T lymphocytes redirected against the chondroitin sulfate proteoglycan-4 control the growth of multiple solid tumors both in vitro and in vivo

Clinical Cancer Research

Volumn 20, Issue 4, 2014, Pages 962-971

  Geldres, Claudia ^a,e   Savoldo, Barbara ^a,b   Hoyos, Valentina ^a   Caruana, Ignazio ^a   Zhang, Ming ^a   Yvon, Eric ^a   Del Vecchio, Michele ^a   Creighton, Chad J ^e   Ittmann, Michael ^c,e,h   Ferrone, Soldano ^g,i   Dotti, Gianpietro ^a,c,d,e,f  

^a CENTER FOR CELL AND GENE THERAPY   (United States)

^b Departments of Pediatrics   (United States)

^c Departments of Immunology Pathology   (United States)

^d Departments of Internal Medicine   (United States)

^e BAYLOR COLLEGE OF MEDICINE   (United States)

^f TEXAS CHILDREN S HOSPITAL   (United States)

^g Vascular Neurology Program   (United States)

^h MICHAEL E DEBAKEY VETERANS AFFAIRS MEDICAL CENTER   (United States)

ⁱ MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD28 ANTIGEN; CHIMERIC ANTIGEN RECEPTOR; CHIMERIC PROTEIN; CHONDROITIN SULFATE PROTEOGLYCAN 4; PROTEOCHONDROITIN SULFATE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST CARCINOMA; CANCER CONTROL; CANCER GROWTH; CANCER IMMUNOTHERAPY; CANCER INHIBITION; CLEAR CELL CARCINOMA; COMPUTER MODEL; CONTROLLED STUDY; CSPG4 GENE; DNA MODIFICATION; GENE EXPRESSION PROFILING; GENETIC CODE; GLIOBLASTOMA; HEAD AND NECK CARCINOMA; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; KIDNEY CARCINOMA; MELANOMA; MESOTHELIOMA; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; SARCOMA; SQUAMOUS CELL CARCINOMA; T LYMPHOCYTE;

ADOPTIVE TRANSFER; ANIMALS; BREAST NEOPLASMS; CARCINOMA, DUCTAL, BREAST; CARCINOMA, SQUAMOUS CELL; CHONDROITIN SULFATE PROTEOGLYCANS; COCULTURE TECHNIQUES; CYTOTOXICITY, IMMUNOLOGIC; HEAD AND NECK NEOPLASMS; HUMANS; MELANOMA; MEMBRANE PROTEINS; MESOTHELIOMA; MICE; MICE, SCID; NEOPLASM TRANSPLANTATION; NEUROBLASTOMA; RECEPTORS, ANTIGEN; T-LYMPHOCYTES;

EID: 84896721190     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-13-2218     Document Type: Article

References (37)

