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Review

Combining therapeutic vaccines with chemo- and immunotherapies in the treatment of cancer

, ORCID Icon, & ORCID Icon
Pages 89-99 | Received 09 Jun 2020, Accepted 14 Aug 2020, Published online: 31 Aug 2020

References

  • Mellman I, Coukos G, Dranoff G. Cancer immunotherapy comes of age. Nature. 2011;480:480–489.
  • Farkona S, Diamandis EP, Blasutig IM. Cancer immunotherapy: the beginning of the end of cancer? BMC Med. 2016;14:73.
  • Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer. 2012;12:252–264.
  • Waldman AD, Fritz JM, Lenardo MJ. A guide to cancer immunotherapy: from T cell basic science to clinical pratice. Nat Rev Immunol. 2020;20:1-18.
  • Wu R, Forget M-A, Chacon J, et al. Adoptive T-cell therapy using autologous tumor-infiltrating lymphocytes for metastatic melanoma: current status and future outlook. Cancer J. 2012;18:160.
  • Lee PP, Yee C, Savage PA, et al. Characterization of circulating T cells specific for tumor-associated antigens in melanoma patients. Nat Med. 1999;5:677–685.
  • Yee C, Greenberg P. Modulating T-cell immunity to tumours: new strategies for monitoring T-cell responses. Nat Rev Cancer. 2002;2:409–419.
  • Zhang L, Conejo-Garcia JR, Katsaros D, et al. Intratumoral T cells, recurrence, and survival in epithelial ovarian cancer. N Engl J Med. 2003;348:203–213.
  • John SY, Liu G, Ying H, et al. Vaccination with tumor lysate-pulsed dendritic cells elicits antigen-specific, cytotoxic T-cells in patients with malignant glioma. Cancer Res. 2004;64:4973–4979.
  • Tosolini M, Kirilovsky A, Mlecnik B, et al. Clinical impact of different classes of infiltrating T cytotoxic and helper cells (Th1, th2, treg, th17) in patients with colorectal cancer. Cancer Res. 2011;71:1263–1271.
  • Franco EL, Harper DM. Vaccination against human papillomavirus infection: a new paradigm in cervical cancer control. Vaccine. 2005;23:2388–2394.
  • Martin D, Gutkind J. Human tumor-associated viruses and new insights into the molecular mechanisms of cancer. Oncogene. 2008;27:S31–S42.
  • Saraiya M, Unger ER, Thompson TD, et al. US assessment of HPV types in cancers: implications for current and 9-valent HPV vaccines. JNCI. 2015;107(6):djv086.
  • Melief CJ, van Hall T, Arens R, et al. Therapeutic cancer vaccines. J Clin Invest. 2015;125:3401–3412.
  • Yadav M, Jhunjhunwala S, Phung QT, et al. Predicting immunogenic tumour mutations by combining mass spectrometry and exome sequencing. Nature. 2014;515:572–576.
  • Gilboa E. How tumors escape immune destruction and what we can do about it. Cancer Immunol Immunother. 1999;48:382–385.
  • Havel JJ, Chowell D, Chan TA. The evolving landscape of biomarkers for checkpoint inhibitor immunotherapy. Nat Rev Cancer. 2019;19:133–150.
  • Moyer TJ, Zmolek AC, Irvine DJ. Beyond antigens and adjuvants: formulating future vaccines. J Clin Invest. 2016;126:799–808.
  • Overwijk WW. Cancer vaccines in the era of checkpoint blockade: the magic is in the adjuvant. Curr Opin Immunol. 2017;47:103–109.
  • Majzner RG, Mackall CL. Clinical lessons learned from the first leg of the CAR T cell journey. Nat Med. 2019;25:1341–1355.
  • Pusuluri A, Wu D, Mitragotri S. Immunological consequences of chemotherapy: single drugs, combination therapies and nanoparticle-based treatments. J Control Release. 2019;305:130–154.
  • Reck M, Rodríguez-Abreu D, Robinson AG, et al. Pembrolizumab versus chemotherapy for PD-L1–positive non–small-cell lung cancer. N Engl J Med. 2016;375:1823–1833.
  • Shen X, Zhang L, Li J, et al. Findings in the regulation of programmed death ligand 1 expression. Front Immunol. 2019;10:1337.
