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Review

Emerging immunotherapy for the treatment of esophageal cancer

, , &
Pages 667-677 | Received 29 Nov 2015, Accepted 04 Mar 2016, Published online: 24 Mar 2016

References

  • Enzinger PC, Mayer RJ. Esophageal cancer. N Engl J Med. 2003;349:2241–2252.
  • Pisani P, Parkin DM, Bray F, et al. Erratum: estimates of the worldwide mortality from 25 cancers in 1990. Int. J. Cancer. 1999;83:18–29, 870–873.
  • Arnold M, Soerjomataram I, Ferlay J, et al. Global incidence of oesophageal cancer by histological subtype in 2012. Gut. 2015;64:381–387.
  • Rubenstein JH, Shaheen NJ. Epidemiology, diagnosis, and management of esophageal adenocarcinoma. Gastroenterology. 2015;149(302–317):e301.
  • Mathieu LN, Kanarek NF, Tsai H-L, et al. Age and sex differences in the incidence of esophageal adenocarcinoma: results from the surveillance, epidemiology, and end results (SEER) registry (1973-2008). Dis Esophagus. 2014;27:757–763.
  • Lawrence MS, Stojanov P, Polak P, et al. Mutational heterogeneity in cancer and the search for new cancer-associated genes. Nature. 2013;499:214–218.
  • Chang S, Kohrt H, Maecker HT. Monitoring the immune competence of cancer patients to predict outcome. Cancer Immunol Immunother. 2014;63:713–719.
  • Meyer C, Cagnon L, Costa-Nunes CM, et al. Frequencies of circulating MDSC correlate with clinical outcome of melanoma patients treated with ipilimumab. Cancer Immunol Immunother. 2014;63:247–257.
  • Reichert JM, Valge-Archer VE. Development trends for monoclonal antibody cancer therapeutics. Nat Rev Drug Discov. 2007;6:349–356.
  • Clynes RA, Towers TL, Presta LG, et al. Inhibitory Fc receptors modulate in vivo cytotoxicity against tumor targets. Nat Med. 2000;6:443–446.
  • Al-Kasspooles M, Moore JH, Orringer MB, et al. Amplification and over-expression of the EGFR and erbB-2 genes in human esophageal adenocarcinomas. Int J Cancer. 1993;54:213–219.
  • Ku GY, Ilson DH. Emerging mAbs for the treatment of esophagogastric cancer. Expert Opin Emerg Drugs. 2015;20:63–74.
  • Van Cutsem E, Bang YJ, Feng-Yi F, et al. HER2 screening data from ToGA: targeting HER2 in gastric and gastroesophageal junction cancer. Gastric Cancer. 2015;18:476–484.
  • Reichelt U, Duesedau P, Tsourlakis M, et al. Frequent homogeneous HER-2 amplification in primary and metastatic adenocarcinoma of the esophagus. Mod Pathol. 2007;20:120–129.
  • Bang Y-J, Van Cutsem E, Feyereislova A, et al. Trastuzumab in combination with chemotherapy versus chemotherapy alone for treatment of HER2-positive advanced gastric or gastro-oesophageal junction cancer (ToGA): a phase 3, open-label, randomised controlled trial. Lancet. 2010;376:687–697.
  • Ohtsu A, Shah MA, Van Cutsem E, et al. Bevacizumab in combination with chemotherapy as first-line therapy in advanced gastric cancer: a randomized, double-blind, placebo-controlled phase III study. J Clin Oncol. 2011;29:3968–3976.
  • Wilke H, Muro K, Van Cutsem E, et al. Ramucirumab plus paclitaxel versus placebo plus paclitaxel in patients with previously treated advanced gastric or gastro-oesophageal junction adenocarcinoma (RAINBOW): a double-blind, randomised phase 3 trial. Lancet Oncol. 2014;15:1224–1235.
  • Fuchs CS, Tomasek J, Yong CJ, et al. Ramucirumab monotherapy for previously treated advanced gastric or gastro-oesophageal junction adenocarcinoma (REGARD): an international, randomised, multicentre, placebo-controlled, phase 3 trial. Lancet. 2014;383:31–39.