1. Pluschke G, Vanek M, Evans A, Dittmar T, Schmid P, Itin P, et al. Molecular cloning of a human melanoma-associated chondroitin sulfate proteoglycan. Proc Natl Acad Sci U S A 1996;93:9710-5.
2. Rivera Z, Ferrone S, Wang X, Jube S, Yang H, Pass HI, et al. CSPG4 as a target of antibody-based immunotherapy for malignant mesothelioma. Clin Cancer Res 2012;18:5352-63.
3. Wang X, Wang Y, Yu L, Sakakura K, Visus C, Schwab JH, et al. CSPG4 in cancer: multiple roles. Curr Mol Med 2010;10:419-29.
4. Campoli MR, Chang CC, Kageshita T, Wang X, McCarthy JB, Ferrone S. Human high molecular weight-melanoma-associated antigen (HMW-MAA): a melanoma cell surface chondroitin sulfate proteoglycan (MSCP) with biological and clinical significance. Crit Rev Immunol 2004;24:267-96.
5. Iida J, Wilhelmson KL, Ng J, Lee P, Morrison C, Tam E, et al. Cell surface chondroitin sulfate glycosaminoglycan in melanoma: role in the activation of pro-MMP-2 (pro-gelatinase A). Biochem J 2007;403: 553-63.
6. Yang J, Price MA, Neudauer CL, Wilson C, Ferrone S, Xia H, et al. Melanoma chondroitin sulfate proteoglycan enhances FAK and ERK activation by distinct mechanisms. J Cell Biol 2004;165:881-91.
7. Hafner C, Breiteneder H, Ferrone S, Thallinger C, Wagner S, Schmidt WM, et al. Suppression of human melanoma tumor growth in SCID mice by a human high molecular weight-melanoma associated antigen (HMW-MAA) specific monoclonal antibody. Int J Cancer 2005;114: 426-32.
8. Dotti G, Savoldo B, Brenner M. Fifteen years of gene therapy based on chimeric antigen receptors: "are we nearly there yet?". Hum Gene Ther 2009;20:1229-39.
9. Eshhar Z, Waks T, Gross G, Schindler DG. Specific activation and targeting of cytotoxic lymphocytes through chimeric single chains consisting of antibody-binding domains and the gamma or zeta subunits of the immunoglobulin and T-cell receptors. Proc Natl Acad Sci U S A 1993;90:720-4.
10. Sadelain M, Brentjens R, Riviere I. The promise and potential pitfalls of chimeric antigen receptors. Curr Opin Immunol 2009;21: 215-23.
11. Maher J, Brentjens RJ, Gunset G, Riviere I, Sadelain M. Human Tlymphocyte cytotoxicity and proliferation directed by a single chimeric TCRz/CD28 receptor. Nat Biotechnol 2002;20:70-5.
12. Imai C, Mihara K, Andreansky M, Nicholson IC, Pui CH, Geiger TL, et al. Chimeric receptors with 4-1BB signaling capacity provoke potent cytotoxicity against acute lymphoblastic leukemia. Leukemia 2004;18: 676-84.
13. Savoldo B, Ramos CA, Liu E, Mims MP, Keating MJ, Carrum G, et al. CD28 costimulation improves expansion and persistence of chimeric antigen receptor-modified T cells in lymphoma patients. J Clin Invest 2011;121:1822-6.
14. 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.
15. Kochenderfer JN, Wilson WH, Janik JE, Dudley ME, Stetler-Stevenson M, Feldman SA, et al. Eradication of B-lineage cells and regression of lymphoma in a patient treated with autologous T cells genetically engineered to recognize CD19. Blood 2010;116:4099-102.
16. 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.
17. Burns WR, Zhao Y, Frankel TL, Hinrichs CS, Zheng Z, Xu H, et al. A high molecular weight melanoma-associated antigen-specific chimeric antigen receptor redirects lymphocytes to target human melanomas. Cancer Res 2010;70:3027-33.
18. Yvon E, Del VM, Savoldo B, Hoyos V, Dutour A, Anichini A, et al. Immunotherapy of metastatic melanoma using genetically engineered GD2-specific T cells. Clin Cancer Res 2009;15:5852-60.
19. Yu W, Feng S, Dakhova O, Creighton CJ, Cai Y, Wang J, et al. FGFR-4 Arg(3)(8)(8) enhances prostate cancer progression via extracellular signal-related kinase and serum response factor signaling. Clin Cancer Res 2011;17:4355-66.
20. Temponi M, Gold AM, Ferrone S. Binding parameters and idiotypic profile of the whole immunoglobulin and Fab' fragments of murine monoclonal antibody to distinct determinants of the human high molecular weight-melanoma associated antigen. Cancer Res 1992; 52:2497-503.