  • Addeo A, Banna GL, Metro G, et al. Chemotherapy in combination with immune checkpoint inhibitors for the first-line treatment of patients with advanced non-small cell lung cancer: a systematic review and literature-based meta-analysis. Front Oncol. 2019;9. DOI:10.3389/fonc.2019.00264
  • Nuhn P, De Bono JS, Fizazi K, et al. Update on systemic prostate cancer therapies: management of metastatic castration-resistant prostate cancer in the era of precision oncology. Eur Urol. 2019;75:88–99.
  • Kwon ED, Drake CG, Scher HI, et al. Ipilimumab versus placebo after radiotherapy in patients with metastatic castration-resistant prostate cancer that had progressed after docetaxel chemotherapy (CA184-043): a multicentre, randomised, double-blind, phase 3 trial. The Lancet Oncology. 2014;15(7):700–712.
  • Ozpiskin OM, Zhang L, Li JJ. Immune targets in the tumor microenvironment treated by radiotherapy. Theranostics. 2019;9:1215.
  • Weiss T, Weller M, Roth P. Immunological effects of chemotherapy and radiotherapy against brain tumors. Expert Rev Anticancer Ther. 2016;16:1087–1094.
  • Hader M, Frey B, Fietkau R, et al. Immune biological rationales for the design of combined radio-and immunotherapies. Cancer Immunol Immunother. 2020;69:293–306.
  • Jung S, Unutmaz D, Wong P, et al. In vivo depletion of CD11c+ dendritic cells abrogates priming of CD8+ T cells by exogenous cell-associated antigens. Immunity. 2002;17:211–220.
  • Mempel TR, Henrickson SE, von Andrian UH. T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases. Nature. 2004;427:154–159.
  • Torralba D, Baixauli F, Villarroya-Beltri C, et al. Priming of dendritic cells by DNA-containing extracellular vesicles from activated T cells through antigen-driven contacts. Nat Commun. 2018;9:2658.
  • Palucka K, Banchereau J. Dendritic-cell-based therapeutic cancer vaccines. Immunity. 2013;39:38–48.
  • Cheever MA, Higano CS. PROVENGE (Sipuleucel-T) in prostate cancer: the first FDA-approved therapeutic cancer vaccine. Clin Cancer Res. 2011;17:3520.
  • Arlen Philip M, Skarupa L, Pazdur M, et al. Clinical safety of a viral vector based prostate cancer vaccine strategy. J Urol. 2007;178:1515–1520.
  • Kantoff PW, Schuetz TJ, Blumenstein BA, et al. Overall survival analysis of a phase II randomized controlled trial of a poxviral-based PSA-targeted immunotherapy in metastatic castration-resistant prostate cancer. J Clin Oncol. 2010;28:1099–1105.
  • Guo Y, Walsh AM, Canavan M, et al. Immune checkpoint inhibitor PD-1 pathway is down-regulated in synovium at various stages of rheumatoid arthritis disease progression. PloS One. 2018;13:e0192704–e0192704.
  • Weinmann SC, Pisetsky DS. Mechanisms of immune-related adverse events during the treatment of cancer with immune checkpoint inhibitors. Rheumatology (Oxford). 2019;58:vii59–vii67.
  • Avigan D, Rosenblatt J. Vaccine therapy in hematologic malignancies. Blood. 2018;131:2640–2650.
  • van de Loosdrecht AA, van Wetering S, Santegoets SJ, et al. A novel allogeneic off-the-shelf dendritic cell vaccine for post-remission treatment of elderly patients with acute myeloid leukemia. Cancer Immunol Immunother. 2018;67:1505–1518.
  • Simons JW, Jaffee EM, Weber CE, et al. Bioactivity of autologous irradiated renal cell carcinoma vaccines generated by ex vivo granulocyte-macrophage colony-stimulating factor gene transfer. Cancer Res. 1997;57:1537–1546.
  • Shirota H, Klinman DM. CpG-conjugated apoptotic tumor cells elicit potent tumor-specific immunity. Cancer Immunol Immunother. 2011;60:659–669.
  • Curry WT Jr., Gorrepati R, Piesche M, et al. Vaccination with irradiated autologous tumor cells mixed with irradiated GM-K562 cells stimulates antitumor immunity and T lymphocyte activation in patients with recurrent malignant glioma. Clin Cancer Res off J Am Assoc Cancer Res. 2016;22:2885–2896.