  • Waddell T, Chau I, Cunningham D, et al. Epirubicin, oxaliplatin, and capecitabine with or without panitumumab for patients with previously untreated advanced oesophagogastric cancer (REAL3): a randomised, open-label phase 3 trial. Lancet Oncol. 2013;14:481–489.
  • Crosby T, Hurt CN, Falk S, et al. Chemoradiotherapy with or without cetuximab in patients with oesophageal cancer (SCOPE1): a multicentre, phase 2/3 randomised trial. Lancet Oncol. 2013;14:627–637.
  • Kasper S, Schuler M. Targeted therapies in gastroesophageal cancer. Eur J Cancer. 2014;50:1247–1258.
  • Okines A, Cunningham D, Chau I. Targeting the human EGFR family in esophagogastric cancer. Nat Rev Clin Oncol. 2011;8:492–503.
  • Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer. 2012;12:252–264.
  • Hodi FS, O’Day SJ, McDermott DF, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med. 2010;363:711–723.
  • Robert C, Long GV, Brady B, et al. Nivolumab in previously untreated melanoma without BRAF mutation. N Engl J Med. 2015;372:320–330.
  • Motzer RJ, Escudier B, McDermott DF, et al. Nivolumab versus everolimus in advanced renal-cell carcinoma. N Engl J Med. 2015;373:1803–1813.
  • Borghaei H, Paz-Ares L, Horn L, et al. Nivolumab versus docetaxel in advanced nonsquamous non-small-cell lung cancer. N Engl J Med. 2015;373:1627–1639.
  • Brahmer J, Reckamp KL, Baas P, et al. Nivolumab versus docetaxel in advanced squamous-cell non-small-cell lung cancer. N Engl J Med. 2015;373:123–135.
  • Garon EB, Rizvi NA, Hui R, et al. Pembrolizumab for the treatment of non-small-cell lung cancer. N Engl J Med. 2015;372:2018–2028.
  • Krummel MF, Allison JP. CD28 and CTLA-4 have opposing effects on the response of T cells to stimulation. J Exp Med. 1995;182:459–465.
  • Sakaguchi S, Fukuma K, Kuribayashi K, et al. Organ-specific autoimmune diseases induced in mice by elimination of T cell subset. I. Evidence for the active participation of T cells in natural self-tolerance; deficit of a T cell subset as a possible cause of autoimmune disease. J Exp Med. 1985;161:72–87.
  • Hori S, Nomura T, Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Science. 2003;299:1057–1061.
  • Calabrò L, Morra A, Fonsatti E, et al. Tremelimumab for patients with chemotherapy-resistant advanced malignant mesothelioma: an open-label, single-arm, phase 2 trial. Lancet Oncol. 2013;14:1104–1111.
  • Ralph C, Elkord E, Burt DJ, et al. Modulation of lymphocyte regulation for cancer therapy: a phase II trial of tremelimumab in advanced gastric and esophageal adenocarcinoma. Clin Cancer Res. 2010;16:1662–1672.
  • Shinohara T, Taniwaki M, Ishida Y, et al. Structure and chromosomal localization of the human PD-1 gene (PDCD1). Genomics. 1994;23:704–706.
  • Ribas A, Chesney JA, Gordon MS, et al. Safety profile and pharmacokinetic analyses of the anti-CTLA4 antibody tremelimumab administered as a one hour infusion. J Transl Med. 2012;10:236.
  • Cancer Genome Atlas Research N. Comprehensive molecular characterization of gastric adenocarcinoma. Nature. 2014;513:202–209.
  • Ohigashi Y, Sho M, Yamada Y, et al. Clinical significance of programmed death-1 ligand-1 and programmed death-1 ligand-2 expression in human esophageal cancer. Clin Cancer Res. 2005;11:2947–2953.
