T cells bearing a chimeric antigen receptor against prostate-specific membrane antigen mediate vascular disruption and result in tumor regression

Cancer Immunology Research

Volumn 3, Issue 1, 2015, Pages 68-84

  Santoro, Stephen P ^a   Kim, Soorin ^a   Motz, Gregory T ^a   Alatzoglou, Dimitrios ^a   Li, Chunsheng ^a   Irving, Melita ^b   Powell, Daniel J ^a   Coukos, George ^a,b,c  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

^c LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CHIMERIC ANTIGEN RECEPTOR; MONOCLONAL ANTIBODY J591; PROSTATE SPECIFIC ANTIGEN; GLUTAMATE CARBOXYPEPTIDASE II; GLUTAMATE CARBOXYPEPTIDASE II, HUMAN; LYMPHOCYTE ANTIGEN RECEPTOR; MEMBRANE ANTIGEN; SINGLE CHAIN FRAGMENT VARIABLE ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL THERAPY; CONTROLLED STUDY; ENDOTHELIUM CELL; FEMALE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SIGNALING; METASTASIS; MOUSE; NONHUMAN; OVARY CANCER; PROTEIN EXPRESSION; SOLID TUMOR; T LYMPHOCYTE; TUMOR REGRESSION; TUMOR VASCULARIZATION; VASCULAR TUMOR; ANIMAL; CELL LINE; DISEASE MODEL; GENETIC TRANSDUCTION; IMMUNOLOGY; NONOBESE DIABETIC MOUSE; OVARY TUMOR; PATHOLOGY; SIGNAL TRANSDUCTION; TUMOR VOLUME; VASCULAR NEOPLASMS;

ANIMALS; ANTIGENS, SURFACE; CELL LINE; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; FEMALE; GLUTAMATE CARBOXYPEPTIDASE II; HUMANS; MICE; MICE, INBRED NOD; OVARIAN NEOPLASMS; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; SINGLE-CHAIN ANTIBODIES; TRANSDUCTION, GENETIC; TUMOR BURDEN; VASCULAR NEOPLASMS;

EID: 84962247223     PISSN: 23266066     EISSN: 23266074     Source Type: Journal    
DOI: 10.1158/2326-6066.CIR-14-0192     Document Type: Article

References (52)

