Immunotherapy-induced CD8+ T cells instigate immune suppression in the tumor

Molecular Therapy

Volumn 22, Issue 1, 2014, Pages 206-218

  McGray, A J Robert ^a   Hallett, Robin ^a   Bernard, Dannie ^a   Swift, Stephanie L ^a   Zhu, Ziqiang ^b   Teoderascu, Florentina ^a   VanSeggelen, Heather ^a   Hassell, John A ^a   Hurwitz, Arthur A ^b   Wan, Yonghong ^a   Bramson, Jonathan L ^a  

^a MCMASTER UNIVERSITY   (Canada)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VACCINE;

ADAPTIVE IMMUNITY; ADOPTIVE IMMUNOTHERAPY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER IMMUNIZATION; CANCER IMMUNOTHERAPY; CANCER INHIBITION; CANCER RECURRENCE; CANCER REGRESSION; CD8+ T LYMPHOCYTE; CELL EXPANSION; CELLULAR IMMUNITY; CONTROLLED STUDY; DRUG EFFICACY; FEMALE; LYMPHOCYTE COUNT; LYMPHOCYTIC INFILTRATION; MELANOMA; MOUSE; NONHUMAN; TUMOR REGRESSION; UPREGULATION;

MURINAE;

ADAPTIVE IMMUNITY; ADENOVIRUSES, HUMAN; ANIMALS; ANTIGENS, NEOPLASM; CANCER VACCINES; CD8-POSITIVE T-LYMPHOCYTES; FEMALE; GENETIC VECTORS; IMMUNOMODULATION; IMMUNOTHERAPY; IMMUNOTHERAPY, ADOPTIVE; INTERFERON-GAMMA; INTRAMOLECULAR OXIDOREDUCTASES; LYMPHOCYTES, TUMOR-INFILTRATING; MICE; NEOPLASM RECURRENCE, LOCAL; NEOPLASMS; T-LYMPHOCYTE SUBSETS; TUMOR BURDEN; VACCINATION; VACCINES, SYNTHETIC;

EID: 84891831962     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2013.255     Document Type: Article

References (45)

