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Review Article

Clinical Combinatorial Treatments Based on Cancer Vaccines: Combination with Checkpoint Inhibitors and Beyond

Author(s): Mojdeh Soltani, Lyudmila V. Savvateeva, Mazdak Ganjalikhani-Hakemi and Andrey A. Zamyatnin*

Volume 23, Issue 11, 2022

Published on: 21 June, 2022

Page: [1072 - 1084] Pages: 13

DOI: 10.2174/1389450123666220421124542

Price: $65

Abstract

The efficacy of the cancer vaccine is influenced by several factors, but one of the most important is the immunosuppressive tumor microenvironment, which can attenuate treatment effects. The combination of therapeutic cancer vaccines with other immunotherapies or conventional therapeutic approaches can promote vaccine efficacy by increasing immune surveillance and tumor immunogenicity and modulating immune escape in the tumor microenvironment. Inhibitory checkpoints have a significant role in the modulation of anticancer immune responses, and according to preclinical and clinical trials, administration of immune checkpoint inhibitors (ICIs) in combination with cancer vaccines can markedly improve their therapeutic effects, considering their low clinical efficacy. In addition, these combinatorial therapies have acceptable safety and minimal additional toxicity compared to single-agent cancer vaccines or ICIs. In this review, based on the results of previous studies, we introduce and discuss treatments that can be combined with therapeutic cancer vaccines to improve their potency. Our major focus is on checkpoint blockade therapies, which are the most well-known and applicable immunotherapies.

Keywords: Cancer vaccine, immune checkpoint inhibitors, combinatorial therapies, therapeutic cancer, tumors, carcinogenesis.

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[1]
Coley WB. The treatment of inoperable sarcoma by bacterial toxins (the mixed toxins of the Streptococcus erysipelas and the Bacillus prodigiosus). Proceedings of the Royal Society of Medicine. 1-48.
[http://dx.doi.org/10.1177/003591571000301601]
[2]
Pallerla S, Abdul AURM, Comeau J, Jois S. Cancer vaccines, treatment of the future: With emphasis on her2-positive breast cancer. Int J Mol Sci 2021; 22(2): 779.
[http://dx.doi.org/10.3390/ijms22020779] [PMID: 33466691]
[3]
Lollini P-L, Cavallo F, Nanni P, Forni G. Vaccines for tumour prevention. Nat Rev Cancer 2006; 6(3): 204-16.
[http://dx.doi.org/10.1038/nrc1815] [PMID: 16498443]
[4]
Vergati M, Intrivici C, Huen N-Y, Schlom J, Tsang KY. Strategies for cancer vaccine development. J Biomed Biotechnol 2010; 2010: 596432.
[http://dx.doi.org/10.1155/2010/596432]
[5]
Hu Z, Ott PA, Wu CJ. Towards personalized, tumour-specific, therapeutic vaccines for cancer. Nat Rev Immunol 2018; 18(3): 168-82.
[http://dx.doi.org/10.1038/nri.2017.131] [PMID: 29226910]
[6]
Wong KK, Li WA, Mooney DJ, Dranoff G. Advances in therapeutic cancer vaccines. Adv Immunol 2016; 130: 191-249.
[http://dx.doi.org/10.1016/bs.ai.2015.12.001] [PMID: 26923002]
[7]
Schlom J. Therapeutic cancer vaccines: Current status and moving forward. J Natl Cancer Inst 2012; 104(8): 599-613.
[http://dx.doi.org/10.1093/jnci/djs033] [PMID: 22395641]
[8]
Yadav M, Jhunjhunwala S, Phung QT, et al. Predicting immunogenic tumour mutations by combining mass spectrometry and exome sequencing. Nature 2014; 515(7528): 572-6.
[http://dx.doi.org/10.1038/nature14001] [PMID: 25428506]
[9]
Gilboa E. How tumors escape immune destruction and what we can do about it. Cancer Immunol Immunother 1999; 48(7): 382-5.
[http://dx.doi.org/10.1007/s002620050590] [PMID: 10501851]
[10]
van der Burg SH, Arens R, Ossendorp F, van Hall T, Melief CJ. Vaccines for established cancer: Overcoming the challenges posed by immune evasion. Nat Rev Cancer 2016; 16(4): 219-33.
[http://dx.doi.org/10.1038/nrc.2016.16] [PMID: 26965076]
[11]
Overwijk WW. Cancer vaccines in the era of checkpoint blockade: The magic is in the adjuvant. Curr Opin Immunol 2017; 47: 103-9.
[http://dx.doi.org/10.1016/j.coi.2017.07.015] [PMID: 28806603]
[12]
Sharma P, Hu-Lieskovan S, Wargo JA, Ribas A. Leading edge review primary, adaptive, and acquired resistance to cancer immunotherapy. Cell 2017; 168(4): 707-23.
[http://dx.doi.org/10.1016/j.cell.2017.01.017] [PMID: 28187290]
[13]
Seidel JA, Otsuka A, Kabashima K. Anti-PD-1 and Anti-CTLA-4 therapies in cancer: Mechanisms of action, efficacy, and limitations. Front Oncol 2018; 8: 86.
