2,415
Views
40
CrossRef citations to date
0
Altmetric
Original Research

CAR T-cell immunotherapy of MET-expressing malignant mesothelioma

, ORCID Icon, , , , , , , , , , , & show all
Article: e1363137 | Received 10 Apr 2017, Accepted 31 Jul 2017, Published online: 25 Aug 2017

References

  • Bianchi C, Bianchi T. Global mesothelioma epidemic: Trend and features. Indian J Occup Environ Med. 2014;18:82-8. doi:10.4103/0019-5278.146897. PMID:25568603.
  • Izzi V, Masuelli L, Tresoldi I, Foti C, Modesti A, Bei R. Immunity and malignant mesothelioma: from mesothelial cell damage to tumor development and immune response-based therapies. Cancer Lett. 2012;322:18-34. doi:10.1016/j.canlet.2012.02.034. PMID:22394996.
  • Thapa B, Watkins DN, John T. Immunotherapy for malignant mesothelioma: reality check. Expert Rev Anticancer Ther. 2016;16:1167-1176. doi:10.1080/14737140.2016.1241149. PMID:27669108.
  • Lievense LA, Sterman DH, Cornelissen R, Aerts JG. Checkpoint Blockade in Lung Cancer and Mesothelioma. Am J Respir Crit Care Med. 2017;196:274-282. doi:10.1164/rccm.201608-1755CI. PMID:28252315.
  • Whilding LM, Maher J. CAR T-cell immunotherapy: The path from the by-road to the freeway? Mol Oncol. 2015;9:1994-2018. doi:10.1016/j.molonc.2015.10.012. PMID:26563646.
  • Adusumilli PS, Cherkassky L, Villena-Vargas J, Colovos C, Servais E, Plotkin J, Jones DR, Sadelain M. Regional delivery of mesothelin-targeted CAR T cell therapy generates potent and long-lasting CD4-dependent tumor immunity. Sci Transl Med. 2014;6:261ra151. doi:10.1126/scitranslmed.3010162. PMID:25378643.
  • Cherkassky L, Morello A, Villena-Vargas J, Feng Y, Dimitrov DS, Jones DR, Sadelain M, Adusumilli PS. Human CAR T cells with cell-intrinsic PD-1 checkpoint blockade resist tumor-mediated inhibition. J Clin Invest. 2016;126:3130-44. doi:10.1172/JCI83092. PMID:27454297.
  • Schuberth PC, Hagedorn C, Jensen SM, Gulati P, van den Broek M, Mischo A, Soltermann A, Jungel A, Marroquin Belaunzaran O, Stahel R, et al. Treatment of malignant pleural mesothelioma by fibroblast activation protein-specific re-directed T cells. J Transl Med. 2013;11:187. doi:10.1186/1479-5876-11-187. PMID:23937772.
  • Moon EK, Wang LC, Dolfi DV, Wilson CB, Ranganathan R, Sun J, Kapoor V, Scholler J, Pure E, Milone MC, et al. Multifactorial T-cell hypofunction that is reversible can limit the efficacy of chimeric antigen receptor-transduced human T cells in solid tumors. Clin Cancer Res. 2014;20:4262-73. doi:10.1158/1078-0432.CCR-13-2627. PMID:24919573.
  • Mayor M, Zeltsman M, McGee E, Adusumilli PS. A regional approach for CAR T-cell therapy for mesothelioma: from mouse models to clinical trial. Immunotherapy. 2016;8:491-4. doi:10.2217/imt-2016-0008. PMID:27140404.
  • O'Hara M, Stashwick C, Haas AR, Tanyi JL. Mesothelin as a target for chimeric antigen receptor-modified T cells as anticancer therapy. Immunotherapy. 2016;8:449-60. doi:10.2217/imt.16.4. PMID:26973126.
  • Beatty GL, Haas AR, Maus MV, Torigian DA, Soulen MC, Plesa G, Chew A, Zhao Y, Levine BL, Albelda SM, et al. Mesothelin-specific chimeric antigen receptor mRNA-engineered T cells induce anti-tumor activity in solid malignancies. Cancer Immunol Res. 2014;2:112-20. doi:10.1158/2326-6066.CIR-13-0170. PMID:24579088.
