4,527
Views
6
CrossRef citations to date
0
Altmetric
REVIEW

PD-1 blockade synergizes with oxaliplatin-based, but not cisplatin-based, chemotherapy of gastric cancer

, , , , ORCID Icon, & show all
Article: 2093518 | Received 16 Jun 2022, Accepted 20 Jun 2022, Published online: 24 Jun 2022

References

  • Rottenberg S, Disler C, Perego P. The rediscovery of platinum-based cancer therapy. Nat Rev Cancer. 2021;21:37–9. doi:10.1038/s41568-020-00308-y.
  • Dasari S, Tchounwou PB. Cisplatin in cancer therapy: molecular mechanisms of action. Eur J Pharmacol. 2014;740:364–378. doi:10.1016/j.ejphar.2014.07.025.
  • Cocetta V, Ragazzi E, Montopoli M. Links between cancer metabolism and cisplatin resistance. Int Rev Cell Mol Biol. 2020;354:107–164. doi:10.1016/bs.ircmb.2020.01.005.
  • Kelland L. The resurgence of platinum-based cancer chemotherapy. Nat Rev Cancer. 2007;7(8):573–584. doi:10.1038/nrc2167.
  • Yamada Y, Higuchi K, Nishikawa K, Gotoh M, Fuse N, Sugimoto N, Nishina T, Amagai K, Chin K, Niwa Y, et al. Phase III study comparing oxaliplatin plus S-1 with cisplatin plus S-1 in chemotherapy-naive patients with advanced gastric cancer. Ann Oncol. 2015;26(1):141–148. doi:10.1093/annonc/mdu472.
  • Cunningham D, Starling N, Rao S, Iveson T, Nicolson M, Coxon F, Middleton G, Daniel F, Oates J, Norman AR, et al. Capecitabine and oxaliplatin for advanced esophagogastric cancer. N Engl J Med. 2008;358(1):36–46. doi:10.1056/NEJMoa073149.
  • Chinen T, Sasabuchi Y, Matsui H, Yamaguchi H, Yasunaga H. Oxaliplatin- versus cisplatin-based regimens for elderly individuals with advanced gastric cancer: a retrospective cohort study. BMC Cancer. 2022;22(1):460. doi:10.1186/s12885-022-09581-6.
  • Huang J, Zhao Y, Xu Y, Zhu Y, Huang J, Liu Y, Zhao L, Li Z, Liu H, Wang Q-L, et al. Comparative effectiveness and safety between oxaliplatin-based and cisplatin-based therapy in advanced gastric cancer: a meta-analysis of randomized controlled trials. Oncotarget. 2016;7(23):34824–34831. doi:10.18632/oncotarget.9189.
  • Zhang F, Zhang Y, Jia Z, Wu H, Gu K. Oxaliplatin-based regimen is superior to cisplatin-based regimen in tumour remission as first-line chemotherapy for advanced gastric cancer: a meta-analysis. J Cancer. 2019;10(8):1923–1929. doi:10.7150/jca.28896.
  • Montagnani F, Turrisi G, Marinozzi C, Aliberti C, Fiorentini G. Effectiveness and safety of oxaliplatin compared to cisplatin for advanced, unresectable gastric cancer: a systematic review and meta-analysis. Gastric Cancer. 2011;14:50–55. doi:10.1007/s10120-011-0007-7.
  • Tesniere A, Schlemmer F, Boige V, Kepp O, Martins I, Ghiringhelli F, Aymeric L, Michaud M, Apetoh L, Barault L, et al. Immunogenic death of colon cancer cells treated with oxaliplatin. Oncogene. 2010;29:482–491. doi:10.1038/onc.2009.356.
  • Vanmeerbeek I, Sprooten J, De Ruysscher D, Tejpar S, Vandenberghe P, Fucikova J, Spisek R, Zitvogel L, Kroemer G, Galluzzi L, et al. Trial watch: chemotherapy-induced immunogenic cell death in immuno-oncology. Oncoimmunology. 2020;9:1703449. doi:10.1080/2162402X.2019.1703449.