  • Derks S, Nason KS, Liao X, et al. Epithelial PD-L2 expression marks Barrett’s esophagus and esophageal adenocarcinoma. Cancer Immunol Res. 2015;3:1123–1129.
  • Huang H, Zhang G, Li G, et al. Circulating CD14(+)HLA-DR(-/low) myeloid-derived suppressor cell is an indicator of poor prognosis in patients with ESCC. Tumour Biol. 2015;36:7987–7996.
  • Goel G, Sun W. Advances in the management of gastrointestinal cancers–an upcoming role of immune checkpoint blockade. J Hematol Oncol. 2015;8:86.
  • Triebel F, Jitsukawa S, Baixeras E, et al. LAG-3, a novel lymphocyte activation gene closely related to CD4. J Exp Med. 1990;171:1393–1405.
  • Triebel F. LAG-3: a regulator of T-cell and DC responses and its use in therapeutic vaccination. Trends Immunol. 2003;24:619–622.
  • Hannier S, Tournier M, Bismuth G, et al. CD3/TCR complex-associated lymphocyte activation gene-3 molecules inhibit CD3/TCR signaling. J Immunol. 1998;161:4058–4065.
  • Maçon-Lemaître L, Triebel F. The negative regulatory function of the lymphocyte-activation gene-3 co-receptor (CD223) on human T cells. Immunology. 2005;115:170–178.
  • Workman CJ, Vignali DAA. The CD4-related molecule, LAG-3 (CD223), regulates the expansion of activated T cells. Eur J Immunol. 2003;33:970–979.
  • Rosenberg SA, Restifo NP, Yang JC, et al. Adoptive cell transfer: a clinical path to effective cancer immunotherapy. Nat Rev Cancer. 2008;8:299–308.
  • Rosenberg S. Lymphokine-activated killer cells: a new approach to immunotherapy of cancer. J Natl Cancer Inst. 1985;75:595–603.
  • Rosenberg SA, Spiess P, Lafreniere R. A new approach to the adoptive immunotherapy of cancer with tumor-infiltrating lymphocytes. Science. 1986;233:1318–1321.
  • Yun YS, Hargrove ME, Ting CC. In vivo antitumor activity of anti-CD3-induced activated killer cells. Cancer Res. 1989;49:4770–4774.
  • Rutella S, Iudicone P, Bonanno G, et al. Adoptive immunotherapy with cytokine-induced killer cells generated with a new good manufacturing practice-grade protocol. Cytotherapy. 2012;14:841–850.
  • Rosenberg SA, Lotze MT, Muul LM, et al. Observations on the systemic administration of autologous lymphokine-activated killer cells and recombinant interleukin-2 to patients with metastatic cancer. N Engl J Med. 1985;313:1485–1492.
  • Dudley ME, Wunderlich JR, Yang JC, et al. Adoptive cell transfer therapy following non-myeloablative but lymphodepleting chemotherapy for the treatment of patients with refractory metastatic melanoma. J Clin Oncol. 2005;23:2346–2357.
  • Besser MJ, Shapira-Frommer R, Schachter J. Tumor-infiltrating lymphocytes: clinical experience. Cancer J. 2015;21:465–469.
  • Toh U, Yamana H, Sueyoshi S, et al. Locoregional cellular immunotherapy for patients with advanced esophageal cancer. Clin Cancer Res. 2000;6:4663–4673.
  • Toh U, Sudo T, Kido K, et al. Locoregional adoptive immunotherapy resulted in regression in distant metastases of a recurrent esophageal cancer. Int J Clin Oncol. 2002;7:372–375.
  • Fujiwara S, Wada H, Miyata H, et al. Clinical trial of the intratumoral administration of labeled DC combined with systemic chemotherapy for esophageal cancer. J Immunother. 2012;35:513–521.
  • Kono K, Takahashi A, Ichihara F, et al. Prognostic significance of adoptive immunotherapy with tumor-associated lymphocytes in patients with advanced gastric cancer: a randomized trial. Clin Cancer Res. 2002;8:1767–1771.
