Redirected antitumor activity of primary human lymphocytes transduced with a fully human anti-mesothelin chimeric receptor

Molecular Therapy

Volumn 20, Issue 3, 2012, Pages 633-643

  Lanitis, Evripidis ^a,b   Poussin, Mathilde ^a   Hagemann, Ian S ^c   Coukos, George ^a   Sandaltzopoulos, Raphael ^b   Scholler, Nathalie ^a   Powell Jr , Daniel J ^a,c  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b DEMOCRITUS UNIVERSITY OF THRACE   (Greece)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHIMERIC PROTEIN; GAMMA INTERFERON; INTERLEUKIN 2; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MESOTHELIN; MESOTHELIN CHIMERIC RECEPTOR ANTIBODY; PROTEIN ANTIBODY; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN SPECIFICITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; BIOLUMINESCENCE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL THERAPY; COCULTURE; CONTROLLED STUDY; CYTOKINE RELEASE; DEGRANULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOGENICITY; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTE ACTIVATION; MOUSE; NONHUMAN; OVARY CANCER; PROTEIN CROSS LINKING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN POLYMORPHISM; SIGNAL TRANSDUCTION; T LYMPHOCYTE; UPREGULATION;

EID: 84857794017     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2011.256     Document Type: Article

References (44)