  • Vacchelli E, Galluzzi L, Fridman WH, Galon J, Sautès-Fridman C, Tartour E, Kroemer G. Trial watch: chemotherapy with immunogenic cell death inducers. Oncoimmunology. 2012;1:179–188. doi:10.4161/onci.1.2.19026.
  • Galluzzi L, Vitale I, Warren S, Adjemian S, Agostinis P, Martinez AB, Chan TA, Coukos G, Demaria S, Deutsch E, et al. Consensus guidelines for the definition, detection and interpretation of immunogenic cell death. J Immunother Cancer. 2020;8:e000337. doi:10.1136/jitc-2019-000337.
  • Kepp O, Bezu, L., Yamazaki, T., Di Virgilio, F., Smyth, M. J., Kroemer, G., & Galluzzi, L. ATP and cancer immunosurveillance. EMBO J. 2021;40:e108130. doi:10.15252/embj.2021108130.
  • Kroemer G, Galassi C, Zitvogel L, Galluzzi L. Immunogenic cell stress and death. Nat Immunol. 2022;23(4):487–500. doi:10.1038/s41590-022-01132-2.
  • Kroemer G, Galluzzi L, Kepp O, Zitvogel L. Immunogenic cell death in cancer therapy. Annu Rev Immunol. 2013;31(1):51–72. doi:10.1146/annurev-immunol-032712-100008.
  • Kroemer G, Kepp O. Radiochemotherapy-induced elevations of plasma HMGB1 levels predict therapeutic responses in cancer patients. Oncoimmunology. 2021;10(1):2005859. doi:10.1080/2162402X.2021.2005859.
  • Kepp O, Menger L, Vacchelli E, Locher C, Adjemian S, Yamazaki T, Martins I, Sukkurwala AQ, Michaud M, Senovilla L, et al. Crosstalk between ER stress and immunogenic cell death. Cytokine Growth Factor Rev. 2013;24(4):311–318. doi:10.1016/j.cytogfr.2013.05.001.
  • Sistigu A, Yamazaki T, Vacchelli E, Chaba K, Enot DP, Adam J, Vitale I, Goubar A, Baracco EE, Remédios C, et al. Cancer cell-autonomous contribution of type I interferon signaling to the efficacy of chemotherapy. Nat Med. 2014;20(11):1301–1309. doi:10.1038/nm.3708.
  • Sprooten J, Garg AD. Type I interferons and endoplasmic reticulum stress in health and disease. Int Rev Cell Mol Biol. 2020;350:63–118. doi:10.1016/bs.ircmb.2019.10.004.
  • Yamazaki T, Kirchmair A, Sato A, Buqué A, Rybstein M, Petroni G, Bloy N, Finotello F, Stafford L, Navarro Manzano E, et al. Mitochondrial DNA drives abscopal responses to radiation that are inhibited by autophagy. Nat Immunol. 2020;21(10):1160–1171. doi:10.1038/s41590-020-0751-0.
  • Workenhe ST, Pol J, Kroemer G. Tumor-intrinsic determinants of immunogenic cell death modalities. Oncoimmunology. 2021;10(1):1893466. doi:10.1080/2162402X.2021.1893466.
  • Xin M, Lin D, Yan N, Li H, Li J, Huang Z. Oxaliplatin facilitates tumor-infiltration of T cells and natural-killer cells for enhanced tumor immunotherapy in lung cancer model. Anticancer Drugs. 2022;33(2):117–123. doi:10.1097/CAD.0000000000001248.
  • Robert C. A decade of immune-checkpoint inhibitors in cancer therapy. Nat Commun. 2020;11(1):3801. doi:10.1038/s41467-020-17670-y.
