Combined vaccination and immunostimulatory antibodies provides durable cure of murine melanoma and induces transcriptional changes associated with positive outcome in human melanoma patients

OncoImmunology

Volumn 1, Issue 4, 2012, Pages 419-431

  McGray, A J Robert ^a   Bernard, Dannie ^a   Hallett, Robin ^a   Kelly, Ryan ^a   Jha, Mayank ^a   Gregory, Caitlin ^a   Bassett, Jennifer D ^a   Hassell, John A ^a   Pare, Guillaume ^a   Wan, Yonghong ^a   Bramson, Jonathan L ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

4 1BB, PD 1; Gene profiling; Immune suppression; T lymphocyte; Vaccine

Indexed keywords

CD137 ANTIGEN; DOPACHROME TAUTOMERASE; GAMMA INTERFERON; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY CD137; PROGRAMMED DEATH 1 RECEPTOR; PROGRAMMED DEATH 1 RECEPTOR ANTIBODY; RECEPTOR ANTIBODY; RNA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER COMBINATION CHEMOTHERAPY; CANCER IMMUNIZATION; CANCER SURVIVAL; CELLULAR IMMUNITY; COHORT ANALYSIS; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG EFFICACY; DRUG POTENTIATION; FEMALE; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; HUMAN; HUMAN TISSUE; IMMUNOSTIMULATION; MELANOMA; MONOTHERAPY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OVERALL SURVIVAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR BLOCKING; TREATMENT OUTCOME; TUMOR ASSOCIATED LEUKOCYTE; TUMOR GROWTH; TUMOR MICROENVIRONMENT; TUMOR REGRESSION; UPREGULATION;

EID: 84879204726     PISSN: 21624011     EISSN: 2162402X     Source Type: Journal    
DOI: 10.4161/onci.19534     Document Type: Article

References (46)