[http://dx.doi.org/10.3389/fonc.2018.00086] [PMID: 29644214]
[14]
Sharma P, Allison JP. The future of immune checkpoint therapy. Science 2015; 348(6230): 56-61.
[http://dx.doi.org/10.1126/science.aaa8172] [PMID: 25838373]
[15]
Sylvester RJ. van der MEIJDEN AP, Lamm DL. Intravesical bacillus Calmette-Guerin reduces the risk of progression in patients with superficial bladder cancer: A meta-analysis of the published results of randomized clinical trials. J Urol 2002; 168(5): 1964-70.
[http://dx.doi.org/10.1016/S0022-5347(05)64273-5] [PMID: 12394686]
[16]
GuhaThakurta D, Sheikh NA, Fan L-Q, et al. Humoral immune response against nontargeted tumor antigens after treatment with sipuleucel-T and its association with improved clinical outcome. Clin Cancer Res 2015; 21(16): 3619-30.
[http://dx.doi.org/10.1158/1078-0432.CCR-14-2334] [PMID: 25649018]
[17]
Sheikh NA, Petrylak D, Kantoff PW, et al. Sipuleucel-T immune parameters correlate with survival: An analysis of the randomized phase 3 clinical trials in men with castration-resistant prostate cancer. Cancer Immunol Immunother 2013; 62(1): 137-47.
[http://dx.doi.org/10.1007/s00262-012-1317-2] [PMID: 22865266]
[18]
Kohlhapp FJ, Kaufman HL. Molecular pathways: Mechanism of action for talimogene laherparepvec, a new oncolytic virus immunotherapy. Clin Cancer Res 2016; 22(5): 1048-54.
[http://dx.doi.org/10.1158/1078-0432.CCR-15-2667] [PMID: 26719429]
[19]
Gulley JL, Borre M, Vogelzang NJ, et al. Phase III trial of PROSTVAC in asymptomatic or minimally symptomatic metastatic castration-resistant prostate cancer. J Clin Oncol 2019; 37(13): 1051-61.
[http://dx.doi.org/10.1200/JCO.18.02031] [PMID: 30817251]
[20]
Yang A, Farmer E, Wu TC, Hung C-F. Perspectives for therapeutic HPV vaccine development. J Biomed Sci 2016; 23(1): 75.
[http://dx.doi.org/10.1186/s12929-016-0293-9] [PMID: 27809842]
[21]
Hargadon KM, Johnson CE, Williams CJ. Immune checkpoint blockade therapy for cancer: An overview of FDA-approved immune checkpoint inhibitors. Int Immunopharmacol 2018; 62: 29-39.
[http://dx.doi.org/10.1016/j.intimp.2018.06.001] [PMID: 29990692]
[22]
Karaki S, Anson M, Tran T, et al. Is there still room for cancer vaccines at the era of checkpoint inhibitors. Vaccines (Basel) 2016; 4(4): 37.
[http://dx.doi.org/10.3390/vaccines4040037] [PMID: 27827885]
[23]
Duperret EK, Wise MC, Trautz A, et al. Synergy of immune checkpoint blockade with a novel synthetic consensus DNA vaccine targeting TERT. Mol Ther 2018; 26(2): 435-45.
[http://dx.doi.org/10.1016/j.ymthe.2017.11.010] [PMID: 29249395]
[24]
Weir GM, Hrytsenko O, Quinton T, Berinstein NL, Stanford MM, Mansour M. Anti-PD-1 increases the clonality and activity of tumor infiltrating antigen specific T cells induced by a potent immune therapy consisting of vaccine and metronomic cyclophosphamide. J Immunother Cancer 2016; 4(1): 68.
[http://dx.doi.org/10.1186/s40425-016-0169-2] [PMID: 27777777]
[25]
Sun N-Y, Chen Y-L, Lin H-W, et al. Immune checkpoint Ab enhances the antigen-specific anti-tumor effects by modulating both dendritic cells and regulatory T lymphocytes. Cancer Lett 2019; 444: 20-34.
[http://dx.doi.org/10.1016/j.canlet.2018.11.039] [PMID: 30543813]
[26]
Garon EB, Rizvi NA, Hui R, et al. Pembrolizumab for the treatment of non-small-cell lung cancer. N Engl J Med 2015; 372(21): 2018-28.
[http://dx.doi.org/10.1056/NEJMoa1501824] [PMID: 25891174]
[27]
Robert C, Ribas A, Wolchok JD, et al. Anti-programmed-death-receptor-1 treatment with pembrolizumab in ipilimumab-refractory advanced melanoma: A randomised dose-comparison cohort of a phase 1 trial. Lancet 2014; 384(9948): 1109-17.
[http://dx.doi.org/10.1016/S0140-6736(14)60958-2] [PMID: 25034862]
[28]
Gandhi L, Rodríguez-Abreu D, Gadgeel S, Esteban E, Felip E, De Angelis F, et al. John Vida, Ziwen Wei, Jing Yang, Harry Raftopoulos, M Catherine Pietanza, and Marina C Garassino. KEYNOTE 189 (adeno): Pembrolizumab plus Chemotherapy (carbo/pemetrexed) in Metastatic Non-Small-Cell Lung Cancer (adeno). N Engl J Med 378: 22.