  • Husstegge M, Hoang NA, Rebstock J, Monecke A, Gockel I, Weimann A, Schumacher G, Bechmann I, Lordick F, Kallendrusch S, et al. PD-1 inhibition in patient derived tissue cultures of human gastric and gastroesophageal adenocarcinoma. Oncoimmunology. 2021;10(1):1960729. doi:10.1080/2162402X.2021.1960729.
  • Vitale I, Shema E, Loi S, Galluzzi L. Intratumoral heterogeneity in cancer progression and response to immunotherapy. Nat Med. 2021;27(2):212–224. doi:10.1038/s41591-021-01233-9.
  • Galluzzi L, Humeau J, Buque A, Zitvogel L, Kroemer G. Immunostimulation with chemotherapy in the era of immune checkpoint inhibitors. Nat Rev Clin Oncol. 2020;17(12):725–741. doi:10.1038/s41571-020-0413-z.
  • Pfirschke C, Engblom C, Rickelt S, Cortez-Retamozo V, Garris C, Pucci F, Yamazaki T, Poirier-Colame V, Newton A, Redouane Y, et al. Immunogenic chemotherapy sensitizes tumors to checkpoint blockade therapy. Immunity. 2016;44(2):343–354. doi:10.1016/j.immuni.2015.11.024.
  • Zhu H, Shan, Y., Ge, K., Lu, J., Kong, W., & Jia, C. Oxaliplatin induces immunogenic cell death in hepatocellular carcinoma cells and synergizes with immune checkpoint blockade therapy. Cell Oncol (Dordr). 2020;43(6):1203–1214. doi:10.1007/s13402-020-00552-2.
  • Levesque S, Le Naour, J., Pietrocola, F., Paillet, J., Kremer, M., Castoldi, F., & Pol, J. G. A synergistic triad of chemotherapy, immune checkpoint inhibitors, and caloric restriction mimetics eradicates tumors in mice. Oncoimmunology. 2019;8(11):e1657375. doi:10.1080/2162402X.2019.1657375.
  • Sun F, Cui L, Li T, Chen S, Song J, Li D. Oxaliplatin induces immunogenic cells death and enhances therapeutic efficacy of checkpoint inhibitor in a model of murine lung carcinoma. journal of Receptors and Signal transduction. 2019;39(3):208–214. doi:10.1080/10799893.2019.1655050.
  • Song W, Shen L, Wang Y, Liu Q, Goodwin TJ, Li J, Dorosheva O, Liu T, Liu R, Huang L, et al. Synergistic and low adverse effect cancer immunotherapy by immunogenic chemotherapy and locally expressed PD-L1 trap. Nat Commun. 2018;9(1):2237. doi:10.1038/s41467-018-04605-x.
  • Wang W, Wu L, Zhang J, Wu H, Han E, Guo Q. Chemoimmunotherapy by combining oxaliplatin with immune checkpoint blockades reduced tumor burden in colorectal cancer animal model. Biochem Biophys Res Commun. 2017;487(1):1–7. doi:10.1016/j.bbrc.2016.12.180.
  • Maharjan R, Choi JU, Kweon S, Pangeni R, Lee NK, Park SJ, Chang K-Y, Park JW, Byun Y. A novel oral metronomic chemotherapy provokes tumor specific immunity resulting in colon cancer eradication in combination with anti-PD-1 therapy. Biomaterials. 2022;281:121334. doi:10.1016/j.biomaterials.2021.121334.
  • Limagne E, Thibaudin M, Nuttin L, Spill A, Derangère V, Fumet J-D, Amellal N, Peranzoni E, Cattan V, Ghiringhelli F, et al. Trifluridine/Tipiracil plus Oxaliplatin Improves PD-1 Blockade in Colorectal Cancer by Inducing Immunogenic Cell Death and Depleting Macrophages. Cancer Immunol Res. 2019;7(12):1958–1969. doi:10.1158/2326-6066.CIR-19-0228.