1. Mansoor, W, Gilham, DE, Thistlethwaite, FC and Hawkins, RE (2005). Engineering T cells for cancer therapy. Br J Cancer 93: 1085-1091. (Pubitemid 41670690)
2. Han, LY, Fletcher, MS, Urbauer, DL, Mueller, P, Landen, CN, Kamat, AA et al. (2008). HLA class I antigen processing machinery component expression and intratumoral T-Cell infiltrate as independent prognostic markers in ovarian carcinoma. Clin Cancer Res 14: 3372-3379.
3. Gross, G, Waks, T and Eshhar, Z (1989). Expression of immunoglobulin-T-cell receptor chimeric molecules as functional receptors with antibody-type specificity. Proc Natl Acad Sci USA 86: 10024-10028. (Pubitemid 20030768)
4. Jena, B, Dotti, G and Cooper, LJ (2010). Redirecting T-cell specificity by introducing a tumor-specific chimeric antigen receptor. Blood 116: 1035-1044.
5. Kershaw, MH, Westwood, JA, Parker, LL, Wang, G, Eshhar, Z, Mavroukakis, SA et al. (2006). A phase I study on adoptive immunotherapy using gene-modified T cells for ovarian cancer. Clin Cancer Res 12(20 Pt 1): 6106-6115. (Pubitemid 44703776)
6. Park, JR, Digiusto, DL, Slovak, M, Wright, C, Naranjo, A, Wagner, J et al. (2007). Adoptive transfer of chimeric antigen receptor re-directed cytolytic T lymphocyte clones in patients with neuroblastoma. Mol Ther 15: 825-833. (Pubitemid 46432004)
7. Chang, K and Pastan, I (1996). Molecular cloning of mesothelin, a differentiation antigen present on mesothelium, mesotheliomas, and ovarian cancers. Proc Natl Acad Sci USA 93: 136-140. (Pubitemid 26041483)
8. Argani, P, Iacobuzio-Donahue, C, Ryu, B, Rosty, C, Goggins, M, Wilentz, RE et al. (2001). Mesothelin is overexpressed in the vast majority of ductal adenocarcinomas of the pancreas: identification of a new pancreatic cancer marker by serial analysis of gene expression (SAGE). Clin Cancer Res 7: 3862-3868. (Pubitemid 34044602)
9. Ho, M, Bera, TK, Willingham, MC, Onda, M, Hassan, R, FitzGerald, D et al. (2007). Mesothelin expression in human lung cancer. Clin Cancer Res 13: 1571-1575. (Pubitemid 46450449)
10. Scholler, N, Fu, N, Yang, Y, Ye, Z, Goodman, GE, HellstR̈, KE et al. (1999). Soluble member(s) of the mesothelin/megakaryocyte potentiating factor family are detectable in sera from patients with ovarian carcinoma. Proc Natl Acad Sci USA 96: 11531-11536. (Pubitemid 29487415)
11. Robinson, BW, Creaney, J, Lake, R, Nowak, A, Musk, AW, de Klerk, N et al. (2005). Soluble mesothelin-related protein-a blood test for mesothelioma. Lung Cancer 49 (suppl. 1): S109-S111. (Pubitemid 40798859)
12. Hassan, R, Remaley, AT, Sampson, ML, Zhang, J, Cox, DD, Pingpank, J et al. (2006). Detection and quantitation of serum mesothelin, a tumor marker for patients with mesothelioma and ovarian cancer. Clin Cancer Res 12: 447-453. (Pubitemid 43166134)
13. Rump, A, Morikawa, Y, Tanaka, M, Minami, S, Umesaki, N, Takeuchi, M et al. (2004). Binding of ovarian cancer antigen CA125/MUC16 to mesothelin mediates cell adhesion. J Biol Chem 279: 9190-9198. (Pubitemid 38295982)
14. Kaneko, O, Gong, L, Zhang, J, Hansen, JK, Hassan, R, Lee, B et al. (2009). A binding domain on mesothelin for CA125/MUC16. J Biol Chem 284: 3739-3749.
15. Cheng, WF, Huang, CY, Chang, MC, Hu, YH, Chiang, YC, Chen, YL et al. (2009). High mesothelin correlates with chemoresistance and poor survival in epithelial ovarian carcinoma. Br J Cancer 100: 1144-1153.
16. Thomas, AM, Santarsiero, LM, Lutz, ER, Armstrong, TD, Chen, YC, Huang, LQ et al. (2004). Mesothelin-specific CD8(+) T cell responses provide evidence of in vivo cross-priming by antigen-presenting cells in vaccinated pancreatic cancer patients. J Exp Med 200: 297-306. (Pubitemid 39031249)
17. Carpenito, C, Milone, MC, Hassan, R, Simonet, JC, Lakhal, M, Suhoski, MM et al. (2009). Control of large, established tumor xenografts with genetically retargeted human T cells containing CD28 and CD137 domains. Proc Natl Acad Sci USA 106: 3360-3365.
18. Bergan, L, Gross, JA, Nevin, B, Urban, N and Scholler, N (2007). Development and in vitro validation of anti-mesothelin biobodies that prevent CA125/Mesothelindependent cell attachment. Cancer Lett 255: 263-274. (Pubitemid 47268642)
19. Milone, MC, Fish, JD, Carpenito, C, Carroll, RG, Binder, GK, Teachey, D et al. (2009). Chimeric receptors containing CD137 signal transduction domains mediate enhanced survival of T cells and increased antileukemic efficacy in vivo. Mol Ther 17: 1453-1464.
20. Jackaman, C, Bundell, CS, Kinnear, BF, Smith, AM, Filion, P, van Hagen, D et al. (2003). IL-2 intratumoral immunotherapy enhances CD8+ T cells that mediate destruction of tumor cells and tumor-associated vasculature: a novel mechanism for IL-2. J Immunol 171: 5051-5063. (Pubitemid 37432786)
21. Hassan, R, Kreitman, RJ, Pastan, I and Willingham, MC (2005). Localization of mesothelin in epithelial ovarian cancer. Appl Immunohistochem Mol Morphol 13: 243-247. (Pubitemid 41209017)
22. Betts, MR, Brenchley, JM, Price, DA, De Rosa, SC, Douek, DC, Roederer, M et al. (2003). Sensitive and viable identification of antigen-specific CD8+ T cells by a flow cytometric assay for degranulation. J Immunol Methods 281: 65-78. (Pubitemid 37324571)
23. Yen, MJ, Hsu, CY, Mao, TL, Wu, TC, Roden, R, Wang, TL et al. (2006). Diffuse mesothelin expression correlates with prolonged patient survival in ovarian serous carcinoma. Clin Cancer Res 12(3 Pt 1): 827-831. (Pubitemid 43259864)