1. Schlom, J (2012). Therapeutic cancer vaccines: Current status and moving forward. J Natl Cancer Inst 104: 599-613
2. Klebanoff, CA, Acquavella, N, Yu, Z and Restifo, NP (2011). Therapeutic cancer vaccines: Are we there yet? Immunol Rev 239: 27-44
3. Rosenberg, SA (2012). Raising the bar: The curative potential of human cancer immunotherapy. Sci Transl Med 4: 127ps8
4. Kantoff, PW, Schuetz, TJ, Blumenstein, BA, Glode, LM, Bilhartz, DL, Wyand, M et al. (2010). Overall survival analysis of a phase II randomized controlled trial of a Poxviralbased PSA-targeted immunotherapy in metastatic castration-resistant prostate cancer. J Clin Oncol 28: 1099-1105
5. Schwartzentruber, DJ, Lawson, DH, Richards, JM, Conry, RM, Miller, DM, Treisman, J et al. (2011). gp100 peptide vaccine and interleukin-2 in patients with advanced melanoma. N Engl J Med 364: 2119-2127
6. Schuster, SJ, Neelapu, SS, Gause, BL, Janik, JE, Muggia, FM, Gockerman, JP et al. (2011). Vaccination with patient-specific tumor-derived antigen in first remission improves disease-free survival in follicular lymphoma. J Clin Oncol 29: 2787-2794
7. Odunsi, K, Matsuzaki, J, Karbach, J, Neumann, A, Mhawech-Fauceglia, P, Miller, A et al. (2012). Efficacy of vaccination with recombinant vaccinia and fowlpox vectors expressing NY-ESO-1 antigen in ovarian cancer and melanoma patients. Proc Natl Acad Sci USA 109: 5797-5802
8. Kantoff, PW, Higano, CS, Shore, ND, Berger, ER, Small, EJ, Penson, DF et al.; IMPACT Study Investigators. (2010). Sipuleucel-T immunotherapy for castration-resistant prostate cancer. N Engl J Med 363: 411-422
9. Sims, RB (2012). Development of sipuleucel-T: Autologous cellular immunotherapy for the treatment of metastatic castrate resistant prostate cancer. Vaccine 30: 4394-4397
10. Galluzzi, L, Vacchelli, E, Eggermont, A, Fridman, WH, Galon, J, Sautès-Fridman, C et al. (2012). Trial Watch: Adoptive cell transfer immunotherapy. Oncoimmunology 1: 306-315
11. Porter, DL, Levine, BL, Kalos, M, Bagg, A and June, CH (2011). Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. N Engl J Med 365: 725-733
12. Kochenderfer, JN, Dudley, ME, Feldman, SA, Wilson, WH, Spaner, DE, Maric, I et al. (2012). B-cell depletion and remissions of malignancy along with cytokine-associated toxicity in a clinical trial of anti-CD19 chimeric-antigen-receptor-transduced T cells. Blood 119: 2709-2720
13. Rosenberg, SA, Yang, JC, Sherry, RM, Kammula, US, Hughes, MS, Phan, GQ et al. (2011). Durable complete responses in heavily pretreated patients with metastatic melanoma using T-cell transfer immunotherapy. Clin Cancer Res 17: 4550-4557
14. Malyguine, AM, Strobl, SL and Shurin, MR (2012). Immunological monitoring of the tumor immunoenvironment for clinical trials. Cancer Immunol Immunother 61: 239-247
15. Gajewski, TF, Fuertes, M, Spaapen, R, Zheng, Y and Kline, J (2011). Molecular profiling to identify relevant immune resistance mechanisms in the tumor microenvironment. Curr Opin Immunol 23: 286-292
16. Gajewski, TF (2012). Cancer immunotherapy. Mol Oncol 6: 242-250
17. Stewart, TJ and Smyth, MJ (2011). Improving cancer immunotherapy by targeting tumor-induced immune suppression. Cancer Metastasis Rev 30: 125-140
18. Schreiber, RD, Old, LJ and Smyth, MJ (2011). Cancer immunoediting: Integrating immunity's roles in cancer suppression and promotion. Science 331: 1565-1570
19. Landsberg, J, Kohlmeyer, J, Renn, M, Bald, T, Rogava, M, Cron, M et al. (2012). Melanomas resist T-cell therapy through inflammation-induced reversible dedifferentiation. Nature 490: 412-416
20. Kaluza, KM, Thompson, JM, Kottke, TJ, Flynn Gilmer, HC, Knutson, DL and Vile, RG (2012). Adoptive T cell therapy promotes the emergence of genomically altered tumor escape variants. Int J Cancer 131: 844-854
21. Grinshtein, N, Ventresca, M, Margl, R, Bernard, D, Yang, TC, Millar, JB et al. (2009). High-dose chemotherapy augments the efficacy of recombinant adenovirus vaccines and improves the therapeutic outcome. Cancer Gene Ther 16: 338-350
22. Slifka, MK, Rodriguez, F and Whitton, JL (1999). Rapid on/off cycling of cytokine production by virus-specific CD8+ T cells. Nature 401: 76-79
23. McGray, AJ, Bernard, D, Hallett, R, Kelly, R, Jha, M, Gregory, C et al. (2012). Combined vaccination and immunostimulatory antibodies provides durable cure of murine melanoma and induces transcriptional changes associated with positive outcome in human melanoma patients. Oncoimmunology 1: 419-431
