Specificity redirection by CAR with human VEGFR-1 affinity endows T lymphocytes with tumor-killing ability and anti-angiogenic potency

Gene Therapy

Volumn 20, Issue 10, 2013, Pages 970-978

  Wang, W ^a   Ma, Y ^a   Li, J ^a   Shi, H S ^a   Wang, L Q ^a   Guo, F C ^a   Zhang, J ^a   Li, D ^a   Mo, B H ^a   Wen, F ^a   Liu, T ^a   Liu, Y T ^a   Wang, Y S ^a   Wei, Y Q ^a  

^a SICHUAN UNIVERSITY   (China)

Author keywords

anti angiogenesis; chimeric antigen receptor; T lymphocytes; VEGFR 1

Indexed keywords

CHIMERIC ANTIGEN RECEPTOR; INTERLEUKIN 15; LYMPHOCYTE ANTIGEN RECEPTOR; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR 1;

ADOPTIVE IMMUNOTHERAPY; ADOPTIVE TRANSFER; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ANTIGEN RECOGNITION; ANTIGEN SPECIFICITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER IMMUNOTHERAPY; CANCER INHIBITION; CONTROLLED STUDY; CYTOLYSIS; CYTOPATHOGENIC EFFECT; ELECTROPORATION; ENDOTHELIUM CELL; GENETIC ENGINEERING; HUMAN; HUMAN CELL; METASTASIS INHIBITION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR AFFINITY; T LYMPHOCYTE; TUMOR CELL DESTRUCTION; TUMOR XENOGRAFT;

ANIMALS; ANTIGENS, NEOPLASM; CELL DEATH; CELLS, CULTURED; CYTOTOXICITY, IMMUNOLOGIC; ELECTROPORATION; GENETIC THERAPY; HELA CELLS; HUMANS; IMMUNOTHERAPY, ADOPTIVE; MICE; MICE, SCID; NEOPLASMS, EXPERIMENTAL; RECEPTORS, ANTIGEN, T-CELL; RECOMBINANT FUSION PROTEINS; T-CELL ANTIGEN RECEPTOR SPECIFICITY; T-LYMPHOCYTES; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84885636151     PISSN: 09697128     EISSN: 14765462     Source Type: Journal    
DOI: 10.1038/gt.2013.19     Document Type: Article

References (50)

