Anti-GD3 chimeric sFv-CD28/T-cell receptor ζ designer T cells for treatment of metastatic melanoma and other neuroectodermal tumors

Clinical Cancer Research

Volumn 16, Issue 10, 2010, Pages 2769-2780

  Lo, Agnes S Y ^b   Ma, Qiangzhong ^a,b   Liu, David L ^b   Junghans, Richard P ^a,b  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD28 ANTIGEN; CYTOKINE; GANGLIOSIDE GD3; IMMUNOGLOBULIN RECEPTOR; INTERLEUKIN 2; T LYMPHOCYTE RECEPTOR; T LYMPHOCYTE RECEPTOR ZETA; UNCLASSIFIED DRUG;

ADOPTIVE TRANSFER; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER IMMUNOTHERAPY; CANCER MODEL; CANCER REGRESSION; CELL KILLING; CELL PROLIFERATION; CHIMERA; CONTINUOUS INFUSION; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOTOXICITY; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; MAXIMUM TOLERATED DOSE; MELANOMA; MOUSE; NEUROECTODERM TUMOR; NONHUMAN; NUDE MOUSE; OSMOTIC PUMP; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; T LYMPHOCYTE; TREATMENT OUTCOME;

ANIMALS; ANTIGENS, CD28; BLOTTING, WESTERN; CELL LINE, TUMOR; CELL SEPARATION; CHIMERA; CYTOKINES; FEMALE; FLOW CYTOMETRY; GANGLIOSIDES; HUMANS; IMMUNOTHERAPY, ADOPTIVE; INTERLEUKIN-2; MELANOMA, EXPERIMENTAL; MICE; MICE, NUDE; NEUROECTODERMAL TUMORS; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTES; TRANSDUCTION, GENETIC; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 77952361779     PISSN: 10780432     EISSN: None     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-10-0043     Document Type: Article

References (55)