24. Bernal, M, Ruiz-Cabello, F, Concha, A, Paschen, A and Garrido, F (2012). Implication of the ß2-microglobulin gene in the generation of tumor escape phenotypes. Cancer Immunol Immunother 61: 1359-1371
25. Zhang, B, Karrison, T, Rowley, DA and Schreiber, H (2008). IFN-gamma- and TNF-dependent bystander eradication of antigen-loss variants in established mouse cancers. J Clin Invest 118: 1398-1404
26. Khong, HT and Restifo, NP (2002). Natural selection of tumor variants in the generation of tumor escape; phenotypes. Nat Immunol 3: 999-1005
27. Taube, JMJ, Anders, RAR, Young, GDG, Xu, HH, Sharma, RR, McMiller, TLT et al. (2012). Colocalization of inflammatory response with B7-h1 expression in human melanocytic lesions supports an adaptive resistance mechanism of immune escape. Sci Trans Med 4: 127ra37
28. Hamanishi, J, Mandai, M, Iwasaki, M, Okazaki, T, Tanaka, Y, Yamaguchi, K et al. (2007). Programmed cell death 1 ligand 1 and tumor-infiltrating CD8+ T lymphocytes are prognostic factors of human ovarian cancer. Proc Natl Acad Sci USA 104: 3360-3365
29. Robbins, PF, Morgan, RA, Feldman, SA, Yang, JC, Sherry, RM, Dudley, ME et al. (2011). Tumor regression in patients with metastatic synovial cell sarcoma and melanoma using genetically engineered lymphocytes reactive with NY-ESO-1. J Clin Oncol 29: 917-924
30. Ahmadzadeh, M, Johnson, LA, Heemskerk, B, Wunderlich, JR, Dudley, ME, White, DE et al. (2009). Tumor antigen-specific CD8 T cells infiltrating the tumor express high levels of PD-1 and are functionally impaired. Blood 114: 1537-1544
31. Harlin, H, Meng, Y, Peterson, AC, Zha, Y, Tretiakova, M, Slingluff, C et al. (2009). Chemokine expression in melanoma metastases associated with CD8+ T-cell recruitment. Cancer Res 69: 3077-3085
32. Baitsch, L, Baumgaertner, P, Devêvre, E, Raghav, SK, Legat, A, Barba, L et al. (2011). Exhaustion of tumor-specific CD8? T cells in metastases from melanoma patients. J Clin Invest 121: 2350-2360
33. Gajewski, TF (2007). Failure at the effector phase: Immune barriers at the level of the melanoma tumor microenvironment. Clin Cancer Res 13(18 Pt 1): 5256-5261
34. Bos, R and Sherman, LA (2010). CD4+ T-cell help in the tumor milieu is required for recruitment and cytolytic function of CD8+ T lymphocytes. Cancer Res 70: 8368-8377
35. Shafer-Weaver, KA, Watkins, SK, Anderson, MJ, Draper, LJ, Malyguine, A, Alvord, WG et al. (2009). Immunity to murine prostatic tumors: Continuous provision of T-cell help prevents CD8 T-cell tolerance and activates tumor-infiltrating dendritic cells. Cancer Res 69: 6256-6264
36. Corthay, A, Skovseth, DK, Lundin, KU, Røsjø, E, Omholt, H, Hofgaard, PO et al. (2005). Primary antitumor immune response mediated by CD4+ T cells. Immunity 22: 371-383
37. Perez-Diez, A, Joncker, NT, Choi, K, Chan, WF, Anderson, CC, Lantz, O et al. (2007). CD4 cells can be more efficient at tumor rejection than CD8 cells. Blood 109: 5346-5354
38. Muranski, P, Boni, A, Antony, PA, Cassard, L, Irvine, KR, Kaiser, A et al. (2008). Tumor-specific Th17-polarized cells eradicate large established melanoma. Blood 112: 362-373
39. Kerkar, SP, Goldszmid, RS, Muranski, P, Chinnasamy, D, Yu, Z, Reger, RN et al. (2011). IL-12 triggers a programmatic change in dysfunctional myeloid-derived cells within mouse tumors. J Clin Invest 121: 4746-4757
40. Ng, P, Parks, RJ, Cummings, DT, Evelegh, CM and Graham, FL (2000). An enhanced system for construction of adenoviral vectors by the two-plasmid rescue method. Hum Gene Ther 11: 693-699
41. Leitch, J, Fraser, K, Lane, C, Putzu, K, Adema, GJ, Zhang, QJ et al. (2004). CTLdependent and -independent antitumor immunity is determined by the tumor not the vaccine. J Immunol 172: 5200-5205
42. Bernard, D, Ventresca, MS, Marshall, LA, Evelegh, C, Wan, Y and Bramson, JL (2010). Processing of tumor antigen differentially impacts the development of helper and effector CD4+ T-cell responses. Mol Ther 18: 1224-1232
43. Irizarry, RA, Hobbs, B, Collin, F, Beazer-Barclay, YD, Antonellis, KJ, Scherf, U et al. (2003). Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4: 249-264
44. Huang, DW, Sherman, BT and Lempicki, RA (2009). Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57
45. Schaefer, CF, Anthony, K, Krupa, S, Buchoff, J, Day, M, Hannay, T et al. (2009). PID: The Pathway Interaction Database. Nucleic Acids Res 37(Database issue): D674-D679