  • Ali OA, Huebsch N, Cao L, et al. infection-mimicking materials to program dendritic cells in situ. Nat Mater. 2009;8:151–158.
  • Ali OA, Emerich D, Dranoff G, et al. In situ regulation of DC subsets and T cells mediates tumor regression in mice. Sci Transl Med. 2009;1:8ra19.
  • Jaffee EM, Hruban RH, Biedrzycki B, et al. Novel allogeneic granulocyte-macrophage colony-stimulating factor–secreting tumor vaccine for pancreatic cancer: a phase i trial of safety and immune activation. J Clin Oncol. 2001;19:145–156.
  • Lutz E, Yeo CJ, Lillemoe KD, et al. A lethally irradiated allogeneic granulocyte-macrophage colony stimulating factor-secreting tumor vaccine for pancreatic adenocarcinoma. A phase II trial of safety, efficacy, and immune activation. Ann Surg. 2011;253:328–335.
  • Santegoets SJAM, Schreurs MWJ, Masterson AJ, et al. In vitro priming of tumor-specific cytotoxic T lymphocytes using allogeneic dendritic cells derived from the human MUTZ-3 cell line. Cancer Immunol Immunother. 2006;55:1480–1490.
  • Li B, VanRoey M, Wang C, et al. 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.
  • Wada S, Jackson CM, Yoshimura K, et al. Sequencing CTLA-4 blockade with cell-based immunotherapy for prostate cancer. J Transl Med. 2013;11:89.
  • Duraiswamy J, Kaluza KM, Freeman GJ, et al. Dual blockade of PD-1 and CTLA-4 combined with tumor vaccine effectively restores T-cell rejection function in tumors. Cancer Res. 2013;73:3591–3603.
  • Santos PM, Adamik J, Howes TR, et al. impact of checkpoint blockade on cancer vaccine–activated CD8+ T cell responses. J Exp Med. 2020;217. DOI:10.1084/jem.20191369
  • Versteven M, Van den Bergh JM, Marcq E, et al. Dendritic cells and programmed death-1 blockade: a joint venture to combat cancer. Front Immunol. 2018;9:394.
  • Mouraviev V, Mariados N, Albala D, et al. The rationale for optimal combination therapy with sipuleucel-T for patients with castration-resistant prostate cancer. Rev Urol. 2014;16:122–130.
  • Hollingsworth RE, Jansen K. Turning the corner on therapeutic cancer vaccines. NPJ Vaccines. 2019;4:1–10.
  • Kerk SA, Finkel KA, Pearson AT, et al. 5T4-targeted therapy ablates cancer stem cells and prevents recurrence of head and neck squamous cell carcinoma. Clin Cancer Res. 2017;23:2516–2527.
  • Wang L, Pan L, Yao M, et al. Expression of oncofetal antigen glypican-3 associates significantly with poor prognosis in HBV-related hepatocellular carcinoma. Oncotarget. 2016;7:42150.
  • Kalyan A, Kircher S, Shah H, et al. Updates on immunotherapy for colorectal cancer. J Gastrointest Oncol. 2018;9:160.
  • Warnecke-Eberz U, Metzger R, Hölscher AH, et al. Diagnostic marker signature for esophageal cancer from transcriptome analysis. Tumor Biol. 2016;37:6349–6358.
  • Cua S, Tan HL, Fong WJ, et al. Targeting of embryonic annexin A2 expressed on ovarian and breast cancer by the novel monoclonal antibody 2448. Oncotarget. 2018;9:13206.
  • Hirayama M, Tomita Y, Yuno A, et al. An oncofetal antigen, IMP-3-derived long peptides induce immune responses of both helper T cells and CTLs. Oncoimmunology. 2016;5:e1123368–e1123368.
  • Tamai T, Mizukoshi E, Kumagai M, et al. A novel α-fetoprotein-derived helper T-lymphocyte epitope with strong immunogenicity in patients with hepatocellular carcinoma. Sci Rep. 2020;10:4021.
  • Hensel JA, Khattar V, Ashton R, et al. Recombinant AAV-CEA tumor vaccine in combination with an immune adjuvant breaks tolerance and provides protective immunity. Mol Ther Oncolytics. 2018;12:41–48.