1. Bergers G, Benjamin LE. Tumorigenesisand the angiogenicswitch. Nat Rev Cancer 2003;3:401-10.
2. Neiva KG, Warner KA, Campos MS, Zhang Z, Moren J, Danciu TE, et al. Endothelial cell-derived interleukin-6 regulates tumor growth. BMC Cancer 2014;14:99.
3. Lu J, Ye X, Fan F, Xia L, Bhattacharya R, Bellister S, et al. Endothelial cells promote the colorectal cancer stem cell phenotype through a soluble form of Jagged-1. Cancer Cell 2013;23:171-85.
4. Buckanovich RJ, Facciabene A, Kim S, Benencia F, Sasaroli D, Balint K, et al. Endothelin B receptor mediates the endothelial barrier to T cell homing to tumors and disables immune therapy. Nat Med 2008;14:28-36.
5. Motz GT, Santoro SP, Wang LP, Garrabrant T, Lastra RR, Hagemann IS, et al. Tumor endotheliumFasLestablishesaselective immunebarrier promoting tolerance in tumors. Nat Med 2014;20:607-15.
6. Dotti G, Gottschalk S, Savoldo B, Brenner MK. Design and development of therapies using chimeric antigen receptor-expressing T cells. Immunol Rev 2014;257:107-26.
7. Smith NR, Baker D, James NH, Ratcliffe K, Jenkins M, Ashton SE, et al. Vascular endothelial growth factor receptors VEGFR-2 and VEGFR-3 are localized primarily to the vasculature in human primary solid cancers. Clin Cancer Res 2010;16:3548-61.
8. Chinnasamy D, Yu Z, Theoret MR, Zhao Y, Shrimali RK, Morgan RA, et al. Gene therapy using genetically modified lymphocytes targeting VEGFR-2 inhibits the growth of vascularized syngenic tumors in mice. J Clin Invest 2010;120:3953-68.
9. Niederman TM, Ghogawala Z, Carter BS, Tompkins HS, Russell MM, Mulligan RC. Antitumor activity of cytotoxic T lymphocytes engineered to target vascular endothelial growth factor receptors. Proc Natl Acad Sci U S A 2002;99:7009-14.
10. Chang SS, O'Keefe DS, Bacich DJ, Reuter VE, Heston WD, Gaudin PB. Prostate-specific membrane antigen is produced in tumor-associated neovasculature. Clin Cancer Res 1999;5:2674-81.
11. Chang SS, Reuter VE, Heston WD, Bander NH, Grauer LS, Gaudin PB. Five different anti-prostate-specific membrane antigen (PSMA) antibodies confirm PSMA expression in tumor-associated neovasculature. Cancer Res 1999;59:3192-8.
12. Cao KY, Mao XP, Wang DH, Xu L, Yuan GQ, Dai SQ, et al. High expression of PSM-E correlated with tumor grade in prostate cancer: a new alternatively spliced variant of prostate-specific membrane antigen. Prostate 2007;67:1791-800.
13. Schmittgen TD, Teske S, Vessella RL, True LD, Zakrajsek BA. Expression of prostate specific membrane antigen and three alternatively spliced variants of PSMA in prostate cancer patients. Int J Cancer 2003;107: 323-9.
14. Su SL, Huang IP, Fair WR, Powell CT, Heston WD. Alternatively spliced variants of prostate-specific membrane antigen RNA: ratio of expression as a potential measurement of progression. Cancer Res 1995;55:1441-3.
15. Yao V, Berkman CE, Choi JK, O'Keefe DS, Bacich DJ. Expressionofprostate-specific membrane antigen (PSMA), increases cell folate uptake and proliferation and suggests a novel role for PSMA in the uptake of the non-polyglutamated folate, folic acid. Prostate 2010;70:305-16.
16. Conway RE, Petrovic N, Li Z, Heston W, Wu D, Shapiro LH. Prostate-specific membrane antigen regulates angiogenesis by modulating integrin signal transduction. Mol Cell Biol 2006;26:5310-24.
17. Colombatti M, Grasso S, Porzia A, Fracasso G, Scupoli MT, Cingarlini S, et al. The prostate specific membrane antigen regulates the expression of IL-6 and CCL5 in prostate tumour cells by activating the MAPK pathways. PLoS One 2009;4:e4608.
18. Zhong XS, Matsushita M, Plotkin J, Riviere I, Sadelain M. Chimeric antigen receptors combining 4-1BB and CD28 signaling domains augment PI3ki-nase/AKT/Bcl-XL activation and CD8+ T cell-mediated tumor eradication. Mol Ther 2010;18:413-20.
19. Song DG, Ye Q, Carpenito C, Poussin M, Wang LP, Ji C, et al. In vivo persistence, tumor localization, and antitumor activity of CAR-engineered T cells is enhanced by costimulatory signaling through CD137 (4-1BB). Cancer Res 2011;71:4617-27.
20. Carpenito C, Milone MC, Hassan R, Simonet JC, Lakhal M, Suhoski MM, et al. Control of large, established tumor xenografts with genetically retargeted human T cells containing CD28 and CD137 domains. Proc Natl Acad Sci U S A 2009;106:3360-5.
21. Dull T, Zufferey R, Kelly M, Mandel RJ, Nguyen M, Trono D, et al. A third-generation lentivirus vector with a conditional packaging system. J Virol 1998;72:8463-71.
22. Lanitis E, Poussin M, Hagemann IS, Coukos G, Sandaltzopoulos R, Scholler N, et al. Redirected antitumor activity of primary human lymphocytes transduced with a fully human anti-mesothelin chimeric receptor. Mol Ther 2012;20:633-43.
23. Garlanda C, Parravicini C, Sironi M, De Rossi M, Wainstok de Calmanovici R, Carozzi F, et al. Progressive growth in immunodeficient mice and host cell recruitment by mouse endothelial cells transformed by polyoma middle-sized T antigen: implications for the pathogenesis of opportunistic vascular tumors. Proc Natl Acad Sci U S A 1994;91: 7291-5.
24. Ades EW, Candal FJ, Swerlick RA, George VG, Summers S, Bosse DC, et al. HMEC-1: establishment of an immortalized human microvascular endothelial cell line. J Invest Dermatol 1992;99:683-90.
25. Liu H, Moy P, Kim S, Xia Y, Rajasekaran A, Navarro V, et al. Monoclonal antibodies to the extracellular domain of prostate-specific membrane antigen also react with tumor vascular endothelium. Cancer Res 1997;57: 3629-34.