1. Harrop R, John J, Carroll MW. Recombinant viral vectors: cancer vaccines. Adv Drug Deliv Rev 2006; 58:931-47; PMID:17030074; http://dx.doi.org/10.1016/j.addr.2006.05.005
2. Anderson RJ, Schneider J. Plasmid DNA and viral vectorbased vaccines for the treatment of cancer. Vaccine 2007; 25(Suppl 2):B24-34; PMID:17698262; http://dx.doi.org/10.1016/j.vaccine.2007.05.030
3. Lane C, Leitch J, Tan X, Hadjati J, Bramson JL, Wan Y. Vaccination-induced autoimmune vitiligo is a consequence of secondary trauma to the skin. Cancer Res 2004; 64:1509-14; PMID:14973051; http://dx.doi.org/10.1158/0008-5472.CAN-03-3227
4. Kianizad K, Marshall LA, Grinshtein N, Bernard D, Margl R, Cheng S, et al. Elevated frequencies of selfreactive CD8+ T cells following immunization with a xenoantigen are due to the presence of a heteroclitic CD4+ T-cell helper epitope. Cancer Res 2007; 67: 6459-67; PMID:17616707; http://dx.doi.org/10.1158/0008-5472.CAN-06-4336
5. Bernard D, Ventresca MS, Marshall LA, Evelegh C, Wan Y, Bramson JL. Processing of tumor antigen differentially impacts the development of helper and effector CD4+ T-cell responses. Mol Ther 2010;18:1224-32; PMID:20179673; http://dx.doi.org/10.1038/mt.2010.30
6. Grinshtein N, Bridle B, Wan Y, Bramson JL. Neoadjuvant vaccination provides superior protection against tumor relapse following surgery compared with adjuvant vaccination. Cancer Res 2009; 69:3979-85; PMID:19383917; http://dx.doi.org/10.1158/0008-5472.CAN-08-3385
7. Grinshtein N, Ventresca M, Margl R, Bernard D, Yang TC, Millar JB, et al. High-dose chemotherapy augments the efficacy of recombinant adenovirus vaccines and improves the therapeutic outcome. Cancer Gene Ther 2009; 16:338-50; PMID:18989352; http://dx.doi.org/10.1038/cgt.2008.89
8. Lowin B, Hahne M, Mattmann C, Tschopp J. Cytolytic T-cell cytotoxicity is mediated through perforin and Fas lytic pathways. Nature 1994; 370: 650-2; PMID:7520535; http://dx.doi.org/10.1038/370650a0
9. Ashkenazi A, Dixit VM. Death receptors: signaling and modulation. Science 1998; 281:1305-8; PMID: 9721089; http://dx.doi.org/10.1126/science.281.5381.1305
10. Chawla-Sarkar M, Lindner DJ, Liu YF, Williams BR, Sen GC, Silverman RH, et al. Apoptosis and interferons: role of interferon-stimulated genes as mediators of apoptosis. Apoptosis 2003; 8:237-49; PMID:12766484; http://dx.doi.org/10.1023/A:1023668705040
11. Dalton DK, Pitts-Meek S, Keshav S, Figari IS, Bradley A, Stewart TA. Multiple defects of immune cell function in mice with disrupted interferon-gamma genes. Science 1993; 259:1739-42; PMID:8456300; http://dx.doi.org/10.1126/science.8456300
12. Wigginton JM, Gruys E, Geiselhart L, Subleski J, Komschlies KL, Park JW, et al. IFN-gamma and Fas/ FasL are required for the antitumor and antiangiogenic effects of IL-12/pulse IL-2 therapy. J Clin Invest 2001; 108:51-62; PMID:11435457
13. Kim PS, Ahmed R. Features of responding T cells in cancer and chronic infection. Curr Opin Immunol 2010; 22:223-30; PMID:20207527; http://dx.doi.org/10.1016/j.coi.2010.02.005
14. Watts TH. TNF/TNFR family members in costimulation of T cell responses. Annu Rev Immunol 2005; 23:23-68; PMID:15771565; http://dx.doi.org/10.1146/annurev.immunol.23.021704.115839
15. Sharpe AH, Freeman GJ. The B7-CD28 superfamily. Nat Rev Immunol 2002; 2:116-26; PMID:11910893; http://dx.doi.org/10.1038/nri727
16. Shuford WW, Klussman K, Tritchler DD, Loo DT, Chalupny J, Siadak AW, et al. 4-1BB costimulatory signals preferentially induce CD8+ T cell proliferation and lead to the amplification in vivo of cytotoxic T cell responses. J Exp Med 1997; 186:47-55; PMID: 9206996; http://dx.doi.org/10.1084/jem.186.1.47