  • Cheever MA, Allison JP, Ferris AS, et al. The prioritization of cancer antigens: a national cancer institute pilot project for the acceleration of translational research. Clin Cancer Res off J Am Assoc Cancer Res. 2009;15:5323–5337.
  • Chapuis AG, Egan DN, Bar M, et al. T cell receptor gene therapy targeting WT1 prevents acute myeloid leukemia relapse post-transplant. Nat Med. 2019;25:1064–1072.
  • Maslak PG, Dao T, Bernal Y, et al. Phase 2 trial of a multivalent WT1 peptide vaccine (galinpepimut-S) in acute myeloid leukemia. Blood Adv. 2018;2:224–234.
  • Batchu RB, Gruzdyn O, Potti RB, et al. MAGE-A3 with cell-penetrating domain as an efficient therapeutic cancer vaccine. JAMA Surg. 2014;149:451–457.
  • Gérard C, Baudson N, Ory T, et al. Tumor mouse model confirms MAGE-A3 cancer immunotherapeutic as an efficient inducer of long-lasting anti-tumoral responses. PloS One. 2014;9:e94883–e94883.
  • Junwei W, Xiumin Z, Jing Y, et al. In vivo enhancement of the MAGE-specific cellular immune response by a recombinant MAGE1-MAGE3-TBHSP70 tumor vaccine. Cancer Cell Int. 2016;16:45.
  • Sypniewska RK, Hoflack L, Tarango M, et al. Prevention of metastases with a Mage-b DNA vaccine in a mouse breast tumor model: potential for breast cancer therapy. Breast Cancer Res Treat. 2005;91:19–28.
  • Castro F, Leal B, Denny A, et al. Vaccination with MAGE-b DNA induces CD8 T-cell responses at young but not old age in mice with metastatic breast cancer. Br J Cancer. 2009;101:1329–1337.
  • Duperret EK, Liu S, Paik M, et al. A designer cross-reactive DNA immunotherapeutic vaccine that targets multiple MAGE-A family members simultaneously for cancer therapy. Clin Cancer Res. 2018;24:6015–6027.
  • Parvanova I, Rettig L, Knuth A, et al. The form of NY-ESO-1 antigen has an impact on the clinical efficacy of anti-tumor vaccination. Vaccine. 2011;29:3832–3836.
  • Li M, Shi H, Mu Y, et al. Effective inhibition of melanoma tumorigenesis and growth via a new complex vaccine based on NY-ESO-1-alum-polysaccharide-HH2. Mol Cancer. 2014;13:179.
  • Xue W, Metheringham RL, Brentville VA, et al. SCIB2, an antibody DNA vaccine encoding NY-ESO-1 epitopes, induces potent antitumor immunity which is further enhanced by checkpoint blockade. OncoImmunology. 2016;5:e1169353.
  • Albershardt TC, Campbell DJ, Parsons AJ, et al. LV305, a dendritic cell-targeting integration-deficient ZVexTM-based lentiviral vector encoding NY-ESO-1, induces potent anti-tumor immune response. Mol Ther Oncolytics. 2016;3:16010.
  • Somaiah N, Block MS, Kim JW, et al. First-in-class, first-in-human study evaluating LV305, a dendritic-cell tropic lentiviral vector, in sarcoma and other solid tumors expressing NY-ESO-1. Clin Cancer Res. 2019;25(19):5808–5817. clincanres.1025.2019.
  • Kawakami Y, Eliyahu S, Delgado CH, et al. Cloning of the gene coding for a shared human melanoma antigen recognized by autologous T cells infiltrating into tumor. Proc Natl Acad Sci U S A. 1994;91:3515–3519.
  • Kawakami Y, Eliyahu S, Sakaguchi K, et al. Identification of the immunodominant peptides of the MART-1 human melanoma antigen recognized by the majority of HLA-A2-restricted tumor infiltrating lymphocytes. J Exp Med. 1994;180:347–352.
  • Cormier JN, Salgaller ML, Prevette T, et al. Enhancement of cellular immunity in melanoma patients immunized with a peptide from MART-1/Melan A. Cancer J Sci Am. 1997;3:37–44.
  • Yan J, Tingey C, Lyde R, et al. Novel and enhanced anti-melanoma DNA vaccine targeting the tyrosinase protein inhibits myeloid-derived suppressor cells and tumor growth in a syngeneic prophylactic and therapeutic murine model. Cancer Gene Ther. 2014;21:507–517.