  • Jeannon JP, Ofu E, Balfour A, Bowman J, Simo R. The natural history of untreated squamous cell carcinoma of the head and neck: how we do it. Clin Otolaryngol. 2011;36:384-8. doi:10.1111/j.1749-4486.2011.02325.x. PMID:21848553.
  • Papa S, van Schalkwyk M, Maher J. Clinical Evaluation of ErbB-Targeted CAR T-Cells, Following Intracavity Delivery in Patients with ErbB-Expressing Solid Tumors. Methods Mol Biol. 2015;1317:365-82. doi:10.1007/978-1-4939-2727-2_21. PMID:26072418.
  • Klampatsa A, Achkova DY, Davies DM, Parente-Pereira AC, Woodman N, Rosekilly J, Osborne G, Thayaparan T, Bille A, Sheaf M, et al. Intracavitary ‘T4 immunotherapy’ of malignant mesothelioma using pan-ErbB re-targeted CAR T-cells. Cancer Lett. 2017;393:52-9. doi:10.1016/j.canlet.2017.02.015. PMID:28223167.
  • Tolnay E, Kuhnen C, Wiethege T, Konig JE, Voss B, Muller KM. Hepatocyte growth factor/scatter factor and its receptor c-Met are overexpressed and associated with an increased microvessel density in malignant pleural mesothelioma. Journal of cancer research and clinical oncology 1998;124:291-6. doi:10.1007/s004320050171. PMID:9692834.
  • Kawaguchi K, Murakami H, Taniguchi T, Fujii M, Kawata S, Fukui T, Kondo Y, Osada H, Usami N, Yokoi K, et al. Combined inhibition of MET and EGFR suppresses proliferation of malignant mesothelioma cells. Carcinogenesis. 2009;30:1097-105. doi:10.1093/carcin/bgp097. PMID:19380521.
  • Jagadeeswaran R, Ma PC, Seiwert TY, Jagadeeswaran S, Zumba O, Nallasura V, Ahmed S, Filiberti R, Paganuzzi M, Puntoni R, et al. Functional analysis of c-Met/hepatocyte growth factor pathway in malignant pleural mesothelioma. Cancer Res. 2006;66:352-61. doi:10.1158/0008-5472.CAN-04-4567. PMID:16397249.
  • Levallet G, Vaisse-Lesteven M, Le Stang N, Ilg AG, Brochard P, Astoul P, Pairon JC, Bergot E, Zalcman G, Galateau-Salle F. Plasma cell membrane localization of c-MET predicts longer survival in patients with malignant mesothelioma: a series of 157 cases from the MESOPATH Group. Journal of thoracic oncology: official publication of the International Association for the Study of Lung Cancer. 2012;7:599-606. doi:10.1097/JTO.0b013e3182417da5. PMID:22246193.
  • Bronte G, Incorvaia L, Rizzo S, Passiglia F, Galvano A, Rizzo F, Rolfo C, Fanale D, Listi A, Natoli C, et al. The resistance related to targeted therapy in malignant pleural mesothelioma: why has not the target been hit yet? Critical Reviews in Oncology/ Hematology. 2016;107:20-32. doi:10.1016/j.critrevonc.2016.08.011. PMID:27823648.
  • Thayaparan T, Spicer JF, Maher J. The role of the HGF/Met axis in mesothelioma. Biochemical Society transactions. 2016;44:363-70. doi:10.1042/BST20150252. PMID:27068941.
  • Kanteti R, Dhanasingh I, Kawada I, Lennon FE, Arif Q, Bueno R, Hasina R, Husain AN, Vigneswaran W, Seiwert T, et al. MET and PI3K/mTOR as a potential combinatorial therapeutic target in malignant pleural mesothelioma. PloS one. 2014;9:e105919. doi:10.1371/journal.pone.0105919. PMID:25221930.
  • Leon LG, Gemelli M, Sciarrillo R, Avan A, Funel N, Giovannetti E. Synergistic activity of the c-Met and tubulin inhibitor tivantinib (ARQ197) with pemetrexed in mesothelioma cells. Curr Drug Targets. 2014;15:1331-40. doi:10.2174/1389450116666141205160924. PMID:25483224.