[29]
Chao J, Chen Y, Frankel PH, et al. Combining pembrolizumab and palliative radiotherapy in gastroesophageal cancer to enhance anti-tumor T-cell response and augment the abscopal effect. J Clin Oncol 2017; 35(4)(Suppl.): 35.
[http://dx.doi.org/10.1200/JCO.2017.35.4_suppl.TPS220]
[30]
Gangadhar TC, Hamid O, Smith DC, et al. Preliminary results from a Phase I/II study of epacadostat (incb024360) in combination with pembrolizumab in patients with selected advanced cancers. J Immunother Cancer 2015; 3(2): 1-2.
[http://dx.doi.org/10.1186/2051-1426-3-S2-O7]
[31]
Robert C, Schachter J, Long GV, et al. Pembrolizumab versus Ipilimumab in Advanced Melanoma. N Engl J Med 2015; 372(26): 2521-32.
[http://dx.doi.org/10.1056/NEJMoa1503093] [PMID: 25891173]
[32]
Choueiri TK, Hodi FS, Thompson JA, et al. Pembrolizumab (pembro) plus low-dose ipilimumab (ipi) for patients (pts) with advanced renal cell carcinoma (RCC): Phase 1 KEYNOTE-029 study. J Clin Oncol 2017; 35(6)(Suppl.): 510-0.
[http://dx.doi.org/10.1200/JCO.2017.35.6_suppl.510]
[33]
Tolcher AW, Sznol M, Hu-Lieskovan S, et al. Phase Ib study of utomilumab (PF-05082566), a 4-1BB/CD137 agonist, in combination with pembrolizumab (MK-3475) in patients with advanced solid tumors. Clin Cancer Res 2017; 23(18): 5349-57.
[http://dx.doi.org/10.1158/1078-0432.CCR-17-1243] [PMID: 28634283]
[34]
Harrington KJ, Kong A, Mach N, Rordorf T, Jaime JC, Espeli V, et al. Safety and preliminary efficacy of talimogene laherparepvec (T-VEC) in combination (combo) with pembrobrolizumab (Pembro) in patients (pts) with recurrent or metastatic squamous cell carcinoma of the head and neck (R/M HNSCC): A multicenter, phase 1b study (MASTERKEY-232). J Clin Oncol 2018; 36(15 Suppl.): 6036-.
[http://dx.doi.org/10.1200/JCO.2018.36.15_suppl.6036]
[35]
Long GV, Dummer R, Ribas A, et al. A Phase I/III, multicenter, open-label trial of talimogene laherparepvec (T-VEC) in combination with pembrolizumab for the treatment of unresected, stage IIIb-IV melanoma (MASTERKEY-265). J Immunother Cancer 2015; 3(2): 1-2.
[http://dx.doi.org/10.1186/2051-1426-3-S2-P181]
[36]
Ribas A, Medina T, Kummar S, et al. SD-101 in combination with pembrolizumab in advanced melanoma: Results of a phase Ib, multicenter study. Cancer Discov 2018; 8(10): 1250-7.
[http://dx.doi.org/10.1158/2159-8290.CD-18-0280] [PMID: 30154193]
[37]
McNeel DG, Eickhoff JC, Jeraj R, et al. DNA vaccine with pembrolizumab to elicit antitumor responses in patients with metastatic, castration-resistant prostate cancer (mCRPC). J Clin Oncol 2017; 35(7)(Suppl.): 168.
[http://dx.doi.org/10.1200/JCO.2017.35.7_suppl.168]
[38]
Ansell SM, Lesokhin AM, Borrello I, et al. PD-1 blockade with nivolumab in relapsed or refractory Hodgkin’s lymphoma. N Engl J Med 2015; 372(4): 311-9.
[http://dx.doi.org/10.1056/NEJMoa1411087] [PMID: 25482239]
[39]
Motzer RJ, Escudier B, McDermott DF, et al. Nivolumab versus everolimus in advanced renal-cell carcinoma. N Engl J Med 2015; 373(19): 1803-13.
[http://dx.doi.org/10.1056/NEJMoa1510665] [PMID: 26406148]
[40]
Kok M, Horlings H, Van de Vijver K, et al. Adaptive phase II randomized non-comparative trial of nivolumab after induction treatment in triple negative breast cancer: TONIC-trial. Ann Oncol 2017; 28: v608.
[http://dx.doi.org/10.1093/annonc/mdx440.006]
[41]
Nivolumab with or without varlilumab in treating patients with relapsed or refractory aggressive B-cell lymphomas. National Cancer Institute. 2017. Available from: https://clinicaltrials.gov/ct2/show/NCT03038672 Accessed on October 28, 2017.
[42]
Larkin J, Chiarion-Sileni V, Gonzalez R, et al. Combined nivolumab and ipilimumab or monotherapy in untreated melanoma [published online May 31. N Engl J Med 2015; 373(1): 23-34.
[http://dx.doi.org/10.1056/NEJMoa1504030]
[43]
Tchekmedyian N, Gray JE, Creelan BC, et al. Propelling immunotherapy combinations into the clinic. Oncology (Williston Park) 2015; 29(12): 990-1002.
[PMID: 26680224]
[44]
Weber JS, Kudchadkar RR, Yu B, et al. Safety, efficacy, and biomarkers of nivolumab with vaccine in ipilimumab-refractory or -naive melanoma. J Clin Oncol 2013; 31(34): 4311-8.