  • Grasselly C, Denis M, Bourguignon A, Talhi N, Mathe D, Tourette A, Serre L, Jordheim LP, Matera EL, Dumontet C, et al. The Antitumor Activity of Combinations of Cytotoxic Chemotherapy and Immune Checkpoint Inhibitors Is Model-Dependent. Front Immunol. 2018;9:2100. doi:10.3389/fimmu.2018.02100.
  • Kim W, Chu TH, Nienhüser H, Jiang Z, Del Portillo A, Remotti HE, White RA, Hayakawa Y, Tomita H, Fox JG, et al. PD-1 Signaling Promotes Tumor-Infiltrating Myeloid-Derived Suppressor Cells and Gastric Tumorigenesis in Mice. Gastroenterology. 2021;160(3):781–796. doi:10.1053/j.gastro.2020.10.036.
  • Yamazaki T, Buque A, Ames TD, Galluzzi L. PT-112 induces immunogenic cell death and synergizes with immune checkpoint blockers in mouse tumor models. Oncoimmunology. 2020;9(1):1721810. doi:10.1080/2162402X.2020.1721810.
  • Liu P, Zhao L, Pol J, Levesque S, Petrazzuolo A, Pfirschke C, Engblom C, Rickelt S, Yamazaki T, Iribarren K, et al. Crizotinib-induced immunogenic cell death in non-small cell lung cancer. Nat Commun. 2019;10(1):1486. doi:10.1038/s41467-019-09415-3.
  • Petrazzuolo A, Perez-Lanzon M, Liu P, Maiuri MC, Kroemer G. Crizotinib and ceritinib trigger immunogenic cell death via on-target effects. Oncoimmunology. 2021;10(1):1973197. doi:10.1080/2162402X.2021.1973197.
  • Petrazzuolo A, Perez-Lanzon M, Martins I, Liu P, Kepp O, Minard-Colin V, Maiuri MC, Kroemer G. Pharmacological inhibitors of anaplastic lymphoma kinase (ALK) induce immunogenic cell death through on-target effects. Cell Death Dis. 2021;12(8):713. doi:10.1038/s41419-021-03997-x.
  • Hossain DMS, Javaid S, Cai M, Zhang C, Sawant A, Hinton M, Sathe M, Grein J, Blumenschein W, Pinheiro EM, et al. Dinaciclib induces immunogenic cell death and enhances anti-PD1-mediated tumor suppression. J Clin Invest. 2018;128(2):644–654. doi:10.1172/JCI94586.
  • Xie W, Forveille S, Iribarren K, Sauvat A, Senovilla L, Wang Y, Humeau J, Perez-Lanzon M, Zhou H, Martínez-Leal JF, et al. Lurbinectedin synergizes with immune checkpoint blockade to generate anticancer immunity. Oncoimmunology. 2019;8(11):e1656502. doi:10.1080/2162402X.2019.1656502.
  • Kepp O, Zitvogel L, Kroemer G. Lurbinectedin: an FDA-approved inducer of immunogenic cell death for the treatment of small-cell lung cancer. Oncoimmunology. 2020;9(1):1795995. doi:10.1080/2162402X.2020.1795995.
  • Orecchioni S, Talarico G, Labanca V, Calleri A, Mancuso P, Bertolini F. Vinorelbine, cyclophosphamide and 5-FU effects on the circulating and intratumoural landscape of immune cells improve anti-PD-L1 efficacy in preclinical models of breast cancer and lymphoma. Br J Cancer. 2018;118(10):1329–1336. doi:10.1038/s41416-018-0076-z.
  • Xie W, Mondragón L, Mauseth B, Wang Y, Pol J, Lévesque S, Zhou H, Yamazaki T, Eksteen JJ, Zitvogel, et al. Tumor lysis with LTX-401 creates anticancer immunity. Oncoimmunology. 2019;8(7):1594555. doi:10.1080/2162402X.2019.1594555.