  • Cioce V, Csaky KG, Chan AM, Bottaro DP, Taylor WG, Jensen R, Aaronson SA, Rubin JS. Hepatocyte growth factor (HGF)/NK1 is a naturally occurring HGF/scatter factor variant with partial agonist/antagonist activity. J Biol Chem 1996;271:13110-5. doi:10.1074/jbc.271.22.13110. PMID:8662798.
  • Lokker NA, Godowski PJ. Generation and characterization of a competitive antagonist of human hepatocyte growth factor, HGF/NK1. J Biol Chem 1993;268:17145-50. PMID:8349603.
  • Jakubczak JL, LaRochelle WJ, Merlino G. NK1, a natural splice variant of hepatocyte growth factor/scatter factor, is a partial agonist in vivo. Molecular and cellular biology 1998;18:1275-83. doi:10.1128/MCB.18.3.1275. PMID:9488442.
  • Simon Davis DA, Parish CR. Heparan sulfate: a ubiquitous glycosaminoglycan with multiple roles in immunity. Front Immunol. 2013;4:470. doi:10.3389/fimmu.2013.00470. PMID:24391644.
  • Lietha D, Chirgadze DY, Mulloy B, Blundell TL, Gherardi E. Crystal structures of NK1-heparin complexes reveal the basis for NK1 activity and enable engineering of potent agonists of the MET receptor. EMBO J. 2001;20:5543-55. doi:10.1093/emboj/20.20.5543. PMID:11597998.
  • Maher J, Brentjens RJ, Gunset G, Riviere I, Sadelain M. Human T-lymphocyte cytotoxicity and proliferation directed by a single chimeric TCRzeta /CD28 receptor. Nat Biotechnol. 2002;20:70-5. doi:10.1038/nbt0102-70. PMID:11753365.
  • Jones DS, 2nd, Tsai PC, Cochran JR. Engineering hepatocyte growth factor fragments with high stability and activity as Met receptor agonists and antagonists. Proc Natl Acad Sci U S A. 2011;108:13035-40. doi:10.1073/pnas.1102561108. PMID:21788476.
  • Whilding LM, Parente-Pereira AC, Zabinski T, Davies DM, Petrovic RM, Kao YV, Saxena SA, Romain A, Costa-Guerra JA, Violette S, et al. Targeting of Aberrant alphavbeta6 Integrin Expression in Solid Tumors Using Chimeric Antigen Receptor-Engineered T Cells. Mol Ther. 2017;25:259-73. doi:10.1016/j.ymthe.2016.10.012. PMID:28129120.
  • Davies DM, Foster J, Van Der Stegen SJ, Parente-Pereira AC, Chiapero-Stanke L, Delinassios GJ, Burbridge SE, Kao V, Liu Z, Bosshard-Carter L, et al. Flexible targeting of ErbB dimers that drive tumorigenesis by using genetically engineered T cells. Mol Med. 2012;18:565-76. doi:10.2119/molmed.2011.00493. PMID:22354215.
  • Wilkie S, Burbridge SE, Chiapero-Stanke L, Pereira AC, Cleary S, van der Stegen SJ, Spicer JF, Davies DM, Maher J. Selective expansion of chimeric antigen receptor-targeted T-cells with potent effector function using interleukin-4. J Biol Chem. 2010;285:25538-44. doi:10.1074/jbc.M110.127951. PMID:20562098.
  • Volz Y, Koschut D, Matzke-Ogi A, Dietz MS, Karathanasis C, Richert L, Wagner MG, Mely Y, Heilemann M, Niemann HH, et al. Direct binding of hepatocyte growth factor and vascular endothelial growth factor to CD44v6. Biosci Rep. 2015;35. doi:10.1042/BSR20150093. PMID:26181364.
  • Hartmann G, Prospero T, Brinkmann V, Ozcelik C, Winter G, Hepple J, Batley S, Bladt F, Sachs M, Birchmeier C, et al. Engineered mutants of HGF/SF with reduced binding to heparan sulphate proteoglycans, decreased clearance and enhanced activity in vivo. Current biology: CB 1998;8:125-34. doi:10.1016/S0960-9822(98)70059-4. PMID:9443912.