[http://dx.doi.org/10.1200/JCO.2013.51.4802] [PMID: 24145345]
[45]
Massarelli E, William W, Johnson F, et al. Combining immune checkpoint blockade and tumor-specific vaccine for patients with incurable human papillomavirus 16-related cancer: A phase 2 clinical trial. JAMA Oncol 2019; 5(1): 67-73.
[http://dx.doi.org/10.1001/jamaoncol.2018.4051] [PMID: 30267032]
[46]
Bassani-Sternberg M, Digklia A, Huber F, et al. A phase Ib study of the combination of personalized autologous dendritic cell vaccine, aspirin, and standard of care adjuvant chemotherapy followed by nivolumab for resected pancreatic adenocarcinoma-a proof of antigen discovery feasibility in three patients. Front Immunol 2019; 10: 1832.
[http://dx.doi.org/10.3389/fimmu.2019.01832] [PMID: 31440238]
[47]
Kudchadkar RR, Gallenstein D, Martinez AJ, Yu B, Weber JS. Phase I trial of extended-dose anti-PD-1 antibody BMS-936558 with a multipeptide vaccine for previously treated stage IV melanoma. J Clin Oncol 2012; 30(15 Suppl.): 8582-2.
[http://dx.doi.org/10.1200/jco.2012.30.15_suppl.8582]
[48]
Gibney GT, Kudchadkar RR, DeConti RC, et al. Safety, correlative markers, and clinical results of adjuvant nivolumab in combination with vaccine in resected high-risk metastatic melanoma. Clin Cancer Res 2015; 21(4): 712-20.
[http://dx.doi.org/10.1158/1078-0432.CCR-14-2468] [PMID: 25524312]
[49]
Hsueh EC, Essner R, Foshag LJ, et al. Prolonged survival after complete resection of disseminated melanoma and active immunotherapy with a therapeutic cancer vaccine. J Clin Oncol 2002; 20(23): 4549-54.
[http://dx.doi.org/10.1200/JCO.2002.01.151] [PMID: 12454111]
[50]
Sosman JA, Moon J, Tuthill RJ, et al. A phase 2 trial of complete resection for stage IV melanoma: results of southwest oncology group clinical trial S9430. Cancer 2011; 117(20): 4740-06.
[http://dx.doi.org/10.1002/cncr.26111] [PMID: 21455999]
[51]
Strbo N, Garcia-Soto A, Schreiber TH, Podack ER. Secreted heat shock protein gp96-Ig: Next-generation vaccines for cancer and infectious diseases. Immunol Res 2013; 57(1-3): 311-25.
[http://dx.doi.org/10.1007/s12026-013-8468-x] [PMID: 24254084]
[52]
Bahce I, Hashemi S, Fransen M, et al. 1390P Impact of adding viagenpumatucel-L to nivolumab in non-small cell lung cancer (NSCLC) patients with low levels of tumour infiltrating lymphocytes. Ann Oncol 2020; 31: S883.
[http://dx.doi.org/10.1016/j.annonc.2020.08.1704]
[53]
Srinivasan VM, Ferguson SD, Lee S, Weathers S-P, Kerrigan BCP, Heimberger AB. Tumor vaccines for malignant gliomas. Neurotherapeutics 2017; 14(2): 345-57.
[http://dx.doi.org/10.1007/s13311-017-0522-2] [PMID: 28389997]
[54]
Remy-Ziller C, Thioudellet C, Hortelano J, et al. Sequential administration of MVA-based vaccines and PD-1/PD-L1-blocking antibodies confers measurable benefits on tumor growth and survival: Preclinical studies with MVA-βGal and MVA-MUC1 (TG4010) in a murine tumor model. Hum Vaccin Immunother 2018; 14(1): 140-5.
[http://dx.doi.org/10.1080/21645515.2017.1373921] [PMID: 28925793]
[55]
McNeel DG, Eickhoff JC, Wargowski E, et al. Concurrent, but not sequential, PD-1 blockade with a DNA vaccine elicits anti-tumor responses in patients with metastatic, castration-resistant prostate cancer. Oncotarget 2018; 9(39): 25586-96.
[http://dx.doi.org/10.18632/oncotarget.25387] [PMID: 29876010]
[56]
Wada S, Jackson CM, Yoshimura K, et al. Sequencing CTLA-4 blockade with cell-based immunotherapy for prostate cancer. J Transl Med 2013; 11(1): 89.
[http://dx.doi.org/10.1186/1479-5876-11-89] [PMID: 23557194]
[57]
Hodi FS, O’Day SJ, McDermott DF, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 2010; 363(8): 711-23.
[http://dx.doi.org/10.1056/NEJMoa1003466] [PMID: 20525992]
[58]
Zakharia Y, Drabick JJ, Khleif S, et al. Updates on phase1b/2 trial of the indoleamine 2,3-dioxygenase pathway (IDO) inhibitor indoximod plus checkpoint inhibitors for the treatment of unresectable stage 3 or 4 melanoma. J Clin Oncol 2016; 34(15 Suppl.): 3075.