24. Hellstrom, I (2008). Mesothelin in serum. Biochem Biophys Res Commun 376: 629; author reply 630.
25. Alvarez-Vallina, L and Hawkins, RE (1996). Antigen-specific targeting of CD28-mediated T cell co-stimulation using chimeric single-chain antibody variable fragment-CD28 receptors. Eur J Immunol 26: 2304-2309. (Pubitemid 26340928)
26. Beecham, EJ, Ma, Q, Ripley, R and Junghans, RP (2000). Coupling CD28 costimulation to immunoglobulin T-cell receptor molecules: the dynamics of T-cell proliferation and death. J Immunother 23: 631-642.
27. Kowolik, CM, Topp, MS, Gonzalez, S, Pfeiffer, T, Olivares, S, Gonzalez, N et al. (2006). CD28 costimulation provided through a CD19-specific chimeric antigen receptor enhances in vivo persistence and antitumor efficacy of adoptively transferred T cells. Cancer Res 66: 10995-11004. (Pubitemid 44876999)
28. Chowdhury, PS, Viner, JL, Beers, R and Pastan, I (1998). Isolation of a high-affinity stable single-chain Fv specific for mesothelin from DNA-immunized mice by phage display and construction of a recombinant immunotoxin with anti-tumor activity. Proc Natl Acad Sci USA 95: 669-674. (Pubitemid 28083801)
29. Hassan, R, Bullock, S, Premkumar, A, Kreitman, RJ, Kindler, H, Willingham, MC et al. (2007). Phase I study of SS1P, a recombinant anti-mesothelin immunotoxin given as a bolus I.V. infusion to patients with mesothelin-expressing mesothelioma, ovarian, and pancreatic cancers. Clin Cancer Res 13: 5144-5149. (Pubitemid 47502082)
30. Kreitman, RJ, Hassan, R, Fitzgerald, DJ and Pastan, I (2009). Phase I trial of continuous infusion anti-mesothelin recombinant immunotoxin SS1P. Clin Cancer Res 15: 5274-5279.
31. Lamers, CH, Sleijfer, S, Vulto, AG, Kruit, WH, Kliffen, M, Debets, R et al. (2006). Treatment of metastatic renal cell carcinoma with autologous T-lymphocytes genetically retargeted against carbonic anhydrase IX: first clinical experience. J Clin Oncol 24: e20-e22.
32. Lamers, CH, Langeveld, SC, Groot-van Ruijven, CM, Debets, R, Sleijfer, S and Gratama, JW (2007). Gene-modified T cells for adoptive immunotherapy of renal cell cancer maintain transgene-specific immune functions in vivo. Cancer Immunol Immunother 56: 1875-1883. (Pubitemid 47512609)
33. Lamers, CH, Willemsen, R, van Elzakker, P, van Steenbergen-Langeveld, S, Broertjes, M, Oosterwijk-Wakka, J et al. (2011). Immune responses to transgene and retroviral vector in patients treated with ex vivo-engineered T cells. Blood 117: 72-82.
34. Parkhurst, MR, Yang, JC, Langan, RC, Dudley, ME, Nathan, DA, Feldman, SA et al. (2011). T cells targeting carcinoembryonic antigen can mediate regression of metastatic colorectal cancer but induce severe transient colitis. Mol Ther 19: 620-626.
35. Feldhaus, MJ, Siegel, RW, Opresko, LK, Coleman, JR, Feldhaus, JM, Yeung, YA et al. (2003). Flow-cytometric isolation of human antibodies from a nonimmune Saccharomyces cerevisiae surface display library. Nat Biotechnol 21: 163-170. (Pubitemid 36188215)
36. Nolan, KF, Yun, CO, Akamatsu, Y, Murphy, JC, Leung, SO, Beecham, EJ et al. (1999). Bypassing immunization: optimized design of "designer T cells" against carcinoembryonic antigen (CEA)-expressing tumors, and lack of suppression by soluble CEA. Clin Cancer Res 5: 3928-3941. (Pubitemid 30013767)
37. Hombach, A, Heuser, C, Sircar, R, Tillmann, T, Diehl, V, Pohl, C et al. (1998). An anti-CD30 chimeric receptor that mediates CD3-zeta-independent T-cell activation against Hodgkin's lymphoma cells in the presence of soluble CD30. Cancer Res 58: 1116-1119. (Pubitemid 28183194)
38. Westwood, JA, Murray, WK, Trivett, M, Haynes, NM, Solomon, B, Mileshkin, L et al. (2009). The Lewis-Y carbohydrate antigen is expressed by many human tumors and can serve as a target for genetically redirected T cells despite the presence of soluble antigen in serum. J Immunother 32: 292-301.
39. Turatti, F, Figini, M, Alberti, P, Willemsen, RA, Canevari, S and Mezzanzanica, D (2005). Highly efficient redirected anti-tumor activity of human lymphocytes transduced with a completely human chimeric immune receptor. J Gene Med 7: 158-170. (Pubitemid 40348020)
40. Carpenito, C, Milone, MC, Hassan, R, Simonet, JC, Lakhal, M, Suhoski, MM et al. (2009). Control of large, established tumor xenografts with genetically retargeted human T cells containing CD28 and CD137 domains. Proc Natl Acad Sci USA 106: 3360-3365.
41. Song, D, Ye, Q, Carpenito, C, Poussin, M, Wang, LP, Ji, C et al. (2011). Improved T cell survival provided by CD137 costimulatory signaling to folate receptor-redirected T cells results in tumor localization and eradication. Cancer Res 71: 4617-4627.
42. Scholler, N, Garvik, B, Quarles, T, Jiang, S and Urban, N (2006). Method for generation of in vivo biotinylated recombinant antibodies by yeast mating. J Immunol Methods 317: 132-143. (Pubitemid 44816326)
43. Levine, BL, Bernstein, WB, Connors, M, Craighead, N, Lindsten, T, Thompson, CB et al. (1997). Effects of CD28 costimulation on long-term proliferation of CD4+ T cells in the absence of exogenous feeder cells. J Immunol 159: 5921-5930. (Pubitemid 127471527)
44. Johnson, LA, Heemskerk, B, Powell, DJ Jr, Cohen, CJ, Morgan, RA, Dudley, ME et al. (2006). Gene transfer of tumor-reactive TCR confers both high avidity and tumor reactivity to nonreactive peripheral blood mononuclear cells and tumor-infiltrating lymphocytes. J Immunol 177: 6548-6559. (Pubitemid 44628874)