Cancer immunotherapy beyond immune checkpoint inhibitors

Journal of Hematology and Oncology

Volumn 11, Issue 1, 2018, Pages

  Marin Acevedo, Julian A ^a   Soyano, Aixa E ^a   Dholaria, Bhagirathbhai ^a,b   Knutson, Keith L ^a   Lou, Yanyan ^a  

^a MAYO CLINIC   (United States)

^b H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

Author keywords

Antibody drug conjugates; Chimeric antigen receptor therapy; Immunotherapy; Oncolytic viruses; Tumor vaccines; Tumor directed monoclonal antibodies; Viral gene therapy

Indexed keywords

ABBV 221; ABBV 339; ADCT 301; AFM13; ANTINEOPLASTIC MONOCLONAL ANTIBODY; ASG 22CE; ASG 22ME; BAY 2010112; BLINATUMOMAB; CD133 ANTIGEN; CD19 ANTIGEN; CHECKPOINT KINASE INHIBITOR; ENFORTUMAB; ENSITUXIMAB; ERLOTINIB; GLEMBATUMUMAB; GLEMBATUMUMAB VEDOTIN; INOTUZUMAB OZOGAMICIN; INTERCELLULAR ADHESION MOLECULE 1; LABETUZUMAB GOVITECAN; LORVOTUZUMAB MERTANSINE; LOSATUXIZUMAB; MEDI 4276; MIRVETUXIMAB; MIRVETUXIMAB SORAVTANSINE; OBINUTUZUMAB; RG 7802; RO 6958688; ROVALPITUZUMAB TESIRINE; SACITUZUMAB GOVITECAN; SORAVTANSINE; UNCLASSIFIED DRUG; UNINDEXED DRUG; VEDOTIN; XMT 1522; ANTIBODY CONJUGATE; CANCER VACCINE; IMMUNOLOGICAL ANTINEOPLASTIC AGENT;

ALOPECIA; ANEMIA; ANTINEOPLASTIC ACTIVITY; APHASIA; BRAIN DISEASE; CANCER IMMUNOTHERAPY; CASTRATION RESISTANT PROSTATE CANCER; COLORECTAL CANCER; DIARRHEA; DIFFUSE LARGE B CELL LYMPHOMA; DRUG PROTEIN BINDING; DRUG SAFETY; DRUG TOLERABILITY; ENTERITIS; EPITHELIUM TUMOR; FATIGUE; FEBRILE NEUTROPENIA; FEVER; GENE THERAPY; HODGKIN DISEASE; HUMAN; INFUSION RELATED REACTION; MELANOMA; MUCOSA INFLAMMATION; NEUROPATHY; NEUTROPENIA; NON SMALL CELL LUNG CANCER; NONHODGKIN LYMPHOMA; NONHUMAN; OVARY CANCER; PANCREAS CANCER; PERICARDIAL EFFUSION; PERIPHERAL NEUROPATHY; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PLEURA EFFUSION; PROTEIN TARGETING; RASH; REVIEW; SMALL CELL LUNG CANCER; SOLID MALIGNANT NEOPLASM; THROMBOCYTOPENIA; TREATMENT INDICATION; TREATMENT OUTCOME; TREATMENT RESPONSE; TUMOR ASSOCIATED LEUKOCYTE; TUMOR MICROENVIRONMENT; UNSPECIFIED SIDE EFFECT; UROGENITAL TRACT TUMOR; ADOPTIVE IMMUNOTHERAPY; ANIMAL; IMMUNOLOGY; IMMUNOTHERAPY; NEOPLASM; ONCOLYTIC VIROTHERAPY; PATHOLOGY; PROCEDURES;

ANIMALS; ANTINEOPLASTIC AGENTS, IMMUNOLOGICAL; CANCER VACCINES; HUMANS; IMMUNOCONJUGATES; IMMUNOTHERAPY; IMMUNOTHERAPY, ADOPTIVE; NEOPLASMS; ONCOLYTIC VIROTHERAPY;

EID: 85040457867     PISSN: None     EISSN: 17568722     Source Type: Journal    
DOI: 10.1186/s13045-017-0552-6     Document Type: Review

References (145)

1. Khalil DN, Smith EL, Brentjens RJ, Wolchok JD. The future of cancer treatment: immunomodulation, CARs and combination immunotherapy. Nat Rev Clin Oncol. 2016;13:273-90.
2. Dholaria B, Hammond W, Shreders A, Lou Y. Emerging therapeutic agents for lung cancer. J Hematol Oncol. 2016;9:138.
3. Sharma P, Allison JP. The future of immune checkpoint therapy. Science. 2015;348:56-61.
4. Scott AM, Allison JP, Wolchok JD. Monoclonal antibodies in cancer therapy. Cancer Immun. 2012;12:14.
5. Weidle UH, Kontermann RE, Brinkmann U. Tumor-antigen-binding bispecific antibodies for cancer treatment. Semin Oncol. 2014;41:653-60.