[http://dx.doi.org/10.1200/JCO.2016.34.15_suppl.3075]
[59]
Curti B, Richards J, Faries M, et al. The MITCI (phase 1b) study: A novel immunotherapy combination of coxsackievirus A21 and ipilimumab in patients with advanced melanoma. Ann Oncol 2016; 27: vi360.
[http://dx.doi.org/10.1093/annonc/mdw378.06]
[60]
Long GV, Atkinson V, Cebon JS, et al. Standard-dose pembrolizumab in combination with reduced-dose ipilimumab for patients with advanced melanoma (KEYNOTE-029): An open-label, phase 1b trial. Lancet Oncol 2017; 18(9): 1202-10.
[http://dx.doi.org/10.1016/S1470-2045(17)30428-X] [PMID: 28729151]
[61]
Sarnaik AA, Yu B, Yu D, et al. Extended dose ipilimumab with a peptide vaccine: Immune correlates associated with clinical benefit in patients with resected high-risk stage IIIc/IV melanoma. Clin Cancer Res 2011; 17(4): 896-906.
[http://dx.doi.org/10.1158/1078-0432.CCR-10-2463] [PMID: 21106722]
[62]
Bjoern J, Iversen TZ, Nitschke NJ, Andersen MH, Svane IM. Safety, immune and clinical responses in metastatic melanoma patients vaccinated with a long peptide derived from indoleamine 2,3-dioxygenase in combination with ipilimumab. Cytotherapy 2016; 18(8): 1043-55.
[http://dx.doi.org/10.1016/j.jcyt.2016.05.010] [PMID: 27378345]
[63]
Wilgenhof S, Corthals J, Heirman C, et al. Phase II study of autologous monocyte-derived mRNA electroporated dendritic cells (TriMixDC-MEL) plus ipilimumab in patients with pretreated advanced melanoma. J Clin Oncol 2016; 34(12): 1330-8.
[http://dx.doi.org/10.1200/JCO.2015.63.4121] [PMID: 26926680]
[64]
Singh H, Madan RA, Dahut WL, Coyne GHOS, Rauckhorst M, McMahon S, et al. Combining active immunotherapy and immune checkpoint inhibitors in prostate cancer. J Clin Oncol 2015; 33(15): e14008.
[http://dx.doi.org/10.1200/jco.2015.33.15_suppl.e14008]
[65]
Scholz M, Yep S, Chancey M, et al. Phase I clinical trial of sipuleucel-T combined with escalating doses of ipilimumab in progressive metastatic castrate-resistant prostate cancer. ImmunoTargets Ther 2017; 6: 11-6.
[http://dx.doi.org/10.2147/ITT.S122497] [PMID: 28361045]
[66]
Gerritsen W, Van Den Eertwegh A, De Gruijl T, et al. Expanded phase I combination trial of GVAX immunotherapy for prostate cancer and ipilimumab in patients with metastatic hormone-refractory prostate cancer (mHPRC). J Clin Oncol 2008; 26(15)(Suppl.): 5146.
[http://dx.doi.org/10.1200/jco.2008.26.15_suppl.5146]
[67]
Puzanov I, Diab A, Abdallah K, et al. Managing toxicities associated with immune checkpoint inhibitors: Consensus recommendations from the Society for Immunotherapy of Cancer (SITC) Toxicity Management Working Group. J Immunother Cancer 2017; 5(1): 95.
[http://dx.doi.org/10.1186/s40425-017-0300-z] [PMID: 29162153]
[68]
Le DT, Lutz E, Uram JN, Sugar EA, Onners B, Solt S, et al. Evaluation of ipilimumab in combination with allogeneic pancreatic tumor cells transfected with a GM-CSF gene in previously treated pancreatic cancer. Journal of immunotherapy (Hagerstown, Md: 1997) 2013; 36(7): 382.
[http://dx.doi.org/10.1097/CJI.0b013e31829fb7a2]
[69]
van den Eertwegh AJ, Versluis J, van den Berg HP, et al. Combined immunotherapy with granulocyte-macrophage colony-stimulating factor-transduced allogeneic prostate cancer cells and ipilimumab in patients with metastatic castration-resistant prostate cancer: A phase 1 dose-escalation trial. Lancet Oncol 2012; 13(5): 509-17.
[http://dx.doi.org/10.1016/S1470-2045(12)70007-4] [PMID: 22326922]
[70]
Papachristofilou A, Hipp MM, Klinkhardt U, et al. Phase Ib evaluation of a self-adjuvanted protamine formulated mRNA-based active cancer immunotherapy, BI1361849 (CV9202), combined with local radiation treatment in patients with stage IV non-small cell lung cancer. J Immunother Cancer 2019; 7(1): 38.
[http://dx.doi.org/10.1186/s40425-019-0520-5] [PMID: 30736848]
[71]
Andrews LP, Marciscano AE, Drake CG, Vignali DA. LAG3 (CD223) as a cancer immunotherapy target. Immunol Rev 2017; 276(1): 80-96.
[http://dx.doi.org/10.1111/imr.12519] [PMID: 28258692]
[72]
Das M, Zhu C, Kuchroo VK. Tim-3 and its role in regulating anti-tumor immunity. Immunol Rev 2017; 276(1): 97-111.
[http://dx.doi.org/10.1111/imr.12520] [PMID: 28258697]
[73]
Andrews LP, Yano H, Vignali DAA. Inhibitory receptors and ligands beyond PD-1, PD-L1 and CTLA-4: Breakthroughs or backups. Nat Immunol 2019; 20(11): 1425-34.