26. Denmeade SR, Mhaka AM, Rosen DM, Brennen WN, Dalrymple S, Dach I, et al. Engineering a prostate-specific membrane antigen-activated tumor endothelial cell prodrug for cancer therapy. Sci Transl Med 2012;4: 140ra86.
27. Kalli KR, Oberg AL, Keeney GL, Christianson TJ, Low PS, Knutson KL, et al. Folate receptor alpha as atumor targetinepithelial ovarian cancer. Gynecol Oncol 2008;108:619-26.
28. Markert S, Lassmann S, Gabriel B, Klar M, Werner M, Gitsch G, et al. Alpha-folate receptor expression in epithelial ovarian carcinoma and non-neoplastic ovarian tissue. Anticancer Res 2008;28:3567-72.
29. O'Shannessy DJ, Somers EB, Smale R, Fu YS. Expression of folate receptoralpha (FRA) in gynecologic malignancies and its relationship to the tumor type. Int J Gynecol Pathol 2013;32:258-68.
30. Mhawech-Fauceglia P, Zhang S, Terracciano L, Sauter G, Chadhuri A, Herrmann FR, et al. Prostate-specific membrane antigen (PSMA) protein expression in normal and neoplastic tissues and its sensitivity and specificity in prostate adenocarcinoma: an immunohistochemical study using mutiple tumour tissue microarray technique. Histopathology 2007;50: 472-83.
31. Arbiser JL, Moses MA, Fernandez CA, Ghiso N, Cao Y, Klauber N, et al. Oncogenic H-ras stimulates tumor angiogenesis by two distinct pathways. Proc Natl Acad Sci U S A 1997;94:861-6.
32. Thorpe PE. Vascular targeting agentsas cancer therapeutics. Clin Cancer Res 2004;10:415-27.
33. Lutz AM, Bachawal SV, Drescher CW, Pysz MA, Willmann JK, Gambhir SS. Ultrasound molecular imaging in a human CD276 expression-modulated murine ovarian cancer model. Clin Cancer Res 2014;20: 1313-22.
34. Chacko AM, Li C, Nayak M, Mikitsh JL, Hu J, Hou C, et al. Development of 124I immuno-PET targeting tumor vascular TEM1/endosialin. J Nuclear Med 2014;55:500-7.
35. Li C, Chacko AM, Hu J, Hasegawa K, Swails J, Grasso L, et al. Antibody-based tumor vascular theranostics targeting endosialin/TEM1 in a new mouse tumor vascular model. Cancer Biol Ther 2014;15:443-51.
36. Zhang L, Yang N, Garcia JR, Mohamed A, Benencia F, Rubin SC, et al. Generation of a syngeneic mouse model to study the effects of vascular endothelial growth factor in ovarian carcinoma. Am J Pathol 2002;161: 2295-309.
37. Moreno Garcia V, Basu B, Molife LR, Kaye SB. Combining antiangiogenics to overcome resistance: rationale and clinical experience. Clin Cancer Res 2012;18:3750-61.
38. Kalos M, Levine BL, Porter DL, Katz S, Grupp SA, Bagg A, et al. T cells with chimeric antigen receptors have potent antitumor effects and can establish memory in patients with advanced leukemia. Sci Transl Med 2011; 3:95ra73.
39. Brentjens RJ, Davila ML, Riviere I, Park J, Wang X, Cowell LG, et al. CD19-targeted T cells rapidly induce molecular remissions in adults with chemotherapy-refractory acute lymphoblastic leukemia. Sci Transl Med 2013;5:177ra38.
40. Porter DL, Levine BL, Kalos M, Bagg A, June CH. Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. N Engl J Med 2011;365: 725-33.
41. Louis CU, Savoldo B, Dotti G, Pule M, Yvon E, Myers GD, et al. Antitumor activity and long-term fate of chimeric antigen receptor-positive T cells in patients with neuroblastoma. Blood 2011;118:6050-6.
42. Beatty GL, Haas AR, Maus MV, Torigian DA, Soulen MC, Plesa G, 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.
43. Gilham DE, Debets R, Pule M, Hawkins RE, Abken H. CAR-T cells and solid tumors: tuning T cells to challenge an inveterate foe. Trends Mol Med 2012;18:377-84.
44. Kinoshita Y, Kuratsukuri K, Landas S, Imaida K, Rovito PM Jr, Wang CY, et al. Expression of prostate-specific membrane antigen in normal and malignant human tissues. World J Surg 2006;30:628-36.
45. Silver DA, Pellicer I, Fair WR, Heston WD, Cordon-Cardo C. Prostate-specific membrane antigen expression in normal and malignant human tissues. Clin Cancer Res 1997;3:81-5.
46. Bander NH, Trabulsi EJ, Kostakoglu L, Yao D, Vallabhajosula S, SmithJones P, et al. Targeting metastatic prostate cancer with radiolabeled monoclonal antibody J591 to the extracellular domain of prostate specific membrane antigen. J Urol 2003;170:1717-21.
47. Milowsky MI, Nanus DM, Kostakoglu L, Sheehan CE, Vallabhajosula S, Goldsmith SJ, et al. Vascular targeted therapy with anti-prostate-specific membrane antigen monoclonal antibody J591 in advanced solid tumors. J Clin Oncol 2007;25:540-7.
48. Sasaroli D, Gimotty PA, Pathak HB, Hammond R, Kougioumtzidou E, Katsaros D, et al. Novel surface targets and serum biomarkers from the ovarian cancer vasculature. Cancer Biol Ther 2011;12:169-80.
49. St Croix B, Rago C, Velculescu V, Traverso G, Romans KE, Montgomery E, et al. Genes expressed in human tumor endothelium. Science 2000;289: 1197-202.
50. Horsman MR, Siemann DW. Pathophysiologic effects of vascular-targeting agents and the implications for combination with conventional therapies. Cancer Res 2006;66:11520-39.
51. Siemann DW, Shi W. Dual targeting of tumor vasculature: combining Avastin and vascular disrupting agents (CA4PorOXi4503). Anticancer Res 2008;28:2027-31.
52. Chinnasamy D, Tran E, Yu Z, Morgan RA, Restifo NP, Rosenberg SA. Simultaneous targeting of tumor antigens and the tumor vasculature using T lymphocyte transfer synergize to induce regression of established tumors in mice. Cancer Res 2013;73:3371-80.