6. Zhang X, Yang Y, Fan D, Xiong D. The development of bispecific antibodies and their applications in tumor immune escape. Exp Hematol Oncol. 2017;6:12.
7. Fan G, Wang Z, Hao M, Li J. Bispecific antibodies and their applications. J Hematol Oncol. 2015;8:130.
8. Moore PA, Zhang WJ, Rainey GJ, et al. Application of dual affinity retargeting molecules to achieve optimal redirected T-cell killing of B-cell lymphoma. Blood. 2011;117:4542-51.
9. Rader C. DARTs take aim at BiTEs. Blood. 2011;117:4403-4.
10. Kim RD, Arlen PM, Tsang KY, et al. Ensituximab (E) in patients (pts) with refractory metastatic colorectal cancer (mCRC): results of a phase I/II clinical trial. J Clin Oncol. 2017;35:3081.
11. Tabernero J, Melero I, Ros W, et al. Phase Ia and Ib studies of the novel carcinoembryonic antigen (CEA) T-cell bispecific (CEA CD3 TCB) antibody as a single agent and in combination with atezolizumab: preliminary efficacy and safety in patients with metastatic colorectal cancer (mCRC). J Clin Oncol. 2017;35:3002.
12. Wu J, Fu J, Zhang M, Liu D. Blinatumomab: a bispecific T cell engager (BiTE) antibody against CD19/CD3 for refractory acute lymphoid leukemia. J Hematol Oncol. 2015;8:104.
13. Viardot A, Goebeler ME, Hess G, et al. Phase 2 study of the bispecific T-cell engager (BiTE) antibody blinatumomab in relapsed/refractory diffuse large B-cell lymphoma. Blood. 2016;127:1410-6.
14. Tolcher AW, Alley EW, Chichili G, et al. Phase 1, first-in-human, open label, dose escalation study of MGD009, a humanized B7-H3 x CD3 dual-affinity re-targeting (DART) protein in patients with B7-H3-expressing neoplasms or B7-H3 expressing tumor vasculature. J Clin Oncol. 2016;34:TPS3105.
15. Wu J, Fu J, Zhang M, Liu D. AFM13: a first-in-class tetravalent bispecific anti-CD30/CD16A antibody for NK cell-mediated immunotherapy. J Hematol Oncol. 2015;8:96.
16. Rothe A, Sasse S, Topp MS, et al. A phase 1 study of the bispecific anti-CD30/CD16A antibody construct AFM13 in patients with relapsed or refractory Hodgkin lymphoma. Blood. 2015;125:4024-31.
17. Diamantis N, Banerji U. Antibody-drug conjugates-an emerging class of cancer treatment. Br J Cancer. 2016;114:362-7.
18. Angevin E, Strickler JH, Weekes CD, et al. Phase I study of ABBV-399, a c-Met antibody-drug conjugate (ADC), as monotherapy and in combination with erlotinib in patients (pts) with non-small cell lung cancer (NSCLC). J Clin Oncol. 2017;35:2509.
19. Ott PA, Pavlick AC, Johnson DB, et al. A phase II study of glembatumumab vedotin (GV), an antibody-drug conjugate (ADC) targeting gpNMB, in advanced melanoma. J Clin Oncol. 2017;35:109.
20. Calvo E, Cleary JM, Moreno V, et al. Preliminary results from a phase 1 study of the antibody-drug conjugate ABBV-221 in patients with solid tumors likely to express EGFR. J Clin Oncol. 2017;35:2510.
21. O'Malley DM, Moore KN, Vergote I, et al. Safety findings from FORWARD II: a phase 1b study evaluating the folate receptor alpha (FRα)-targeting antibody-drug conjugate (ADC) mirvetuximab soravtansine (IMGN853) in combination with bevacizumab, carboplatin, pegylated liposomal doxorubicin (PLD), or pembrolizumab in patients (pts) with ovarian cancer. J Clin Oncol. 2017;35:5553.
22. Petrylak DP, Perez RP, Zhang J, et al. A phase I study of enfortumab vedotin (ASG-22CE; ASG-22ME): updated analysis of patients with metastatic urothelial cancer. J Clin Oncol. 2017;35:106.
23. Bardia A, Mayer IA, Diamond JR, et al. Efficacy and safety of anti-Trop-2 antibody drug conjugate sacituzumab govitecan (IMMU-132) in heavily pretreated patients with metastatic triple-negative breast cancer. J Clin Oncol. 2017;35:2141-8.
24. Heist RS, Guarino MJ, Masters G, et al. Therapy of advanced non-small-cell lung cancer with an SN-38-anti-Trop-2 drug conjugate, Sacituzumab Govitecan. J Clin Oncol. 2017;35:2790-7.