[http://dx.doi.org/10.1038/s41590-019-0512-0] [PMID: 31611702]
[74]
Maruhashi T, Sugiura D, Okazaki IM, Okazaki T. LAG-3: From molecular functions to clinical applications. J Immunother Cancer 2020; 8(2): e001014.
[http://dx.doi.org/10.1136/jitc-2020-001014] [PMID: 32929051]
[75]
Foy SP, Sennino B, dela Cruz T, et al. Poxvirus-based active immunotherapy with PD-1 and LAG-3 dual immune checkpoint inhibition overcomes compensatory immune regulation, yielding complete tumor regression in mice. PLoS One 2016; 11(2): e0150084.
[http://dx.doi.org/10.1371/journal.pone.0150084] [PMID: 26910562]
[76]
Legat A, Maby-El Hajjami H, Baumgaertner P, et al. Vaccination with LAG-3Ig (IMP321) and peptides induces specific CD4 and CD8 T-cell responses in metastatic melanoma patients-report of a phase I/IIa clinical trial. Clin Cancer Res 2016; 22(6): 1330-40.
[http://dx.doi.org/10.1158/1078-0432.CCR-15-1212] [PMID: 26500235]
[77]
Bonaventura P, Shekarian T, Alcazer V, et al. Cold tumors: A therapeutic challenge for immunotherapy. Front Immunol 2019; 10: 168.
[http://dx.doi.org/10.3389/fimmu.2019.00168] [PMID: 30800125]
[78]
Snyder A, Makarov V, Merghoub T, et al. Genetic basis for clinical response to CTLA-4 blockade in melanoma. N Engl J Med 2014; 371(23): 2189-99.
[http://dx.doi.org/10.1056/NEJMoa1406498] [PMID: 25409260]
[79]
Le DT, Durham JN, Smith KN, et al. Mismatch repair deficiency predicts response of solid tumors to PD-1 blockade. Science 2017; 357(6349): 409-13.
[http://dx.doi.org/10.1126/science.aan6733] [PMID: 28596308]
[80]
Santegoets SJ, Stam AG, Lougheed SM, et al. T cell profiling reveals high CD4+CTLA-4 + T cell frequency as dominant predictor for survival after prostate GVAX/ipilimumab treatment. Cancer Immunol Immunother 2013; 62(2): 245-56.
[http://dx.doi.org/10.1007/s00262-012-1330-5] [PMID: 22878899]
[81]
Principe DR, Chiec L, Mohindra NA, Munshi HG. Regulatory T-cells as an emerging barrier to immune checkpoint inhibition in lung cancer. Front Oncol 2021; 11: 684098.
[http://dx.doi.org/10.3389/fonc.2021.684098] [PMID: 34141625]
[82]
Choucair K, Morand S, Stanbery L, Edelman G, Dworkin L, Nemunaitis J. TMB: A promising immune-response biomarker, and potential spearhead in advancing targeted therapy trials. Cancer Gene Ther 2020; 27(12): 841-53.
[http://dx.doi.org/10.1038/s41417-020-0174-y] [PMID: 32341410]
[83]
Bai R, Lv Z, Xu D, Cui J. Predictive biomarkers for cancer immunotherapy with immune checkpoint inhibitors. Biomark Res 2020; 8(1): 34.
[http://dx.doi.org/10.1186/s40364-020-00209-0] [PMID: 32864131]
[84]
Galluzzi L, Buqué A, Kepp O, Zitvogel L, Kroemer G. Immunological effects of conventional chemotherapy and targeted anticancer agents. Cancer Cell 2015; 28(6): 690-714.
[http://dx.doi.org/10.1016/j.ccell.2015.10.012] [PMID: 26678337]
[85]
Zitvogel L, Kroemer G. Anticancer immunochemotherapy using adjuvants with direct cytotoxic effects. J Clin Invest 2009; 119(8): 2127-30.
[http://dx.doi.org/10.1172/JCI39991] [PMID: 19620780]
[86]
Emens LA, Middleton G. The interplay of immunotherapy and chemotherapy: Harnessing potential synergies. Cancer Immunol Res 2015; 3(5): 436-43.
[http://dx.doi.org/10.1158/2326-6066.CIR-15-0064] [PMID: 25941355]
[87]
Lutsiak ME, Semnani RT, De Pascalis R, Kashmiri SV, Schlom J, Sabzevari H. Inhibition of CD4(+)25+ T regulatory cell function implicated in enhanced immune response by low-dose cyclophosphamide. Blood 2005; 105(7): 2862-8.
[http://dx.doi.org/10.1182/blood-2004-06-2410] [PMID: 15591121]
[88]
Welters MJ, van der Sluis TC, van Meir H, Loof NM, van Ham VJ, van Duikeren S, et al. Vaccination during myeloid cell depletion by cancer chemotherapy fosters robust T cell responses. Science translational medicine 2016; 8(334): 334ra52-ra52.
[http://dx.doi.org/10.1126/scitranslmed.aad8307]
[89]
Garnett CT, Schlom J, Hodge JW. Combination of docetaxel and recombinant vaccine enhances T-cell responses and antitumor activity: Effects of docetaxel on immune enhancement. Clin Cancer Res 2008; 14(11): 3536-44.