  • Gebremeskel S, Johnston B. Concepts and mechanisms underlying chemotherapy induced immunogenic cell death: impact on clinical studies and considerations for combined therapies. Oncotarget. 2015;6:41600–41619.
  • Bujas T, Marusic Z, Peric Balja M, et al. MAGE-A3/4 and NY-ESO-1 antigens expression in metastatic esophageal squamous cell carcinoma. Eur J Histochem. 2011;55:e7.
  • Forghanifard MM, Gholamin M, Farshchian M, et al. Cancer-testis gene expression profiling in esophageal squamous cell carcinoma: identification of specific tumor marker and potential targets for immunotherapy. Cancer Biol Ther. 2011;12:191–197.
  • Kageyama S, Wada H, Muro K, et al. Dose-dependent effects of NY-ESO-1 protein vaccine complexed with cholesteryl pullulan (CHP-NY-ESO-1) on immune responses and survival benefits of esophageal cancer patients. J Transl Med. 2013;11:246.
  • Kline GS. Update on phase III clinical trial of investigational MAGE-A3 antigen-specific cancer immunotherapeutic in non-small cell lung cancer. 2014;[cited 2016 Feb 24]. Available at https://us.gsk.com/en-us/media/press-releases/2014/update-on-phase-iii-clinical-trial-of-investigational-mage-a3-antigen-specific-cancer-immunotherapeutic-in-non-small-cell-lung-cancer/
  • Finn OJ. Cancer immunology. N Engl J Med. 2008;358:2704–2715.
  • Rosenberg SA, Yang JC, Restifo NP. Cancer immunotherapy: moving beyond current vaccines. Nat Med. 2004;10:909–915.
  • Rosenberg SA, Sherry RM, Morton KE, et al. Tumor progression can occur despite the induction of very high levels of self/tumor antigen-specific CD8+ T cells in patients with melanoma. J Immunol. 2005;175:6169–6176.
  • Kono K, Mizukami Y, Daigo Y, et al. Vaccination with multiple peptides derived from novel cancer-testis antigens can induce specific T-cell responses and clinical responses in advanced esophageal cancer. Cancer Sci. 2009;100:1502–1509.
  • Kono K, Iinuma H, Akutsu Y, et al. Multicenter, phase II clinical trial of cancer vaccination for advanced esophageal cancer with three peptides derived from novel cancer-testis antigens. J Transl Med. 2012;10:141.
  • Iwahashi M, Katsuda M, Nakamori M, et al. Vaccination with peptides derived from cancer-testis antigens in combination with CpG-7909 elicits strong specific CD8+ T cell response in patients with metastatic esophageal squamous cell carcinoma. Cancer Sci. 2010;101:2510–2517.
  • Saito T, Wada H, Yamasaki M, et al. High expression of MAGE-A4 and MHC class I antigens in tumor cells and induction of MAGE-A4 immune responses are prognostic markers of CHP-MAGE-A4 cancer vaccine. Vaccine. 2014;32:5901–5907.
  • Uenaka A, Wada H, Isobe M, et al. T cell immunomonitoring and tumor responses in patients immunized with a complex of cholesterol-bearing hydrophobized pullulan (CHP) and NY-ESO-1 protein. Cancer Immun. 2007;7:9.
  • Wada H, Sato E, Uenaka A, et al. Analysis of peripheral and local anti-tumor immune response in esophageal cancer patients after NY-ESO-1 protein vaccination. Int J Cancer. 2008;123:2362–2369.
  • Kakimi K, Isobe M, Uenaka A, et al. A phase I study of vaccination with NY-ESO-1f peptide mixed with Picibanil OK-432 and Montanide ISA-51 in patients with cancers expressing the NY-ESO-1 antigen. Int J Cancer. 2011;129:2836–2846.
  • Wada H, Isobe M, Kakimi K, et al. Vaccination with NY-ESO-1 overlapping peptides mixed with Picibanil OK-432 and montanide ISA-51 in patients with cancers expressing the NY-ESO-1 antigen. J Immunother. 2014;37:84–92.