17. Wilcox RA, Flies DB, Zhu G, Johnson AJ, Tamada K, Chapoval AI, et al. Provision of antigen and CD137 signaling breaks immunological ignorance, promoting regression of poorly immunogenic tumors. J Clin Invest 2002; 109:651-9; PMID:11877473
18. Kwon BS, Hurtado JC, Lee ZH, Kwack KB, Seo SK, Choi BK, et al. Immune responses in 4-1BB (CD137)- deficient mice. J Immunol 2002; 168:5483-90; PMID: 12023342
19. Takahashi C, Mittler RS, Vella AT. Cutting edge: 4-1BB is a bona fide CD8 T cell survival signal. J Immunol 1999; 162:5037-40; PMID:10227968
20. Melero I, ShufordWW, Newby SA, Aruffo A, Ledbetter JA, Hellström KE, et al. Monoclonal antibodies against the 4-1BB T-cell activation molecule eradicate established tumors. Nat Med 1997; 3:682-5; PMID:9176498; http://dx.doi.org/10.1038/nm0697-682
21. Ju SA, Lee SC, Kwon TH, Heo SK, Park SM, Paek HN, et al. Immunity to melanoma mediated by 4-1BB is associated with enhanced activity of tumourinfiltrating lymphocytes. Immunol Cell Biol 2005; 83:344-51; PMID:16033529; http://dx.doi.org/10.1111/j.1440-1711.2005.01330.x
22. Gray JC, French RR, James S, Al-Shamkhani A, Johnson PW, Glennie MJ. Optimising anti-tumour CD8 T-cell responses using combinations of immunomodulatory antibodies. Eur J Immunol 2008; 38:2499-511; PMID:18792403; http://dx.doi.org/10.1002/eji.200838208
23. Francisco LM, Sage PT, Sharpe AH. The PD-1 pathway in tolerance and autoimmunity. Immunol Rev 2010; 236:219-42; PMID:20636820; http://dx.doi.org/10.1111/j.1600-065X.2010.00923.x
24. Thompson RH, Dong H, Lohse CM, Leibovich BC, Blute ML, Cheville JC, et al. PD-1 is expressed by tumor-infiltrating immune cells and is associated with poor outcome for patients with renal cell carcinoma. Clin Cancer Res 2007; 13:1757-61; PMID:17363529; http://dx.doi.org/10.1158/1078-0432.CCR-06-2599
25. Ahmadzadeh M, Johnson LA, Heemskerk B, Wunderlich JR, Dudley ME, White DE, et al. Tumor antigen-specific CD8 T cells infiltrating the tumor express high levels of PD-1 and are functionally impaired. Blood 2009; 114:1537-44; PMID:19423728; http://dx.doi.org/10.1182/blood-2008-12-195792
26. Barber DL, Wherry EJ, Masopust D, Zhu B, Allison JP, Sharpe AH, et al. Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 2006; 439:682-7; PMID:16382236; http://dx.doi.org/10.1038/nature04444
27. Li B, VanRoey M, Wang C, Chen TH, Korman A, Jooss K. Anti-programmed death-1 synergizes with granulocyte macrophage colony-stimulating factor-secreting tumor cell immunotherapy providing therapeutic benefit to mice with established tumors. Clin Cancer Res 2009; 15:1623-34; PMID:19208793; http://dx.doi.org/10.1158/1078-0432.CCR-08-1825
28. Pilon-Thomas S, Mackay A, Vohra N, Mulé JJ. Blockade of programmed death ligand 1 enhances the therapeutic efficacy of combination immunotherapy against melanoma. J Immunol 2010; 184:3442-9; PMID:20194714; http://dx.doi.org/10.4049/jimmunol.0904114
29. Miller RE, Jones J, Le T, Whitmore J, Boiani N, Gliniak B, et al. 4-1BB-specific monoclonal antibody promotes the generation of tumor-specific immune responses by direct activation of CD8 T cells in a CD40-dependent manner. J Immunol 2002; 169: 1792-800; PMID:12165501
30. Li B, Lin J, Vanroey M, Jure-Kunkel M, Jooss K. Established B16 tumors are rejected following treatment with GM-CSF-secreting tumor cell immunotherapy in combination with anti-4-1BB mAb. Clin Immunol 2007; 125:76-87; PMID:17706463; http://dx.doi.org/10.1016/j.clim.2007.07.005
31. Choi BK, Kim YH, Kang WJ, Lee SK, Kim KH, Shin SM, et al. Mechanisms involved in synergistic anticancer immunity of anti-4-1BB and anti-CD4 therapy. Cancer Res 2007; 67:8891-9; PMID:17875731; http://dx.doi.org/10.1158/0008-5472.CAN-07-1056