25. Pazdur R. Inotuzumab ozogamicin (Besponsa) approval letter. In: Drug approvals and Databases. U.S. Food and Drug Administration, Center for Drug Evaluation and Research. 2017. https://www.accessdata.fda.gov/drugsatfda-docs/appletter/2017/761040Orig1s000ltr.pdf. Accessed 3 October 2017.
26. Sangha R, Davies A, Dang NH, et al. Phase 1 study of inotuzumab ozogamicin combined with R-GDP for the treatment of patients with relapsed/refractory CD22+ B-cell non-Hodgkin lymphoma. J Drug Assess. 2017;6:10-7.
27. Dotan E, Cohen SJ, Starodub AN, et al. Phase I/II trial of labetuzumab govitecan (anti-CEACAM5/SN-38 antibody-drug conjugate) in patients with refractory or relapsing metastatic colorectal cancer. J Clin Oncol. 2017;35:3338-46.
28. Socinski MA, Kaye FJ, Spigel DR, et al. Phase 1/2 study of the CD56-targeting antibody-drug conjugate lorvotuzumab mertansine (IMGN901) in combination with carboplatin/etoposide in small-cell lung cancer patients with extensive-stage disease. Clin Lung Cancer. 2017;18:68-76. e62
29. Rudin CM, Pietanza MC, Bauer TM, et al. Rovalpituzumab tesirine, a DLL3-targeted antibody-drug conjugate, in recurrent small-cell lung cancer: a first-in-human, first-in-class, open-label, phase 1 study. Lancet Oncol. 2017;18:42-51.
30. Flynn MJ, Hartley JA. The emerging role of anti-CD25 directed therapies as both immune modulators and targeted agents in cancer. Br J Haematol. 2017;179:20-35.
31. Horwitz SM, Fanale MA, Spira AI, et al. Interim data from the first clinical study of ADCT-301, a novel pyrrolobenzodiazapine-based antibody drug conjugate, in relapsed/refractory Hodgkin/non-Hodgkin lymphoma. Hematol Oncol. 2017;35:270-1.
32. Almhanna K, Wright D, Mercade TM, et al. A phase II study of antibody-drug conjugate, TAK-264 (MLN0264) in previously treated patients with advanced or metastatic pancreatic adenocarcinoma expressing guanylyl cyclase C. Investig New Drugs. 2017;35:634-41.
33. Trail PA, Dubowchik GM, Lowinger TB. Antibody drug conjugates for treatment of breast cancer: novel targets and diverse approaches in ADC design. Pharmacol Ther. 2018;181:126-42.
34. Rose AAN, Biondini M, Curiel R, Siegel PM. Targeting GPNMB with glembatumumab vedotin: current developments and future opportunities for the treatment of cancer. Pharmacol Ther. 2017;179:127-41.
35. Yardley DA, Weaver R, Melisko ME, et al. EMERGE: a randomized phase II study of the antibody-drug conjugate glembatumumab vedotin in advanced glycoprotein NMB-expressing breast cancer. J Clin Oncol. 2015;33:1609-19.
36. Gomez-Roca CA, Boni V, Moreno V, et al. A phase I study of SAR566658, an anti CA6-antibody drug conjugate (ADC), in patients (Pts) with CA6-positive advanced solid tumors (STs) (NCT01156870). J Clin Oncol. 2016;34:2511.
37. Forero A, Burris H III, Mita M, et al. Abstract P3-14-05: interim analysis of a phase 1 study of the antibody-drug conjugate SGN-LIV1A in patients with metastatic breast cancer. Cancer Research. 2016;76:P3-14-05-P13-14-05.
38. Sachdev JC, Maitland M, Sharma M, et al. A phase 1 study of PF-06647020, an antibody-drug conjugate (ADC) targeting protein tyrosine kinase 7 (PTK7), in patients with advanced solid tumors including platinum resistant ovarian cancer (OVCA). Ann Oncol. 2016;27:LBA35.
39. Garrido-Laguna I, Krop IE, Burris H, et al. A phase I study of PF-06647263, a novel EFNA4-ADC, in patients with metastatic triple negative breast cancer. J Clin Oncol. 2017;35:2511.
40. Kogawa T, Yonemori K, Naito Y, et al. Phase 1/2, multicenter, non-randomized, open-label, multiple-dose first-in-human study of U3-1402 (anti-HER3 antibody drug conjugate) in subjects with HER3-positive metastatic breast cancer. J Clin Oncol. 2017;35:TPS1116.
41. Lassen UN, Ramalingam SS, Lopez JS, et al. GCT1021-01, a first-in-human, open-label, dose-escalation trial with expansion cohorts to evaluate safety of Axl-specific antibody-drug conjugate (HuMax-Axl-ADC) in patients with solid tumors (NCT02988817). J Clin Oncol. 2017;35:TPS2605.
42. Zhang C, Liu J, Zhong JF, Zhang X. Engineering CAR-T cells. Biomark Res. 2017;5:22.
43. Fesnak AD, June CH, Levine BL. Engineered T cells: the promise and challenges of cancer immunotherapy. Nat Rev Cancer. 2016;16:566-81.
