, A. Desrichard, L. A. Walsh, M. A. Postow, P. Wong, T. S. Ho, et al. 2014. Genetic basis for clinical response to CTLA-4 blockade in melanoma. N. Engl. J. Med. 371: 2189-2199.
36. Schumacher, T. N., and R. D. Schreiber. 2015. Neoantigens in cancer immunotherapy. Science 348: 69-74.
37. Diehl, L., A. T. den Boer, S. P. Schoenberger, E. I. van der Voort, T. N. Schumacher, C. J. Melief, R. Offringa, and R. E. Toes. 1999. CD40 activation in vivo overcomes peptide-induced peripheral cytotoxic T-lymphocyte tolerance and augments anti-tumor vaccine efficacy. Nat. Med. 5: 774-779.
38. French, R. R., H. T. Chan, A. L. Tutt, and M. J. Glennie. 1999. CD40 antibody evokes a cytotoxic T-cell response that eradicates lymphoma and bypasses T-cell help. Nat. Med. 5: 548-553.
39. + Tcell tolerance to T-cell priming through in vivo ligation of CD40. Nat. Med. 5: 780-787.
40. Murphy, K. A., M. G. Lechner, F. E. Popescu, J. Bedi, S. A. Decker, P. Hu, J. R. Erickson, M. G. O'Sullivan, L. Swier, A. M. Salazar, et al. 2012. An in vivo immunotherapy screen of costimulatory molecules identifies Fc-OX40L as a potent reagent for the treatment of established murine gliomas. Clin. Cancer Res. 18: 4657-4668.
41. Leach, D. R., M. F. Krummel, and J. P. Allison. 1996. Enhancement of antitumor immunity by CTLA-4 blockade. Science 271: 1734-1736.
42. Hirano, F., K. Kaneko, H. Tamura, H. Dong, S. Wang, M. Ichikawa, C. Rietz, D. B. Flies, J. S. Lau, G. Zhu, et al. 2005. Blockade of B7-H1 and PD-1 by monoclonal antibodies potentiates cancer therapeutic immunity. Cancer Res. 65: 1089-1096.
43. Hodge, J. W., J. Higgins, and J. Schlom. 2009. Harnessing the unique local immunostimulatory properties of modified vaccinia Ankara (MVA) virus to generate superior tumor-specific immune responses and antitumor activity in a diversified prime and boost vaccine regimen. Vaccine 27: 4475-4482.
44. Boudreau, J. E., B. W. Bridle, K. B. Stephenson, K. M. Jenkins, J. Brunellière, J. L. Bramson, B. D. Lichty, and Y. Wan. 2009. Recombinant vesicular stomatitis virus transduction of dendritic cells enhances their ability to prime innate and adaptive antitumor immunity. Mol. Ther. 17: 1465-1472.
45. Dai, W. J., G. Köhler, and F. Brombacher. 1997. Both innate and acquired immunity to Listeria monocytogenes infection are increased in IL-10-deficient mice. J. Immunol. 158: 2259-2267.
46. Sevilla, N., D. B. McGavern, C. Teng, S. Kunz, and M. B. Oldstone. 2004. Viral targeting of hematopoietic progenitors and inhibition of DC maturation as a dual strategy for immune subversion. J. Clin. Invest. 113: 737-745.
47. Masopust, D., S. J. Ha, V. Vezys, and R. Ahmed. 2006. Stimulation history dictates memory CD8 T cell phenotype: implications for prime-boost vaccination. J. Immunol. 177: 831-839.
48. Vezys, V., A. Yates, K. A. Casey, G. Lanier, R. Ahmed, R. Antia, and D. Masopust. 2009. Memory CD8 T-cell compartment grows in size with immunological experience. Nature 457: 196-199.
49. Irvine, K. R., R. S. Chamberlain, E. P. Shulman, D. R. Surman, S. A. Rosenberg, and N. P. Restifo. 1997. Enhancing efficacy of recombinant anticancer vaccines with prime/boost regimens that use two different vectors. J. Natl. Cancer Inst. 89: 1595-1601.
50. Zamarin, D., R. B. Holmgaard, S. K. Subudhi, J. S. Park, M. Mansour, P. Palese, T. Merghoub, J. D. Wolchok, and J. P. Allison. 2014. Localized oncolytic virotherapy overcomes systemic tumor resistance to immune checkpoint blockade immunotherapy. Sci. Transl. Med. 6: 226ra32.
51. Park, S. H., C. J. Breitbach, J. Lee, J. O. Park, H. Y. Lim, W. K. Kang, A. Moon, J. H. Mun, E. M. Sommermann, L. Maruri Avidal, et al. 2015. Phase 1b trial of biweekly intravenous Pexa-Vec (JX-594), an oncolytic and immunotherapeutic vaccinia virus in colorectal cancer. Mol. Ther. 23: 1532-1540.
52. Pecora, A. L., N. Rizvi, G. I. Cohen, N. J. Meropol, D. Sterman, J. L. Marshall, S. Goldberg, P. Gross, J. D. O'Neil, W. S. Groene, et al. 2002. Phase I trial of intravenous administration of PV701, an oncolytic virus, in patients with advanced solid cancers. J. Clin. Oncol. 20: 2251-2266.
53. Dennis, K. L., A. Saadalla, N. R. Blatner, S. Wang, V. Venkateswaran, F. Gounari, H. Cheroutre, C. T. Weaver, A. Roers, N. K. Egilmez, and K. Khazaie. 2015. T-cell expression of IL10 is essential for tumor immune surveillance in the small intestine. Cancer Immunol. Res. 3: 806-814.
54. Dennis, K. L., N. R. Blatner, F. Gounari, and K. Khazaie. 2013. Current status of interleukin-10 and regulatory T-cells in cancer. Curr. Opin. Oncol. 25: 637-645.
55. Muranski, P., and N. P. Restifo. 2013. Essentials of Th17 cell commitment and plasticity. Blood 121: 2402-2414.
56. McGeachy, M. J. 2013. Th17 memory cells: live long and proliferate. J. Leukoc. Biol. 94: 921-926.