  • Derksen PW, Keehnen RM, Evers LM, van Oers MH, Spaargaren M, Pals ST. Cell surface proteoglycan syndecan-1 mediates hepatocyte growth factor binding and promotes Met signaling in multiple myeloma. Blood. 2002;99:1405-10. doi:10.1182/blood.V99.4.1405. PMID:11830493.
  • Latouche JB, Sadelain M. Induction of human cytotoxic T lymphocytes by artificial antigen-presenting cells. Nat Biotechnol. 2000;18:405-9. doi:10.1038/74455. PMID:10748520.
  • Bellosta P, Iwahori A, Plotnikov AN, Eliseenkova AV, Basilico C, Mohammadi M. Identification of receptor and heparin binding sites in fibroblast growth factor 4 by structure-based mutagenesis. Molecular and cellular biology. 2001;21:5946-57. doi:10.1128/MCB.21.17.5946-5957.2001. PMID:11486033.
  • Nasimuzzaman M, Persons DA. Cell Membrane-associated heparan sulfate is a receptor for prototype foamy virus in human, monkey, and rodent cells. Mol Ther. 2012;20:1158-66. doi:10.1038/mt.2012.41. PMID:22434139.
  • Heidari-Hamedani G, Vives RR, Seffouh A, Afratis NA, Oosterhof A, van Kuppevelt TH, Karamanos NK, Metintas M, Hjerpe A, Dobra K, et al. Syndecan-1 alters heparan sulfate composition and signaling pathways in malignant mesothelioma. Cell Signal. 2015;27:2054-67. doi:10.1016/j.cellsig.2015.07.017. PMID:26210886.
  • Komarowska I, Coe D, Wang G, Haas R, Mauro C, Kishore M, Cooper D, Nadkarni S, Fu H, Steinbruchel DA, et al. Hepatocyte Growth Factor Receptor c-Met Instructs T Cell Cardiotropism and Promotes T Cell Migration to the Heart via Autocrine Chemokine Release. Immunity. 2015;42:1087-99. doi:10.1016/j.immuni.2015.05.014. PMID:26070483.
  • Frigault MJ, Lee J, Basil MC, Carpenito C, Motohashi S, Scholler J, Kawalekar OU, Guedan S, McGettigan SE, Posey AD, Jr., et al. Identification of chimeric antigen receptors that mediate constitutive or inducible proliferation of T cells. Cancer Immunol Res. 2015;3:356-67. doi:10.1158/2326-6066.CIR-14-0186. PMID:25600436.
  • Catlow KR, Deakin JA, Wei Z, Delehedde M, Fernig DG, Gherardi E, Gallagher JT, Pavao MS, Lyon M. Interactions of hepatocyte growth factor/scatter factor with various glycosaminoglycans reveal an important interplay between the presence of iduronate and sulfate density. J Biol Chem. 2008;283:5235-48. doi:10.1074/jbc.M706589200. PMID:18156180.
  • Johansson CM. Biophysical characterisation of the hepatocyte growth factor – glycosaminglycan interaction. PhD Thesis submission to the University of Edinburgh. 2011. https://www.era.lib.ed.ac.uk/handle/1842/9904.
  • Zhou H, Casas-Finet JR, Heath Coats R, Kaufman JD, Stahl SJ, Wingfield PT, Rubin JS, Bottaro DP, Byrd RA. Identification and dynamics of a heparin-binding site in hepatocyte growth factor. Biochemistry 1999;38:14793-802. doi:10.1021/bi9908641. PMID:10555961.
  • Merkulova-Rainon T, England P, Ding S, Demerens C, Tobelem G. The N-terminal domain of hepatocyte growth factor inhibits the angiogenic behavior of endothelial cells independently from binding to the c-met receptor. J Biol Chem. 2003;278:37400-8. doi:10.1074/jbc.M212768200. PMID:12847110.
  • Kaur S, Kuznetsova SA, Pendrak ML, Sipes JM, Romeo MJ, Li Z, Zhang L, Roberts DD. Heparan sulfate modification of the transmembrane receptor CD47 is necessary for inhibition of T cell receptor signaling by thrombospondin-1. J Bio Chem. 2011;286:14991-5002. doi:10.1074/jbc.M110.179663. PMID:21343308.