44. Qin L, Zhao R, Li P. Incorporation of functional elements enhances the antitumor capacity of CAR T cells. Exp Hematol Oncol. 2017;6:28.
45. Bryan WW. Kymriah (tisagenlecleucel) approval letter. In: Drug approvals and Databases. U.S. Food and Drug Administration, Center for Drug Evaluation and Research. 2017. https://www.fda.gov/downloads/BiologicsBloodVaccines/CellularGeneTherapyProducts/ApprovedProducts/UCM574106.pdf. Accessed 2 September 2017.
46. Zhang E, Xu H. A new insight in chimeric antigen receptor-engineered T cells for cancer immunotherapy. J Hematol Oncol. 2017;10:1.
47. Yu S, Li A, Liu Q, et al. Chimeric antigen receptor T cells: a novel therapy for solid tumors. J Hematol Oncol. 2017;10:78.
48. Lee DW, Gardner R, Porter DL, et al. Current concepts in the diagnosis and management of cytokine release syndrome. Blood. 2014;124:188-95.
49. Liu B, Song Y, Liu D. Clinical trials of CAR-T cells in China. J Hematol Oncol. 2017;10:166.
50. van Schalkwyk MCI, Papa SE, Jeannon JP, et al. Design of a phase I clinical trial to evaluate intratumoral delivery of ErbB-targeted chimeric antigen receptor T-cells in locally advanced or recurrent head and neck cancer. Hum Gene Ther Clin Dev. 2013;24:134-42.
51. Papa S, Adami A, Metoudi M, et al. Abstract CT118: T4 immunotherapy of head and neck squamous cell carcinoma using pan-ErbB targeted CAR T-cells. Cancer Res. 2017;77:CT118.
52. Stefanski J, Brentjens R, Hollyman D, et al. CD19-targeted normal and CLL patient T cells expanded with beads can eradicate systemic tumors in vivo. Mol Ther. 2006;13:S102.
53. Park JH, Rivere I, Wang X, et al. Abstract CT078: impact of disease burden and transplant on long-term survival after CD19 CAR therapy in adults with relapsed B-cell acute lymphoblastic leukemia. Cancer Res. 2017;77:CT078.
54. Locke FL, Neelapu SS, Bartlett NL, et al. Clinical and biologic covariates of outcomes in ZUMA-1: a pivotal trial of axicabtagene ciloleucel (axi-cel; KTE-C19) in patients with refractory aggressive non-Hodgkin lymphoma (r-NHL). J Clin Oncol. 2017;35:7512.
55. Xia L, Chen Q, Li Q, et al. Abstract CT041: the clinical study on CD19-directed chimeric antigen receptor-modified T cells in patient with Richter syndrome. Cancer Res. 2017;77:CT041.
56. Turtle CJ, Hanafi L-A, Berger C, et al. Rate of durable complete response in ALL, NHL, and CLL after immunotherapy with optimized lymphodepletion and defined composition CD19 CAR-T cells. J Clin Oncol. 2016;34:102.
57. Fan F, Zhao W, Liu J, et al. Durable remissions with BCMA-specific chimeric antigen receptor (CAR)-modified T cells in patients with refractory/relapsed multiple myeloma. J Clin Oncol. 2017;35:LBA3001.
58. Li WP, Guo LJ, Ekaterina M, et al. Immunotherapy of hepatocellular carcinoma with T cells engineered to express glypican-3-specific chimeric antigen receptors. Mol Ther. 2015;23:S164-5.
59. Zhai B, Shi D, Gao H, et al. A phase I study of anti-GPC3 chimeric antigen receptor modified T cells (GPC3 CAR-T) in Chinese patients with refractory or relapsed GPC3+ hepatocellular carcinoma (r/r GPC3+ HCC). J Clin Oncol. 2017;35:3049.
60. Wang Y, Chen M, Wu Z, et al. CD133-redirected chimeric antigen receptor engineered autologous T-cell treatment in patients with advanced and metastatic malignancies. J Clin Oncol. 2017;35:3042.
61. Cohen AD, Garfall AL, Stadtmauer EA, et al. B-cell maturation antigen (BCMA)-specific chimeric antigen receptor T cells (CART-BCMA) for multiple myeloma (MM): initial safety and efficacy from a phase I study. Blood. 2016;128:1147.
62. Berdeja JG, Lin Y, Raje NS, et al. First-in-human multicenter study of bb2121 anti-BCMA CAR T-cell therapy for relapsed/refractory multiple myeloma: updated results. J Clin Oncol. 2017;35:3010.
63. Guo B, Chen M, Han Q, et al. CD138-directed adoptive immunotherapy of chimeric antigen receptor (CAR)-modified T cells for multiple myeloma. J Cellular Immunotherapy. 2016;2:28-35.