1. Rosenberg SA, Restifo NP, Yang JC, Morgan RA, Dudley ME. Adoptive cell transfer: a clinical path to effective cancer immunotherapy. Nat Rev Cancer 2008; 8: 299-308.
2. Sadelain M, Brentjens R, Riviere I. The promise and potential pitfalls of chimeric antigen receptors. Curr Opin Immunol 2009; 21: 215-223.
3. Till BG, Jensen MC, Wang JJ, Chen EY, Wood BL, Greisman HA et al. Adoptive immunotherapy for indolent non-Hodgkin lymphoma and mantle cell lymphoma using genetically modified autologous CD20-specific T cells. Blood 2008; 112: 2261-2271.
4. Haynes NM, Trapani JA, Teng MWL, Jackson JT, Cerruti L, Jane SM et al. Rejection of syngeneic colon carcinoma by CTLs expressing single-chain antibody receptors codelivering CD28 costimulation. Journal of Immunology 2002; 169: 5780-5786.
5. Zhao Y, Wang QJ, Yang S, Kochenderfer JN, Zheng Z, Zhong X et al. A herceptinbased chimeric antigen receptor with modified signaling domains leads to enhanced survival of transduced T lymphocytes and antitumor activity. J Immunol 2009; 183: 5563-5574.
6. 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: 95ra73-95ra73.
7. Porter DL, Levine BL, Kalos M, Bagg A, June CH. Chimeric antigen receptormodified T cells in chronic lymphoid leukemia. N Engl J Med 2011; 365: 725-733.
8. 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: 4099-4102.
9. 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: 3953-3968.
10. Shibuya M. Vascular endothelial growth factor receptor-1 (VEGFR-1/Flt-1): a dual regulator for angiogenesis. Angiogenesis 2006; 9: 225-230.
11. Fong GH, Rossant J, Gertsenstein M, Breitman ML. Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature 1995; 376: 66-70.
12. Hiratsuka S, Minowa O, Kuno J, Noda T, Shibuya M. Flt-1 lacking the tyrosine kinase domain is sufficient for normal development and angiogenesis in mice. Proc Natl Acad Sci USA 1998; 95: 9349-9354.
13. Wu Y, Zhong Z, Huber J, Bassi R, Finnerty B, Corcoran E et al. Anti-vascular endothelial growth factor receptor-1 antagonist antibody as a therapeutic agent for cancer. Clin Cancer Res 2006; 12: 6573-6584.
14. Decaussin M, Sartelet H, Robert C, Moro D, Claraz C, Brambilla C et al. Expression of vascular endothelial growth factor (VEGF) and its two receptors (VEGF-R1-Flt1 and VEGF-R2-Flk1/KDR) in non-small cell lung carcinomas (NSCLCs): correlation with angiogenesis and survival. J Pathol 1999; 188: 369-377.
15. El-Obeid A, Sunnuqrut N, Hussain A, Al-Hussein K, Gutierrez MI, Bhatia K. Immature B cell malignancies synthesize VEGF, VEGFR-1 (Flt-1) and VEGFR-2 (KDR). Leuk Res 2004; 28: 133-137.
16. Morelli MP, Brown AM, Pitts TM, Tentler JJ, Ciardiello F, Ryan A et al. Targeting vascular endothelial growth factor receptor-1 and -3 with cediranib (AZD2171): effects on migration and invasion of gastrointestinal cancer cell lines. Mol Cancer Ther 2009; 8: 2546-2558.
17. Yao J, Wu X, Zhuang G, Kasman IM, Vogt T, Phan V et al. Expression of a functional VEGFR-1 in tumor cells is a major determinant of anti-PlGF antibodies efficacy. Proc Natl Acad Sci USA 2011; 108: 11590-11595.
18. Hiratsuka S, Nakamura K, Iwai S, Murakami M, Itoh T, Kijima H et al. MMP9 induction by vascular endothelial growth factor receptor-1 is involved in lungspecific metastasis. Cancer Cell 2002; 2: 289-300.
19. Schwartz JD, Rowinsky EK, Youssoufian H, Pytowski B, Wu Y. Vascular endothelial growth factor receptor-1 in human cancer: concise review and rationale for development of IMC-18F1 (Human antibody targeting vascular endothelial growth factor receptor-1). Cancer 2010; 116(4 Suppl): 1027-1032.
20. 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-zeta vs Fc epsilon RI-gamma. J Immunol 2001; 166: 182-187.
21. Yoon SH, Lee JM, Cho HI, Kim EK, Kim HS, Park MY et al. Adoptive immunotherapy using human peripheral blood lymphocytes transferred with RNA encoding Her-2/neu-specific chimeric immune receptor in ovarian cancer xenograft model. Cancer Gene Ther 2009; 16: 489-497.
22. Zhao Y, Moon E, Carpenito C, Paulos CM, Liu X, Brennan AL et al. Multiple injections of electroporated autologous T cells expressing a chimeric antigen receptor mediate regression of human disseminated tumor. Cancer Res 2010; 70: 9053-9061.
23. Gresch O, Engel FB, Nesic D, Tran TT, England HM, Hickman ES et al. New non-viral method for gene transfer into primary cells. Methods 2004; 33: 151-163.
24. Martinet W, Schrijvers DM, Kockx MM. Nucleofection as an efficient nonviral transfection method for human monocytic cells. Biotechnol Lett 2003; 25: 1025-1029.
25. Budagian V, Bulanova E, Paus R, Bulfone-Paus S. IL-15/IL-15 receptor biology: a guided tour through an expanding universe. Cytokine Growth Factor Rev 2006; 17: 259-280.