32. Tibshirani R, Hastie T, Narasimhan B, Chu G. Diagnosis of multiple cancer types by shrunken centroids of gene expression. Proc Natl Acad Sci U S A 2002; 99:6567-72; PMID:12011421; http://dx.doi.org/10.1073/pnas.082099299
33. Appay V, Jandus C, Voelter V, Reynard S, Coupland SE, Rimoldi D, et al. New generation vaccine induces effective melanoma-specific CD8+ T cells in the circulation but not in the tumor site. J Immunol 2006; 177:1670-8; PMID:16849476
34. Vinay DS, Kwon BS. 4-1BB signaling beyond T cells. Cell Mol Immunol 2011; 8:281-4; PMID:21217771; http://dx.doi.org/10.1038/cmi.2010.82
35. Zhang Y, Ma CJ, Ni L, Zhang CL, Wu XY, Kumaraguru U, et al. Cross-talk between programmed death-1 and suppressor of cytokine signaling-1 ininhibition of IL-12 production by monocytes/macrophages in hepatitis C virus infection. J Immunol 2011; 186:3093-103; PMID:21263070; http://dx.doi.org/10.4049/jimmunol.1002006
36. Chen Y, Wu S, Guo G, Fei L, Guo S, Yang C, et al. Programmed death (PD)-1-deficient mice are extremely sensitive to murine hepatitis virus strain-3 (MHV-3) infection. PLoS Pathog 2011; 7:e1001347; PMID: 21750671; http://dx.doi.org/10.1371/journal.ppat.1001347
37. Bogunovic D, O'Neill DW, Belitskaya-Levy I, Vacic V, Yu YL, Adams S, et al. Immune profile and mitotic index of metastatic melanoma lesions enhance clinical staging in predicting patient survival. Proc Natl Acad Sci U S A 2009; 106:20429-34; PMID:19915147; http://dx.doi.org/10.1073/pnas.0905139106
38. Jönsson G, Busch C, Knappskog S, Geisler J, Miletic H, Ringnér M, et al. Gene expression profiling-based identification of molecular subtypes in stage IV melanomas with different clinical outcome. Clin Cancer Res 2010; 16:3356-67; PMID:20460471; http://dx.doi.org/10.1158/1078-0432.CCR-09-2509
39. Gajewski TF, Fuertes M, Spaapen R, Zheng Y, Kline J. Molecular profiling to identify relevant immune resistance mechanisms in the tumor microenvironment. Curr Opin Immunol 2011; 23:286-92; PMID: 21185705; http://dx.doi.org/10.1016/j.coi.2010.11.013
40. Lasaro MO, Ertl HC. Targeting inhibitory pathways in cancer immunotherapy. Curr Opin Immunol 2010; 22:385-90; PMID:20466529; http://dx.doi.org/10.1016/j.coi.2010.04.005
41. Ng P, Parks RJ, Cummings DT, Evelegh CM, Graham FL. An enhanced system for construction of adenoviral vectors by the two-plasmid rescue method. Hum Gene Ther 2000; 11:693-9; PMID:10757349; http://dx.doi.org/10.1089/10430340050015590
42. Leitch J, Fraser K, Lane C, Putzu K, Adema GJ, Zhang QJ, et al. CTL-dependent and -independent antitumor immunity is determined by the tumor not the vaccine. J Immunol 2004; 172:5200-5; PMID:15100257
43. Curran MA, Montalvo W, Yagita H, Allison JP. PD-1 and CTLA-4 combination blockade expands infiltrating T cells and reduces regulatory T and myeloid cells within B16 melanoma tumors. Proc Natl Acad Sci U S A 2010; 107:4275-80; PMID:20160101; http://dx.doi.org/10.1073/pnas.0915174107
44. Shi L, Jones WD, Jensen RV, Harris SC, Perkins RG, Goodsaid FM, et al. The balance of reproducibility, sensitivity, and specificity of lists of differentially expressed genes in microarray studies. BMC Bioinformatics 2008; 9(Suppl 9):S10; PMID:18793455; http://dx.doi.org/10.1186/1471-2105-9-S9-S10
45. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, et al. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 2003; 4:249-64; PMID: 12925520; http://dx.doi.org/10.1093/biostatistics/4.2.249
46. Yau C, Esserman L, Moore DH, Waldman F, Sninsky J, Benz CC. A multigene predictor of metastatic outcome in early stage hormone receptor-negative and triple-negative breast cancer. Breast Cancer Res 2010; 12:R85; PMID:20946665; http://dx.doi.org/10.1186/bcr2753