64. Ramos CA, Savoldo B, Torrano V, et al. Clinical responses with T lymphocytes targeting malignancy-associated kappa light chains. J Clin Investig. 2016;126:2588-96.
65. Falini B, Pileri S, Pizzolo G, et al. CD30 (Ki-1) molecule: a new cytokine receptor of the tumor necrosis factor receptor superfamily as a tool for diagnosis and immunotherapy. Blood. 1995;85:1-14.
66. Ramos CA, Ballard B, Zhang H, et al. Clinical and immunological responses after CD30-specific chimeric antigen receptor-redirected lymphocytes. J Clin Invest. 2017;127:3462-71.
67. Brown CE, Alizadeh D, Starr R, et al. Regression of Glioblastoma after chimeric antigen receptor T-cell therapy. N Engl J Med. 2016;375:2561-9.
68. Soriani A, Fionda C, Ricci B, et al. Chemotherapy-elicited upregulation of NKG2D and DNAM-1 ligands as a therapeutic target in multiple myeloma. Oncoimmunology. 2013;2:e26663.
69. Klampatsa A, Haas AR, Moon EK, Albelda SM. Chimeric antigen receptor (CAR) T cell therapy for malignant pleural mesothelioma (MPM). Cancers. 2017;9:115.
70. Govers C, Sebestyen Z, Coccoris M, et al. T cell receptor gene therapy: strategies for optimizing transgenic TCR pairing. Trends Mol Med. 2010;16:77-87.
71. Mackall C, Tap WD, Glod J, et al. Open label, non-randomized, multi-cohort pilot study of genetically engineered NY-ESO-1 specific NY-ESO-1c259t in HLA-A2+ patients with synovial sarcoma (NCT01343043). J Clin Oncol. 2017;35:3000.
72. Draper LM, Kwong MLM, Gros A, et al. Targeting of HPV-16(+) epithelial cancer cells by TCR gene engineered T cells directed against E6. Clin Cancer Res. 2015;21:4431-9.
73. Hinrichs CS, Doran SL, Stevanovic S, et al. A phase I/II clinical trial of E6 T-cell receptor gene therapy for human papillomavirus (HPV)-associated epithelial cancers. J Clin Oncol. 2017;35:3009.
74. Hong DS, Butler MO, Sullivan RJ, et al. A phase I single arm, open label clinical trial evaluating safety of MAGE-A10c796T in subjects with advanced or metastatic head and neck, melanoma, or urothelial tumors (NCT02989064). J Clin Oncol. 2017;35:TPS3098.
75. Rosenberg SA, Yang JC, Sherry RM, et al. Durable complete responses in heavily pretreated patients with metastatic melanoma using T-cell transfer immunotherapy. Clin Cancer Res. 2011;17:4550-7.
76. Goff SL, Dudley M, Citrin DE, et al. A randomized, prospective evaluation comparing intensity of lymphodepletion prior to adoptive transfer of tumor infiltrating lymphocytes for patients with metastatic melanoma. J Clin Oncol. 2016;34:3006.
77. Noonan KA, Huff CA, Davis J, et al. Adoptive transfer of activated marrow-infiltrating lymphocytes induces measurable antitumor immunity in the bone marrow in multiple myeloma. Sci Transl Med. 2015;7:288ra278.
78. Kaufman HL, Kohlhapp FJ, Zloza A. Oncolytic viruses: a new class of immunotherapy drugs. Nat Rev Drug Discov. 2015;14:642-62.
79. Rehman H, Silk AW, Kane MP, Kaufman HL. Into the clinic: talimogene laherparepvec (T-VEC), a first-in-class intratumoral oncolytic viral therapy. J Immunother Cancer. 2016;4:53.
80. Andtbacka RHI, Curti B, Hallmeyer S, et al. Phase II CALM extension study: enhanced immune-cell infiltration within the tumour micro-environment of patients with advanced melanoma following intralesional delivery of coxsackievirus A21. Eur J Cancer. 2015;51:S677.
81. Pandha HS, Ralph C, Harrington K, et al. Keynote-200 phase 1b: a novel combination study of intravenously delivered coxsackievirus A21 and pembrolizumab in advanced cancer patients. J Clin Oncol. 2017;35:TPS3108.
82. Silk AW, Kaufman H, Gabrail N, et al. Abstract CT026: phase 1b study of intratumoral coxsackievirus A21 (CVA21) and systemic pembrolizumab in advanced melanoma patients: interim results of the CAPRA clinical trial. Cancer Res. 2017;77:CT026.
83. Curti BD, Richards JM, Hallmeyer S, et al. Activity of a novel immunotherapy combination of intralesional coxsackievirus A21 and systemic ipilimumab in advanced melanoma patients previously treated with anti-PD1 blockade therapy. J Clin Oncol. 2017;35:3014.