  • Bezu L, Wu Chuang A, Sauvat A, Humeau J, Xie W, Cerrato G, Liu P, Zhao L, Zhang S, Le Naour J, et al. Local anesthetics elicit immune-dependent anticancer effects. J Immunother Cancer. 2022;10(4):e004151. doi:10.1136/jitc-2021-004151.
  • Chen G, Chen Z, Wen D, Wang Z, Li H, Zeng Y, Dotti G, Wirz RE, Gu Z. Transdermal cold atmospheric plasma-mediated immune checkpoint blockade therapy. Proc Natl Acad Sci U S A. 2020;117(7):3687–3692. doi:10.1073/pnas.1917891117.
  • Lin A, Gorbanev Y, De Backer J, Van Loenhout J, Van Boxem W, Lemière F, Cos P, Dewilde S, Smits E, Bogaerts A, et al. Non-Thermal Plasma as a Unique Delivery System of Short-Lived Reactive Oxygen and Nitrogen Species for Immunogenic Cell Death in Melanoma Cells. Adv Sci (Weinh). 2019;6(6):1802062. doi:10.1002/advs.201802062.
  • Herter-Sprie GS, Koyama S, Korideck H, Hai J, Deng J, Li YY, Buczkowski KA, Grant AK, Ullas S, Rhee K, et al. Synergy of radiotherapy and PD-1 blockade in Kras-mutant lung cancer. JCI Insight. 2016;1(9):e87415. doi:10.1172/jci.insight.87415.
  • Zhang H, Xie W, Zhang Y, Dong X, Liu C, Yi J, Zhang S, Wen C, Zheng L, Wang H, et al. Oncolytic adenoviruses synergistically enhance anti-PD-L1 and anti-CTLA-4 immunotherapy by modulating the tumour microenvironment in a 4T1 orthotopic mouse model. Cancer Gene Ther. 2022;29(5):456–465. doi:10.1038/s41417-021-00389-3.
  • Humeau J, Sauvat A, Cerrato G, Xie W, Loos F, Iannantuoni F, Bezu L, Lévesque S, Paillet J, Pol J, et al. Inhibition of transcription by dactinomycin reveals a new characteristic of immunogenic cell stress. EMBO Mol Med. 2020;12(5):e11622. doi:10.15252/emmm.201911622.
  • Kroemer G, Kepp O. Small cell lung cancer responds to immunogenic chemotherapy followed by PD-1 blockade. Oncoimmunology. 2021;10(1996686). doi:10.1080/2162402X.2021.1996686.
  • Zhu H, Shan Y, Ge K, Lu J, Kong W, Jia C. Oxaliplatin induces immunogenic cell death in hepatocellular carcinoma cells and synergizes with immune checkpoint blockade therapy. Cell Oncol (Dordr). 2020;43(6):1203–1214. doi:10.1007/s13402-020-00552-2.
  • Srivastava S, Furlan SN, Jaeger-Ruckstuhl CA, Sarvothama M, Berger C, Smythe KS, Garrison SM, Specht JM, Lee SM, Amezquita RA, et al. Immunogenic Chemotherapy Enhances Recruitment of CAR-T cells to lung tumors and improves antitumor efficacy when combined with checkpoint blockade. Cancer Cell. 2021;39(2):193–208 e110. doi:10.1016/j.ccell.2020.11.005.
  • Siew YY, Soek-Ying Neo, Hui-Chuing Yew, Shun-Wei Lim, Yi-Cheng Ng,Si-Min Lew, Wei-Guang Seetoh, See-Voon Seow, and Hwee-Ling Koh. Oxaliplatin regulates expression of stress ligands in ovarian cancer cells and modulates their susceptibility to natural killer cell-mediated cytotoxicity. Int Immunol. 2015;27(12):621–632. doi:10.1093/intimm/dxv041.