[http://dx.doi.org/10.1158/1078-0432.CCR-07-4025] [PMID: 18519787]
[90]
Heery CR, Ibrahim NK, Arlen PM, et al. Docetaxel alone or in combination with a therapeutic cancer vaccine (PANVAC) in patients with metastatic breast cancer: A randomized clinical trial. JAMA Oncol 2015; 1(8): 1087-95.
[http://dx.doi.org/10.1001/jamaoncol.2015.2736] [PMID: 26291768]
[91]
Harrop R, Chu F, Gabrail N, Srinivas S, Blount D, Ferrari A. Vaccination of castration-resistant prostate cancer patients with TroVax (MVA-5T4) in combination with docetaxel: A randomized phase II trial. Cancer Immunol Immunother 2013; 62(9): 1511-20.
[http://dx.doi.org/10.1007/s00262-013-1457-z] [PMID: 23877659]
[92]
Hardacre JM, Mulcahy M, Small W, et al. Addition of algenpantucel-L immunotherapy to standard adjuvant therapy for pancreatic cancer: A phase 2 study. J Gastrointest Surg 2013; 17(1): 94-100.
[http://dx.doi.org/10.1007/s11605-012-2064-6] [PMID: 23229886]
[93]
Regine WF, Winter KA, Abrams RA, et al. Fluorouracil vs gemcitabine chemotherapy before and after fluorouracil-based chemoradiation following resection of pancreatic adenocarcinoma: A randomized controlled trial. JAMA 2008; 299(9): 1019-26.
[http://dx.doi.org/10.1001/jama.299.9.1019] [PMID: 18319412]
[94]
Dijkgraaf EM, Santegoets SJ, Reyners AK, et al. A phase 1/2 study combining gemcitabine, Pegintron and p53 SLP vaccine in patients with platinum-resistant ovarian cancer. Oncotarget 2015; 6(31): 32228-43.
[http://dx.doi.org/10.18632/oncotarget.4772] [PMID: 26334096]
[95]
Rocha-Lima CM, de Queiroz Marques E Junior, Bayraktar S, et al. A multicenter phase II study of G17DT immunogen plus irinotecan in pretreated metastatic colorectal cancer progressing on irinotecan. Cancer Chemother Pharmacol 2014; 74(3): 479-86.
[http://dx.doi.org/10.1007/s00280-014-2520-y] [PMID: 25030089]
[96]
Chen G, Gupta R, Petrik S, et al. A feasibility study of cyclophosphamide, trastuzumab, and an allogeneic GM-CSF-secreting breast tumor vaccine for HER2+ metastatic breast cancer. Cancer Immunol Res 2014; 2(10): 949-61.
[http://dx.doi.org/10.1158/2326-6066.CIR-14-0058] [PMID: 25116755]
[97]
Huang C, Yu AL, Tseng L, et al. Randomized phase II/III trial of active immunotherapy with OPT-822/OPT-821 in patients with metastatic breast cancer. J Clin Oncol 2016; 34(15)(Suppl.): 1003-3.
[http://dx.doi.org/10.1200/JCO.2016.34.15_suppl.1003]
[98]
Carmeliet P, Jain RK. Molecular mechanisms and clinical applications of angiogenesis. Nature 2011; 473(7347): 298-307.
[http://dx.doi.org/10.1038/nature10144] [PMID: 21593862]
[99]
Welti J, Loges S, Dimmeler S, Carmeliet P. Recent molecular discoveries in angiogenesis and antiangiogenic therapies in cancer. J Clin Invest 2013; 123(8): 3190-200.
[http://dx.doi.org/10.1172/JCI70212] [PMID: 23908119]
[100]
Huang Y, Yuan J, Righi E, et al. Vascular normalizing doses of antiangiogenic treatment reprogram the immunosuppressive tumor microenvironment and enhance immunotherapy. Proc Natl Acad Sci USA 2012; 109(43): 17561-6.
[http://dx.doi.org/10.1073/pnas.1215397109] [PMID: 23045683]
[101]
Amin A, Dudek AZ, Logan TF, et al. Survival with AGS-003, an autologous dendritic cell-based immunotherapy, in combination with sunitinib in unfavorable risk patients with advanced renal cell carcinoma (RCC): Phase 2 study results. J Immunother Cancer 2015; 3(1): 14.
[http://dx.doi.org/10.1186/s40425-015-0055-3] [PMID: 25901286]
[102]
DiPaola RS, Chen Y-H, Bubley GJ, et al. A national multicenter phase 2 study of prostate-specific antigen (PSA) pox virus vaccine with sequential androgen ablation therapy in patients with PSA progression: ECOG 9802. Eur Urol 2015; 68(3): 365-71.
[http://dx.doi.org/10.1016/j.eururo.2014.12.010] [PMID: 25533418]
[103]
Madan RA, Gulley JL, Schlom J, et al. Analysis of overall survival in patients with nonmetastatic castration-resistant prostate cancer treated with vaccine, nilutamide, and combination therapy. Clin Cancer Res 2008; 14(14): 4526-31.