84. Bernstein V, Ellard S, Dent SF, et al. Abstract CT131: a randomized (RCT) phase II study of oncolytic reovirus (pelareorep) plus standard weekly paclitaxel (P) as therapy for metastatic breast cancer (mBC). Cancer Res. 2017;77:CT131.
85. Mahalingam D, Fountzilas C, Moseley J, et al. A phase II study of REOLYSIN(R) (pelareorep) in combination with carboplatin and paclitaxel for patients with advanced malignant melanoma. Cancer Chemother Pharmacol. 2017;79:697-703.
86. Alonso MM, García-Moure M, Gonzalez-Huarriz M, et al. Abstract CT027: oncolytic virus DNX-2401 with a short course of temozolomide for glioblastoma at first recurrence: clinical data and prognostic biomarkers. Cancer Res. 2017;77:CT027.
87. van der Burg SH, Arens R, Ossendorp F, et al. Vaccines for established cancer: overcoming the challenges posed by immune evasion. Nat Rev Cancer. 2016;16:219-33.
88. Morgensztern D, Harb W, Schalper K, et al. MA09.06 Viagenpumatucel-L bolsters response to nivolumab therapy in advanced lung adenocarcinoma: preliminary data from the DURGA trial. J Thorac Oncol. 2017;12:S394-5.
89. Zhang K, Peng Z, Huang X, et al. Phase II trial of adjuvant immunotherapy with autologous tumor-derived Gp96 vaccination in patients with gastric cancer. J Cancer. 2017;8:1826-32.
90. Gray JE, Chiappori A, Williams CC, et al. Phase I/II randomized trial of GM.CD40L vaccine plus/minus CCL21 in advanced lung adenocarcinoma: Final results. J Clin Oncol. 2016;34:9037.
91. Guo C, Manjili MH, Subjeck JR, et al. Therapeutic cancer vaccines: past, present, and future. Adv Cancer Res. 2013;119:421-75.
92. Jabulowsky RA, Loquai C, Diken M, et al. Abstract CT032: a first-in-human phase I/II clinical trial assessing novel mRNA-lipoplex nanoparticles for potent cancer immunotherapy in patients with malignant melanoma. Cancer Res. 2016;76:CT032.
93. Schmitz-Winnenthal FH, Podola L, Hohmann N, et al. A phase 1 trial extension to assess immunologic efficacy and safety of prime-boost vaccination with VXM01, an oral T cell vaccine against VEGF-receptor 2, in patients with advanced pancreatic cancer. J Clin Oncol. 2016;34:3091.
94. Shore ND, Heath EI, Nordquist LT, et al. A clinical trial for the safety and immunogenicity of a DNA-based immunotherapy in men with biochemically (PSA) relapsed prostate cancer. J Clin Oncol. 2017;35:e14634.
95. Teixeira L, Medioni J, Doucet L, et al. Results of a first-in-human phase I study of INVAC-1, an optimized plasmid DNA encoding an inactive form of human telomerase reverse transcriptase (hTERT), in patients with advanced solid tumors. J Clin Oncol. 2017;35:3087.
96. Singh R, Paterson Y. Listeria monocytogenes as a vector for tumor-associated antigens for cancer immunotherapy. Expert Rev Vaccines. 2006;5:541-52.
97. Ghamande SA, Platt D, Wheatley D, et al. Phase I study evaluating high-dose treatment with ADXS11-001, a Listeria monocytogenes-listeriolysin O (Lm-LLO) immunotherapy, in women with cervical cancer. J Clin Oncol. 2016;34:e14580.
98. Jonker DJ, Hotte SJ, Abdul Razak AR, et al. Phase I study of oncolytic virus (OV) MG1 maraba/MAGE-A3 (MG1MA3), with and without transgenic MAGE-A3 adenovirus vaccine (AdMA3) in incurable advanced/metastatic MAGE-A3-expressing solid tumours: CCTG IND.214. J Clin Oncol. 2017;35:e14637.
99. Peace KM, Vreeland TJ, Clifton GT, et al. Abstract CT036: early trial results of an autologous tumor lysate, particle-loaded, dendritic cell (TLPLDC) vaccine in ovarian cancer patients. Cancer Res. 2017;77:CT036.
100. Wood LV, Roberson BD, Agarwal PK, et al. Association of autologous AdHER2 dendritic cell vaccination with antitumor activity and number of circulating tumor cells. J Clin Oncol. 2017;35:3089.
101. Pollack S, Lu H, Somaiah N, et al. Association of CMB305 or LV305-induced and baseline anti-NY-ESO-1 immunity with survival in recurrent cancer patients. J Clin Oncol. 2017;35:3090.
102. Heery CR, Palena C, McMahon S, et al. Phase I study of a poxviral TRICOM-based vaccine directed against the transcription factor brachyury. Clin Cancer Res. 2017;23:6833.
103. Sonpavde G, McMannis JD, Bai Y, et al. Phase I trial of antigen-targeted autologous dendritic cell-based vaccine with in vivo activation of inducible CD40 for advanced prostate cancer. Cancer Immunol Immunother. 2017;66:1345-57.