  • Jones KS, Petrow-Sadowski C, Bertolette DC, Huang Y, Ruscetti FW. Heparan sulfate proteoglycans mediate attachment and entry of human T-cell leukemia virus type 1 virions into CD4+ T cells. J Virol. 2005;79:12692-702. doi:10.1128/JVI.79.20.12692-12702.2005. PMID:16188972.
  • Fadnes B, Husebekk A, Svineng G, Rekdal O, Yanagishita M, Kolset SO, Uhlin-Hansen L. The proteoglycan repertoire of lymphoid cells. Glycoconj J. 2012;29:513-23. doi:10.1007/s10719-012-9427-9. PMID:22777011.
  • Ross J, Gherardi E, Mallorqui-Fernandez N, Bocci M, Sobkowicz A, Rees M, Rowe A, Ellmerich S, Massie I, Soeda J, et al. Protein engineered variants of hepatocyte growth factor/scatter factor promote proliferation of primary human hepatocytes and in rodent liver. Gastroenterology. 2012;142:897-906. doi:10.1053/j.gastro.2011.12.006. PMID:22178588.
  • Long AH, Haso WM, Shern JF, Wanhainen KM, Murgai M, Ingaramo M, Smith JP, Walker AJ, Kohler ME, Venkateshwara VR, et al. 4-1BB costimulation ameliorates T cell exhaustion induced by tonic signaling of chimeric antigen receptors. Nat Med. 2015;21:581-90.doi:10.1038/nm.3838. PMID:25939063.
  • van der Stegen SJ, Davies DM, Wilkie S, Foster J, Sosabowski JK, Burnet J, Whilding LM, Petrovic RM, Ghaem-Maghami S, Mather S, et al. Preclinical in vivo modeling of cytokine release syndrome induced by ErbB-retargeted human T cells: identifying a window of therapeutic opportunity? J Immunol. 2013;191:4589-98. doi:10.4049/jimmunol.1301523. PMID:24062490.
  • Papa S, Adami AA, Metoudi M, Achkova DY, van Schalkwyk M, Parente-Pereira AC, Bosshard-Carter L, Whilding LM, van der Stegen S, Davies D.M., et al. Online Proceedings of the Annual Meeting of the American Association for Cancer Research. http://wwwabstractsonlinecom/pp8/ – !/4292/presentation/12333. 2017.
  • Hultberg A, Morello V, Huyghe L, De Jonge N, Blanchetot C, Hanssens V, De Boeck G, Silence K, Festjens E, Heukers R, et al. Depleting MET-Expressing Tumor Cells by ADCC Provides a Therapeutic Advantage over Inhibiting HGF/MET Signaling. Cancer Res. 2015;75:3373-83. doi:10.1158/0008-5472.CAN-15-0356. PMID:26141862.
  • Wilkie S, van Schalkwyk MC, Hobbs S, Davies DM, van der Stegen SJ, Pereira AC, Burbridge SE, Box C, Eccles SA, Maher J. Dual Targeting of ErbB2 and MUC1 in Breast Cancer Using Chimeric Antigen Receptors Engineered to Provide Complementary Signaling. J Clin Immunol. 2012;32:1059-70. doi:10.1007/s10875-012-9689-9. PMID:22526592.
  • Kloss CC, Condomines M, Cartellieri M, Bachmann M, Sadelain M. Combinatorial antigen recognition with balanced signaling promotes selective tumor eradication by engineered T cells. Nat Biotechnol. 2013;31:71-5. doi:10.1038/nbt.2459. PMID:23242161.
  • Straathof KC, Pule MA, Yotnda P, Dotti G, Vanin EF, Brenner MK, Heslop HE, Spencer DM, Rooney CM. An inducible caspase 9 safety switch for T-cell therapy. Blood. 2005;105:4247-54. doi:10.1182/blood-2004-11-4564. PMID:15728125.
  • Wilkie S, Picco G, Foster J, Davies DM, Julien S, Cooper L, Arif S, Mather SJ, Taylor-Papadimitriou J, Burchell JM, et al. Retargeting of human T cells to tumor-associated MUC1: the evolution of a chimeric antigen receptor. J Immunol. 2008;180:4901-9. doi:10.4049/jimmunol.180.7.4901. PMID:18354214.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.