  • Hoos A. Evolution of end points for cancer immunotherapy trials. Ann Oncol. 2012;23(Suppl 8):viii47–52.
  • Lu J, Lee-Gabel L, Nadeau MC, et al. Clinical evaluation of compounds targeting PD-1/PD-L1 pathway for cancer immunotherapy. J Oncol Pharm Pract. 2015;21:451–467.
  • Garnett CT, Palena C, Chakraborty M, et al. Sublethal irradiation of human tumor cells modulates phenotype resulting in enhanced killing by cytotoxic T lymphocytes. Cancer Res. 2004;64:7985–7994.
  • Corso CD, Ali AN, Diaz R. Radiation-induced tumor neoantigens: imaging and therapeutic implications. Am J Cancer Res. 2011;1:390–412.
  • Teitz-Tennenbaum S, Li Q, Okuyama R, et al. Mechanisms involved in radiation enhancement of intratumoral dendritic cell therapy. J Immunother. 2008;31:345–358.
  • Kingsley DP. An interesting case of possible abscopal effect in malignant melanoma. Br J Radiol. 1975;48:863–866.
  • Rees GJ. Abscopal regression in lymphoma: a mechanism in common with total body irradiation? Clin Radiol. 1981;32:475–480.
  • Rees GJ, Ross CM. Abscopal regression following radiotherapy for adenocarcinoma. Br J Radiol. 1983;56:63–66.
  • Ohba K, Omagari K, Nakamura T, et al. Abscopal regression of hepatocellular carcinoma after radiotherapy for bone metastasis. Gut. 1998;43:575–577.
  • Cotter SE, Dunn GP, Collins KM, et al. Abscopal effect in a patient with metastatic Merkel cell carcinoma following radiation therapy: potential role of induced antitumor immunity. Arch Dermatol. 2011;147:870–872.
  • Akutsu Y, Matsubara H, Urashima T, et al. Combination of direct intratumoral administration of dendritic cells and irradiation induces strong systemic antitumor effect mediated by GRP94/gp96 against squamous cell carcinoma in mice. Int J Oncol. 2007;31:509–515.
  • Shiraishi K, Ishiwata Y, Nakagawa K, et al. Enhancement of antitumor radiation efficacy and consistent induction of the abscopal effect in mice by ECI301, an active variant of macrophage inflammatory protein-1alpha. Clin Cancer Res. 2008;14:1159–1166.
  • Brody JD, Ai WZ, Czerwinski DK, et al. In situ vaccination with a TLR9 agonist induces systemic lymphoma regression: a phase I/II study. J Clin Oncol. 2010;28:4324–4332.
  • Dewan MZ, Galloway AE, Kawashima N, et al. Fractionated but not single-dose radiotherapy induces an immune-mediated abscopal effect when combined with anti-CTLA-4 antibody. Clin Cancer Res. 2009;15:5379–5388.
  • Postow MA, Callahan MK, Barker CA, et al. Immunologic correlates of the abscopal effect in a patient with melanoma. N Engl J Med. 2012;366:925–931.
  • Nesslinger NJ, Sahota RA, Stone B, et al. Standard treatments induce antigen-specific immune responses in prostate cancer. Clin Cancer Res. 2007;13:1493–1502.
  • Schaue D, Comin-Anduix B, Ribas A, et al. T-cell responses to survivin in cancer patients undergoing radiation therapy. Clin Cancer Res. 2008;14:4883–4890.
  • Ma JL, Jin L, Li YD, et al. The intensity of radiotherapy-elicited immune response is associated with esophageal cancer clearance. J Immunol Res. 2014;2014:794249.
  • Tesniere A, Schlemmer F, Boige V, et al. Immunogenic death of colon cancer cells treated with oxaliplatin. Oncogene. 2010;29:482–491.
  • Kroemer G, Zitvogel L. Abscopal but desirable: the contribution of immune responses to the efficacy of radiotherapy. Oncoimmunology. 2012;1:407–408.

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