104. Espinoza-Delgado I. Cancer vaccines. Oncologist. 2002;7:20-33.
105. Oka Y, Tsuboi A, Oji Y, et al. WT1 peptide vaccine for the treatment of cancer. Curr Opin Immunol. 2008;20:211-20.
106. Nishida S, Ishikawa T, Kokura S, et al. Randomized phase II study of WT1 peptide vaccine plus gemcitabine for advanced pancreatic ductal adenocarcinoma (PDAC): clinical efficacy and immune response. J Clin Oncol. 2016;34:3085.
107. Ueda Y, Ogura M, Miyakoshi S, et al. Phase 1/2 study of the WT1 peptide cancer vaccine WT4869 in patients with myelodysplastic syndrome. Cancer Sci. 2017;108:2445-53.
108. Zauderer MG, Tsao AS, Dao T, et al. A randomized phase II trial of adjuvant galinpepimut-S, WT-1 analogue peptide vaccine, after multimodality therapy for patients with malignant pleural mesothelioma. Clin Cancer Res. 2017;23:7483-9.
109. Villella JA, Wilson MK, Berinstein NL, et al. Determination of optimal dose and treatment schedule of the immunotherapeutic vaccine, DPX-Survivac, for combination immunotherapy treatment of ovarian, fallopian tube or peritoneal cancer (OC): a phase Ib study. J Clin Oncol. 2016;34:e14577.
110. Peace KM, Mittendorf EA, Perez SA, et al. Subgroup efficacy evaluation of the AE37 HER2 vaccine in breast cancer patients in the adjuvant setting. J Clin Oncol. 2017;35:3088.
111. Matsui H, Hazama S, Tamada K, et al. A phase I study of novel multi-HLA-binding peptides and a new combination of immune adjuvants against solid tumors. J Clin Oncol. 2017;35:3086.
112. Yasuda T, Nishiki K, Yoshida K, et al. Cancer peptide vaccine to suppress postoperative recurrence in esophageal SCC patients with induction of antigen-specific CD8+ T cell. J Clin Oncol. 2017;35:e14635.
113. Yamaue H, Miyazawa M, Katsuda M, et al. Phase II clinical trial using novel peptide vaccine cocktail as a postoperative adjuvant treatment for surgically resected pancreatic cancer patients. J Clin Oncol. 2016;34:e14587.
114. Slingerland M, Speetjens F, Welters M, et al. A phase I study in patients with a human papillomavirus type 16 positive oropharyngeal tumor treated with second generation synthetic long peptide vaccine conjugated to a defined adjuvant. J Clin Oncol. 2016;34:TPS3113.
115. Ammi R, De Waele J, Willemen Y, et al. Poly(I:C) as cancer vaccine adjuvant: knocking on the door of medical breakthroughs. Pharmacol Ther. 2015;146:120-31.
116. Kyi C, Sabado RL, Saenger YM, et al. In situ, therapeutic vaccination against refractory solid cancers with intratumoral poly-ICLC: a phase I study. J Clin Oncol. 2016;34:3086.
117. Marquez Rodas I, Rodriguez-Ruiz ME, Lopez-Tarruella S, et al. First-in-human clinical trial with intratumoral BO-112 in solid malignancies: a novel immunotherapy based in double-stranded RNA (dsRNA). J Clin Oncol. 2017;35:3082.
118. Schumacher TN, Schreiber RD. Neoantigens in cancer immunotherapy. Science. 2015;348:69-74.
119. Sahin U, Derhovanessian E, Miller M, et al. Personalized RNA mutanome vaccines mobilize poly-specific therapeutic immunity against cancer. Nature. 2017;547:222-6.
120. Ott PA, Hu Z, Keskin DB, et al. An immunogenic personal neoantigen vaccine for patients with melanoma. Nature. 2017;547:217-21.
121. Kumar V, Patel S, Tcyganov E, Gabrilovich DI. The nature of myeloid-derived suppressor cells in the tumor microenvironment. Trends in Immunology. 2016;37:208-20.
122. Liguori M, Buracchi C, Pasqualini F, et al. Functional TRAIL receptors in monocytes and tumor-associated macrophages: a possible targeting pathway in the tumor microenvironment. Oncotarget. 2016;7:41662-76.
123. Forero A, Bendell JC, Kumar P, et al. First-in-human study of the antibody DR5 agonist DS-8273a in patients with advanced solid tumors. Investig New Drugs. 2017;35:298-306.
124. Lasek W, Zagozdzon R, Jakobisiak M. Interleukin 12: still a promising candidate for tumor immunotherapy? Cancer Immunol Immunother. 2014;63:419-35.
125. Barrett JA, Cai H, Miao J, et al. IMPS-03 intratumoral regulated expression of IL-12 as a gene therapy approach to treatment of glioma. Neuro-Oncology. 2015;17:v113.