21. Reinhold U, Liu L, Ludtke-Handjery HC, Heuser C, Hombach A, Wang X, et al. Specific lysis of melanoma cells by receptor grafted T cells is enhanced by anti-idiotypic monoclonal antibodies directed to the scFv domain of the receptor. J Invest Dermatol 1999;112:744-50.
22. Pule MA, Straathof KC, Dotti G, Heslop HE, RooneyCM, BrennerMK.A chimeric T cell antigen receptor that augments cytokine release and supports clonal expansion of primary human T cells.Mol Ther 2005;12: 933-41.
23. Vera J, Savoldo B, Vigouroux S, Biagi E, Pule M, Rossig C, et al. T lymphocytes redirected against the kappa light chain of human immunoglobulin efficiently kill matureBlymphocyte-derived malignant cells. Blood 2006;108:3890-7.
24. Shu L, Qi CF, Schlom J, Kashmiri SV. Secretion of a single-geneencoded immunoglobulin from myeloma cells. Proc Natl Acad Sci U S A 1993;90:7995-9.
25. Glouchkova L, Ackermann B, Zibert A, Meisel R, Siepermann M, Janka-Schaub GE, et al. The CD70/CD27 pathway is critical for stimulation of an effective cytotoxic T cell response against B cell precursor acute lymphoblastic leukemia. J Immunol 2009;182:718-25.
26. Rickman DS, Bobek MP, Misek DE, Kuick R, Blaivas M, Kurnit DM, et al. Distinctive molecular profiles of high-grade and low-grade gliomas based on oligonucleotide microarray analysis. Cancer Res 2001;61:6885-91.
27. Talantov D, Mazumder A, Yu JX, Briggs T, Jiang Y, Backus J, et al. Novel genes associated with malignant melanoma but not benign melanocytic lesions. Clin Cancer Res 2005;11:7234-42.
28. Chekenya M, Krakstad C, Svendsen A, Netland IA, Staalesen V, Tysnes BB, et al. The progenitor cell marker NG2/MPG promotes chemoresistance by activation of integrin-dependent PI3K/Akt signaling. Oncogene 2008;27:5182-94.
29. Hoyos V, Savoldo B, Quintarelli C, Mahendravada A, Zhang M, Vera J, et al. Engineering CD19-specific T lymphocytes with interleukin-15 and a suicide gene to enhance their anti-lymphoma/leukemia effects and safety. Leukemia 2010;24:1160-70.
30. Kowolik CM, Topp MS, Gonzalez S, Pfeiffer T, Olivares S, Gonzalez N, et al. CD28 costimulation provided through a CD19-specific chimeric antigen receptor enhances in vivo persistence and antitumor efficacy of adoptively transferred T cells. Cancer Res 2006;66:10995-1004.
31. Haynes NM, Snook MB, Trapani JA, Cerruti L, Jane SM, Smyth MJ, et al. Redirecting mouse CTL against colon carcinoma: superior signaling efficacy of single-chain variable domain chimeras containing TCR-z vs Fc epsilon RI-g. J Immunol 2001;166:182-7.
32. Heuser C, Hombach A, Losch C, Manista K, Abken H. T-cell activation by recombinant immunoreceptors: impact of the intracellular signalling domain on the stability of receptor expression and antigen-specific activation of grafted T cells. Gene Ther 2003;10:1408-19.
33. Hudecek M, Lupo-Stanghellini MT, Kosasih PL, Sommermeyer D, Jensen MC, Rader C, et al. Receptor affinity and extracellular domain modifications affect tumor recognition by ROR1-specific chimeric antigen receptor T cells. Clin Cancer Res 2013;19:3153-64.
34. Ahmed N, Salsman VS, Yvon E, Louis CU, Perlaky L, Wels WS, et al. Immunotherapy for osteosarcoma: genetic modification of T cells overcomes low levels of tumor antigen expression. Mol Ther 2009; 17:1779-87.
35. Lamers CH, Sleijfer S, Vulto AG, Kruit WH, Kliffen M, Debets R, et al. Treatment of metastatic renal cell carcinoma with autologous T-lymphocytes genetically retargeted against carbonic anhydrase IX: first clinical experience. J Clin Oncol 2006;24:e20-e22.
36. Morgan RA, Yang JC, Kitano M, Dudley ME, LaurencotCM, Rosenberg SA. Case report of a serious adverse event following the administration of T cells transduced with a chimeric antigen receptor recognizing ERBB2. Mol Ther 2010;18:843-51.
37. Di Stasi A, Tey SK, Dotti G, Fujita Y, Kennedy-Nasser A, Martinez C, et al. Inducible apoptosis as a safety switch for adoptive cell therapy.N Engl J Med 2011;365:1673-83.