26. Hsu C, Hughes MS, Zheng Z, Bray RB, Rosenberg SA, Morgan RA. Primary human T lymphocytes engineered with a codon-optimized IL-15 gene resist cytokine withdrawal-induced apoptosis and persist long-term in the absence of exogenous cytokine. J Immunol 2005; 175: 7226-7234.
27. Markley JC, Sadelain M. IL-7 and IL-21 are superior to IL-2 and IL-15 in promoting human T cell-mediated rejection of systemic lymphoma in immunodeficient mice. Blood 2010; 115: 3508-3519.
28. Gattinoni L, Finkelstein SE, Klebanoff CA, Antony PA, Palmer DC, Spiess PJ et al. Removal of homeostatic cytokine sinks by lymphodepletion enhances the efficacy of adoptively transferred tumor-specific CD8 T cells. J Exp Med 2005; 202: 907-912.
29. Teague RM, Sather BD, Sacks JA, Huang MZ, Dossett ML, Morimoto J et al. Interleukin-15 rescues tolerant CD8 T cells for use in adoptive immunotherapy of established tumors. Nat Med 2006; 12: 335-341.
30. Schluns KS, Lefrancois L. Cytokine control of memory T-cell development and survival. Nat Rev Immunol 2003; 3: 269-279.
31. Folkman J. Tumor angiogenesis: therapeutic implications. N Engl J Med 1971; 285: 1182-1186.
32. Sitohy B, Nagy JA, Dvorak HF. Anti-VEGF/VEGFR therapy for cancer: reassessing the target. Cancer Res 2012; 72: 1909-1914.
33. Casanovas O, Hicklin DJ, Bergers G, Hanahan D. Drug resistance by evasion of antiangiogenic targeting of VEGF signaling in late-stage pancreatic islet tumors. Cancer Cell 2005; 8: 299-309.
34. Grepin R, Pages G. Molecular mechanisms of resistance to tumour anti-angiogenic strategies. J Oncol 2010; 2010: 835680.
35. Ellis LM, Hicklin DJ. Pathways mediating resistance to vascular endothelial growth factor-targeted therapy. Clin Cancer Res 2008; 14: 6371-6375.
36. Kadenhe-Chiweshe A, Papa J, McCrudden KW, Frischer J, Bae JO, Huang J et al. Sustained VEGF blockade results in microenvironmental sequestration of VEGF by tumors and persistent VEGF receptor-2 activation. Mol Cancer Res 2008; 6: 1-9.
37. Paez-Ribes M, Allen E, Hudock J, Takeda T, Okuyama H, Vinals F et al. Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell 2009; 15: 220-231.
38. Ebos JM, Lee CR, Cruz-Munoz W, Bjarnason GA, Christensen JG, Kerbel RS. Accelerated metastasis after short-term treatment with a potent inhibitor of tumor angiogenesis. Cancer Cell 2009; 15: 232-239.
39. Wang J, Jensen M, Lin Y, Sui X, Chen E, Lindgren CG et al. Optimizing adoptive polyclonal T cell immunotherapy of lymphomas, using a chimeric T cell receptor possessing CD28 and CD137 costimulatory domains. Hum Gene Ther 2007; 18: 712-725.
40. Hombach AA, Abken H. Costimulation by chimeric antigen receptors revisited the T cell antitumor response benefits from combined CD28-OX40 signalling. Int J Cancer 2011; 129: 2935-2944.
41. Pule MA, Straathof KC, Dotti G, Heslop HE, Rooney CM, Brenner MK. A chimeric T cell antigen receptor that augments cytokine release and supports clonal expansion of primary human T cells. Mol Ther 2005; 12: 933-941.
42. Morgan RA, Yang JC, Kitano M, Dudley ME, Laurencot CM, 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: 843-851.
43. Brentjens R, Yeh R, Bernal Y, Riviere I, Sadelain M. Treatment of chronic lymphocytic leukemia with genetically targeted autologous T cells: case report of an unforeseen adverse event in a phase I clinical trial. Mol Ther 2010; 18: 666-668.
44. Morgan RA, Dudley ME, Wunderlich JR, Hughes MS, Yang JC, Sherry RM et al. Cancer regression in patients after transfer of genetically engineered lymphocytes. Science 2006; 314: 126-129.
45. Dudley ME, Yang JC, Sherry R, Hughes MS, Royal R, Kammula U et al. Adoptive cell therapy for patients with metastatic melanoma: evaluation of intensive myeloablative chemoradiation preparative regimens. J Clin Oncol 2008; 26: 5233-5239.
46. Hacein-Bey-Abina S, Von Kalle C, Schmidt M, McCormack MP, Wulffraat N, Leboulch P et al. LMO2-associated clonal T cell proliferation in two patients after gene therapy for SCID-X1. Science 2003; 302: 415-419.
47. Singh H, Figliola MJ, Dawson MJ, Huls H, Olivares S, Switzer K et al. Reprogramming CD19-specific T cells with IL-21 signaling can improve adoptive immunotherapy of B-lineage malignancies. Cancer Res 2011; 71: 3516-3527.
48. Pan Y, Xu Y, Feng S, Luo S, Zheng R, Yang J et al. SKLB1206, a novel orally available multikinase inhibitor targeting EGFR activating and T790M mutants, ErbB2, ErbB4, and VEGFR2, displays potent antitumor activity both in vitro and in vivo. Mol Cancer Ther 2012; 11: 952-962.
49. Serrano LM, Pfeiffer T, Olivares S, Numbenjapon T, Bennitt J, Kim D et al. Differentiation of naive cord-blood T cells into CD19-specific cytolytic effectors for posttransplantation adoptive immunotherapy. Blood 2006; 107: 2643-2652.
50. Facciabene A, Peng X, Hagemann IS, Balint K, Barchetti A, Wang LP et al. Tumour hypoxia promotes tolerance and angiogenesis via CCL28 and T(reg) cells. Nature 2011; 475: 226-230.