[http://dx.doi.org/10.1158/1078-0432.CCR-07-5048] [PMID: 18628467]
[104]
Chakraborty M, Abrams SI, Camphausen K, et al. Irradiation of tumor cells up-regulates Fas and enhances CTL lytic activity and CTL adoptive immunotherapy. J Immunol 2003; 170(12): 6338-47.
[http://dx.doi.org/10.4049/jimmunol.170.12.6338] [PMID: 12794167]
[105]
Chakraborty M, Abrams SI, Coleman CN, Camphausen K, Schlom J, Hodge JW. External beam radiation of tumors alters phenotype of tumor cells to render them susceptible to vaccine-mediated T-cell killing. Cancer Res 2004; 64(12): 4328-37.
[http://dx.doi.org/10.1158/0008-5472.CAN-04-0073] [PMID: 15205348]
[106]
Gameiro SR, Jammeh ML, Wattenberg MM, Tsang KY, Ferrone S, Hodge JW. Radiation-induced immunogenic modulation of tumor enhances antigen processing and calreticulin exposure, resulting in enhanced T-cell killing. Oncotarget 2014; 5(2): 403-16.
[http://dx.doi.org/10.18632/oncotarget.1719] [PMID: 24480782]
[107]
Sebastian M, Papachristofilou A, Weiss C, et al. Phase Ib study evaluating a self-adjuvanted mRNA cancer vaccine (RNActive®) combined with local radiation as consolidation and maintenance treatment for patients with stage IV non-small cell lung cancer. BMC Cancer 2014; 14(1): 748.
[http://dx.doi.org/10.1186/1471-2407-14-748] [PMID: 25288198]
[108]
Heery CR, Madan RA, Bilusic M, et al. Interim analysis of a phase II randomized clinical trial of samrium-153 (Sm-153) with or without PSA-TRICOM vaccine in metastatic castration-resistant prostate cancer after docetaxel. J Clin Oncol 2012; 30(15)(Suppl.): 2526-6.
[http://dx.doi.org/10.1200/jco.2012.30.15_suppl.2526]
[109]
Heery CR, Madan RA, Stein MN, et al. Samarium-153-EDTMP (Quadramet®) with or without vaccine in metastatic castration-resistant prostate cancer: A randomized Phase 2 trial. Oncotarget 2016; 7(42): 69014-23.
[http://dx.doi.org/10.18632/oncotarget.10883] [PMID: 27486817]
[110]
Yu T-W, Chueh H-Y, Tsai C-C, Lin C-T, Qiu JT. Novel GM-CSF-based vaccines: One small step in GM-CSF gene optimization, one giant leap for human vaccines. Hum Vaccin Immunother 2016; 12(12): 3020-8.
[http://dx.doi.org/10.1080/21645515.2016.1221551] [PMID: 27560197]
[111]
Atkins MB, Lotze MT, Dutcher JP, et al. High-dose recombinant interleukin 2 therapy for patients with metastatic melanoma: Analysis of 270 patients treated between 1985 and 1993. J Clin Oncol 1999; 17(7): 2105-16.
[http://dx.doi.org/10.1200/JCO.1999.17.7.2105] [PMID: 10561265]
[112]
Schwartzentruber DJ, Lawson DH, Richards JM, et al. gp100 peptide vaccine and interleukin-2 in patients with advanced melanoma. N Engl J Med 2011; 364(22): 2119-27.
[http://dx.doi.org/10.1056/NEJMoa1012863] [PMID: 21631324]
[113]
Baek S, Kim CS, Kim SB, et al. Combination therapy of renal cell carcinoma or breast cancer patients with dendritic cell vaccine and IL-2: Results from a phase I/II trial. J Transl Med 2011; 9(1): 178.
[http://dx.doi.org/10.1186/1479-5876-9-178] [PMID: 22013914]
[114]
Hoeller C, Michielin O, Ascierto PA, Szabo Z, Blank CU. Systematic review of the use of granulocyte-macrophage colony-stimulating factor in patients with advanced melanoma. Cancer Immunol Immunother 2016; 65(9): 1015-34.
[http://dx.doi.org/10.1007/s00262-016-1860-3] [PMID: 27372293]
[115]
Lawson DH, Lee S, Zhao F, et al. Randomized, placebo-controlled, Phase III trial of yeast-derived granulocyte-macrophage colony-stimulating factor (GM-CSF) versus peptide vaccination versus GM-CSF plus peptide vaccination versus placebo in patients with no evidence of disease after complete surgical resection of locally advanced and/or stage IV melanoma: A trial of the Eastern Cooperative Oncology Group-American College of Radiology Imaging Network Cancer Research Group (E4697). J Clin Oncol 2015; 33(34): 4066-76.
[http://dx.doi.org/10.1200/JCO.2015.62.0500] [PMID: 26351350]
[116]
Adams S. Toll-like receptor agonists in cancer therapy. Immunotherapy 2009; 1(6): 949-64.
[http://dx.doi.org/10.2217/imt.09.70] [PMID: 20563267]
[117]
Gableh F, Saeidi M, Hemati S, et al. Combination of the toll like receptor agonist and α-Galactosylceramide as an efficient adjuvant for cancer vaccine. J Biomed Sci 2016; 23(1): 16.
[http://dx.doi.org/10.1186/s12929-016-0238-3] [PMID: 26811064]

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