  • Tumeh PC, Harview CL, Yearley JH, et al. PD-1 blockade induces responses by inhibiting adaptive immune resistance. Nature. 2014;515:568–571.
  • Conniot J, Scomparin A, Peres C, et al. Immunization with mannosylated nanovaccines and inhibition of the immune-suppressing microenvironment sensitizes melanoma to immune checkpoint modulators. Nat Nanotechnol. 2019;14:891–901.
  • Kreiter S, Selmi A, Diken M, et al. Intranodal vaccination with naked antigen-encoding RNA elicits potent prophylactic and therapeutic antitumoral immunity. Cancer Res. 2010;70:9031.
  • Sahin U, Derhovanessian E, Miller M, et al. Personalized RNA mutanome vaccines mobilize poly-specific therapeutic immunity against cancer. Nature. 2017;547:222–226.
  • Liang Y, Lü W, Zhang X, et al. Tumor-infiltrating CD8+ and FOXP3+ lymphocytes before and after neoadjuvant chemotherapy in cervical cancer. Diagn Pathol. 2018;13:93.
  • Gao Q, Wang S, Chen X, et al. Cancer-cell-secreted CXCL11 promoted CD8+ T cells infiltration through docetaxel-induced-release of HMGB1 in NSCLC. J Immunother Cancer. 2019;7:42.
  • Opzoomer JW, Sosnowska D, Anstee JE, et al. Cytotoxic chemotherapy as an immune stimulus: a molecular perspective on turning up the immunological heat on cancer. Front Immunol. 2019;10:1654.
  • Bauer C, Sterzik A, Bauernfeind F, et al. Concomitant gemcitabine therapy negatively affects DC vaccine-induced CD8+ T-cell and B-cell responses but improves clinical efficacy in a murine pancreatic carcinoma model. Cancer Immunol Immunother. 2014;63:321–333.
  • Petrizzo A, Mauriello A, Luciano A, et al. Inhibition of tumor growth by cancer vaccine combined with metronomic chemotherapy and anti-PD-1 in a pre-clinical setting. Oncotarget. 2017;9(3):3576–3589.
  • Shah NJ, Najibi AJ, Shih T-Y, et al. A biomaterial-based vaccine eliciting durable tumour-specific responses against acute myeloid leukaemia. Nat Biomed Eng. 2020;4:40–51.
  • Zuber J, Radtke I, Pardee T, et al. Mouse models of human AML accurately predict chemotherapy response. Genes Dev. 2009;23:877–889.
  • Moynihan KD, Opel CF, Szeto GL, et al. Eradication of large established tumors in mice by combination immunotherapy that engages innate and adaptive immune responses. Nat Med. 2016;22:1402.
  • Liu H, Moynihan KD, Zheng Y, et al. Structure-based programming of lymph-node targeting in molecular vaccines. Nature. 2014;507:519–522.
  • Ott PA, Hu Z, Keskin DB, et al. An immunogenic personal neoantigen vaccine for patients with melanoma. Nature. 2017;547:217–221.
  • Grenier JM, Yeung ST, Khanna KM. Combination immunotherapy: taking cancer vaccines to the next level. Front Immunol. 2018;9:610.
  • Romero P, Banchereau J, Bhardwaj N, et al. The human vaccines project: a roadmap for cancer vaccine development. Sci Transl Med. 2016;8:334ps339.
  • Chen G, Emens LA. Chemoimmunotherapy: reengineering tumor immunity. Cancer Immunol Immunother. 2013;62:203–216.
  • Wong KK, Li WA, Mooney DJ, et al. Advances in therapeutic cancer vaccines. Adv Immunol. 2016;130:191–249. Edited by: Elsevier.
  • Schreiber TH, Raez L, Rosenblatt JD, et al. Tumor immunogenicity and responsiveness to cancer vaccine therapy: the state of the art. Semin Immunol. 2010;22:105–112.
  • Bookstaver ML, Tsai SJ, Bromberg JS, et al. Improving vaccine and immunotherapy design using biomaterials. Trends Immunol. 2018;39:135–150.
  • Galon J, Bruni D. Approaches to treat immune hot, altered and cold tumours with combination immunotherapies. Nat Rev Drug Discov. 2019;18:197–218.

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