  • Gou HF, Zhou L, Huang J, Chen XC. Intraperitoneal oxaliplatin administration inhibits the tumor immunosuppressive microenvironment in an abdominal implantation model of colon cancer. Mol Med Rep. 2018;18(2):2335–2341. doi:10.3892/mmr.2018.9219.
  • Stojanovska V, Prakash M, McQuade R, Fraser S, Apostolopoulos V, Sakkal S, Nurgali K. Oxaliplatin treatment alters systemic immune responses. Biomed Res Int. 2019;2019:4650695. doi:10.1155/2019/4650695.
  • Kalanxhi E, Meltzer S, Schou JV, Larsen FO, Dueland S, Flatmark K, Jensen BV, Hole KH, Seierstad T, Redalen KR, et al. Systemic immune response induced by oxaliplatin-based neoadjuvant therapy favours survival without metastatic progression in high-risk rectal cancer. Br J Cancer. 2018;118(10):1322–1328. doi:10.1038/s41416-018-0085-y.
  • Xu J, Xu N, Bai Y, Liu R, Mao C, Sui H, Wang X, Jiang Q, Dou Y. Anti-PD-1 antibody HX008 combined with oxaliplatin plus capecitabine for advanced gastric or esophagogastric junction cancer: a multicenter, single-arm, open-label, phase Ib trial. Oncoimmunology. 2020;10(1):1864908. doi:10.1080/2162402X.2020.1864908.
  • Zhang AZ, Yuan X, Liang WH, Zhang HJ, Li Y, Xie YF, Li JF, Jiang CH, Li FP, Shen XH, et al. Immune infiltration in gastric cancer microenvironment and its clinical significance. Front Cell Dev Biol. 2021;9:762029. doi:10.3389/fcell.2021.762029.
  • Li C, Pan J, Jiang Y, Yu Y, Jin Z, Chen X. Characteristics of the immune cell infiltration landscape in gastric cancer to assistant immunotherapy. Front Genet. 2021;12:793628. doi:10.3389/fgene.2021.793628.
  • Xing X, Shi J, Jia Y, Dou Y, Li Z, Dong B, Guo T, Cheng X, Li X, Du H, et al. Effect of neoadjuvant chemotherapy on the immune microenvironment in gastric cancer as determined by multiplex immunofluorescence and T cell receptor repertoire analysis. J Immunother Cancer. 2022;10(3):e003984. doi:10.1136/jitc-2021-003984.
  • Janjigian YY, Shitara K, Moehler M, Garrido M, Salman P, Shen L, Wyrwicz L, Yamaguchi K, Skoczylas T, Campos Bragagnoli A, et al. First-line nivolumab plus chemotherapy versus chemotherapy alone for advanced gastric, gastro-oesophageal junction, and oesophageal adenocarcinoma (CheckMate 649): a randomised, open-label, phase 3 trial. Lancet. 2021;398(10294):27–40. doi:10.1016/S0140-6736(21)00797-2.
  • Shitara K, Van Cutsem E, Bang Y-J, Fuchs C, Wyrwicz L, Lee K-W, Kudaba I, Garrido M, Chung HC, Lee J, et al. Efficacy and safety of pembrolizumab or pembrolizumab plus chemotherapy vs chemotherapy alone for patients with first-line, advanced gastric cancer: the KEYNOTE-062 phase 3 randomized clinical trial. JAMA Oncol. 2020;6(10):1571–1580. doi:10.1001/jamaoncol.2020.3370.
  • Janjigian YY, Kawazoe A, Yañez P, Li N, Lonardi S, Kolesnik O, Barajas O, Bai Y, Shen L, Tang Y, et al. The KEYNOTE-811 trial of dual PD-1 and HER2 blockade in HER2-positive gastric cancer. Nature. 2021;600(7890):727–730. doi:10.1038/s41586-021-04161-3.