126. Chiocca EA, Yu J, Phuphanich S, et al. Expanded phase I study of intratumoral Ad-RTS-hIL-12 plus oral veledimex: tolerability and survival in recurrent glioblastoma. J Clin Oncol. 2017;35:2044.
127. Tomala J, Kovar M. IL-2/anti-IL-2 mAb immunocomplexes: a renascence of IL-2 in cancer immunotherapy? Oncoimmunology. 2016;5:e1102829.
128. Diab A, Tannir NM, Bernatchez C, et al. A phase 1/2 study of a novel IL-2 cytokine, NKTR-214, and nivolumab in patients with select locally advanced or metastatic solid tumors. J Clin Oncol. 2017;35:e14040.
129. Bernatchez C, Haymaker CL, Hurwitz ME, et al. Effect of a novel IL-2 cytokine immune agonist (NKTR-214) on proliferating CD8+T cells and PD-1 expression on immune cells in the tumor microenvironment in patients with prior checkpoint therapy. J Clin Oncol. 2017;35:2545.
130. Pitt JM, Marabelle A, Eggermont A, et al. Targeting the tumor microenvironment: removing obstruction to anticancer immune responses and immunotherapy. Ann Oncol. 2016;27:1482-92.
131. Moon YW, Hajjar J, Hwu P, Naing A. Targeting the indoleamine 2,3-dioxygenase pathway in cancer. J Immunother Cancer. 2015;3:51.
132. Siu LL, Gelmon K, Chu Q, et al. Abstract CT116: BMS-986205, an optimized indoleamine 2,3-dioxygenase 1 (IDO1) inhibitor, is well tolerated with potent pharmacodynamic (PD) activity, alone and in combination with nivolumab (nivo) in advanced cancers in a phase 1/2a trial. Cancer Res. 2017;77:CT116.
133. 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;34:3075.
134. Bahary N, Garrido-Laguna I, Cinar P, et al. Phase 2 trial of the indoleamine 2,3-dioxygenase pathway (IDO) inhibitor indoximod plus gemcitabine/nab-paclitaxel for the treatment of metastatic pancreas cancer: interim analysis. J Clin Oncol. 2016;34:3020.
135. Jha GG, Gupta S, Tagawa ST, et al. A phase II randomized, double-blind study of sipuleucel-T followed by IDO pathway inhibitor, indoximod, or placebo in the treatment of patients with metastatic castration resistant prostate cancer (mCRPC). J Clin Oncol. 2017;35:3066.
136. Hamid O, Bauer TM, Spira AI, et al. Safety of epacadostat 100 mg bid plus pembrolizumab 200 mg Q3W in advanced solid tumors: phase 2 data from ECHO-202/KEYNOTE-037. J Clin Oncol. 2017;35:3012.
137. Perez RP, Riese MJ, Lewis KD, et al. Epacadostat plus nivolumab in patients with advanced solid tumors: preliminary phase I/II results of ECHO-204. J Clin Oncol. 2017;35:3003.
138. Lu H. TLR agonists for cancer immunotherapy: tipping the balance between the immune stimulatory and inhibitory effects. Front Immunol. 2014;5:83.
139. Gupta S, Grilley-Olson J, Hong D, et al. Abstract CT091: safety and pharmacodynamic activity of MEDI9197, a TLR 7/8 agonist, administered intratumorally in subjects with solid tumors. Cancer Res. 2017;77:CT091.
140. Dredge K, Brennan T, Brown MP, et al. An open-label, multi-center phase I study of the safety and tolerability of the novel immunomodulatory agent PG545 in subjects with advanced solid tumors. J Clin Oncol. 2017;35:3083.
141. de la Torre AN, Contractor S, Castaneda I, et al. A phase I trial using local regional treatment, nonlethal irradiation, intratumoral and systemic polyinosinic-polycytidylic acid polylysine carboxymethylcellulose to treat liver cancer: in search of the abscopal effect. J Hepatocell Carcinoma. 2017;4:111-21.
142. Ananieva E. Targeting amino acid metabolism in cancer growth and anti-tumor immune response. World J Biol Chem. 2015;6:281-9.
143. Papadopoulos KP, Tsai FY-C, Bauer TM, et al. CX-1158-101: a first-in-human phase 1 study of CB-1158, a small molecule inhibitor of arginase, as monotherapy and in combination with an anti-PD-1 checkpoint inhibitor in patients (pts) with solid tumors. J Clin Oncol. 2017;35:3005.
144. Zhou H, Forveille S, Sauvat A, et al. The oncolytic peptide LTX-315 triggers immunogenic cell death. Cell Death Dis. 2016;7:e2134.
145. Spicer JF, Baurain J-F, Awada A, et al. LTX-315, an oncolytic peptide, to convert immunogenically 'cold' tumors to 'hot' in patients with advanced or metastatic tumours: results from an ongoing phase I study. J Clin Oncol. 2017;35:3085.