1. Gajewski TF. Failure at the effector phase: immune barriers at the level of the melanoma tumor microenvironment. Clin Cancer Res 2007;13:5256-5261
2. June C. Adoptive cellular therapies. In: Chabner BA, Longo DL, editors. Cancer chemotherapy and biotherapy: principles and practice. Philadelphia (PA): Lippincott; 2006, p. 718-738
3. Fish RG. Role of gangliosides in tumour progression: a molecular target for cancer therapy? Med Hypotheses 1996;46:140-144
4. Nakakuma H, Horikawa K, Kawaguchi T, et al. Common phenotypic expression of gangliosides GM3 and GD3 in normal human tissues and neoplastic skin lesions. Jpn J Clin Oncol 1992;22:308-312
5. Portoukalian J, David MJ, Shen X, Richard M, Dubreuil C. Tumor size-dependent elevations of serum gangliosides in patients with head and neck carcinomas. Biochem Int 1989;18:759-765 (Pubitemid 19135108)
6. Ravindranath MH, Tsuchida T, Morton DL, Irie RF. Ganglioside GM3: GD3 ratio as an index for the management of melanoma. Cancer 1991;67:3029-3035
7. Nasi ML, Meyers M, Livingston PO, Houghton AN, Chapman PB. Anti-melanoma effects of R24, a monoclonal antibody against GD3 ganglioside. Melanoma Res 1997;7 Suppl 2:S155-62.
8. Forero A, Shah J, Carlisle R, et al. A phase I study of an anti-GD3 monoclonal antibody, KW-2871, in patients with metastatic melanoma. Cancer Biother Radiopharm 2006;21:561-568 (Pubitemid 46175693)
9. Giaccone G, Debruyne C, Felip E, et al. Phase III study of adjuvant vaccination with Bec2/bacille Calmette-Guerin in responding patients with limited-disease small-cell lung cancer (European Organisation for Research and Treatment of Cancer 08971-08971B; Silva Study). J Clin Oncol 2005;23:6854-6864
10. Ravindranath MH, Morton DL. Role of gangliosides in active immunotherapy with melanoma vaccine. Int Rev Immunol 1991;7:303-329
11. Ma QZ, Gonzalo-Daganzo R, Junghans RP. Genetically engineered T cells as adoptive immunotherapy of cancer. In: Giaccone R, Schlinsky R, Sondel P, editors. Cancer chemotherapy and biological response modifiers, annual 20. Oxford: Elsevier Science; 2002, p. 319-345
12. Krause A, Guo HF, Latouche JB, Tan C, Cheung NK, Sadelain M. Antigen-dependent CD28 signaling selectively enhances survival and proliferation in genetically modified activated human primary T lymphocytes. J Exp Med 1998;188:619-626 (Pubitemid 28387925)
13. Pule MA, Savoldo B, Myers GD, et al. Virus-specific T cells engineered to coexpress tumor-specific receptors: persistence and antitumor activity in individuals with neuroblastoma. Nat Med 2008;14:1264-1270
14. Rossig C, Bollard CM, Nuchtern JG, Merchant DA, Brenner MK. Targeting of G(D2)-positive tumor cells by human T lymphocytes engineered to express chimeric T-cell receptor genes. Int J Cancer 2001;94:228-236
15. Yun CO, Nolan KF, Beecham EJ, Reisfeld RA, Junghans RP. Targeting of T lymphocytes to melanoma cells through chimeric anti-GD3 immunoglobulin T-cell receptors. Neoplasia 2000;2:449-459
16. Abken H, Hombach A, Heuser C, Kronfeld K, Seliger B. Tuning tumor-specific T-cell activation: a matter of costimulation? Trends Immunol 2002;23:240-245
17. Geiger TL, Nguyen P, Leitenberg D, Flavell RA. Integrated src kinase and costimulatory activity enhances signal transduction through single-chain chimeric receptors in T lymphocytes. Blood 2001;98:2364-2371
18. Maher J, Brentjens RJ, Gunset G, Riviere I, Sadelain M. Human T-lymphocyte cytotoxicity and proliferation directed by a single chimeric TCRζ/CD28 receptor. Nat Biotechnol 2002;20:70-75 (Pubitemid 34044918)
19. Pinthus JH, Waks T, Kaufman-Francis K, et al. Immuno-gene therapy of established prostate tumors using chimeric receptor-redirected human lymphocytes. Cancer Res 2003;63:2470-2476
20. Nolan KF, Yun CO, Akamatsu Y, et al. Bypassing immunization: optimized design of "designer T cells" against carcinoembryonic antigen (CEA)-expressing tumors, and lack of suppression by soluble CEA. Clin Cancer Res 1999;5:3928-3941
21. Cheresh DA, Honsik CJ, Staffileno LK, Jung G, Reisfeld RA. Disialoganglioside GD3 on human melanoma serves as a relevant target antigen for monoclonal antibody-mediated tumor cytolysis. Proc Natl Acad Sci U S A 1985;82:5155-5159
22. Beecham EJ, Ma Q, Ripley R, Junghans RP. Coupling CD28 co-stimulation to immunoglobulin T-cell receptor molecules: the dynamics of T-cell proliferation and death. J Immunother 2000;23:631-642
23. Emtage PC, Lo AS, Gomes EM, Liu DL, Gonzalo-Daganzo RM, Junghans RP. Second-generation anti-carcinoembryonic antigen designer T cells resist activation-induced cell death, proliferate on tumor contact, secrete cytokines, and exhibit superior antitumor activity in vivo: a preclinical evaluation. Clin Cancer Res 2008;14:8112-8122
24. Brezicka T, Bergman B, Olling S, Fredman P. Reactivity of monoclonal antibodies with ganglioside antigens in human small cell lung cancer tissues. Lung Cancer 2000;28:29-36. (Pubitemid 30125836)
25. Slingluff CL, Flaherty K, Rosenberg SA, Read PW. Cutaneous melanoma. In: DeVita VT, Hellman S, Rosenberg SA, editors. Cancer: principles and practice of oncology. Philadelphia (PA): Lippincott; 2008, p. 1897-1950
26. Kirkwood JM, Tarhini AA, Panelli MC, et al. Next generation of immunotherapy for melanoma. J Clin Oncol 2008;26:3445-3455
27. Houghton AN, Mintzer D, Cordon-Cardo C, et al. Mouse monoclonal IgG3 antibody detecting GD3 ganglioside: a phase I trial in patients with malignant melanoma. Proc Natl Acad Sci U S A 1985;82:1242-1246 (Pubitemid 15100531)
28. Ortaldo JR, Woodhouse C, Morgan AC, Herberman RB, Cheresh DA, Reisfeld R. Analysis of effector cells in human antibody-dependent cellular cytotoxicity with murine monoclonal antibodies. J Immunol 1987;138:3566-3572 (Pubitemid 17071947)
29. Rosenberg SA, Lotze MT, Muul LM, et al. A progress report on the treatment of 157 patients with advanced cancer using lymphokine-activated killer cells and interleukin-2 or high-dose interleukin-2 alone. N Engl J Med 1987;316:889-897
30. Rosenberg SA, Packard BS, Aebersold PM, et al. Use of tumor-infiltrating lymphocytes and interleukin-2 in the immunotherapy of patients with metastatic melanoma. A preliminary report. N Engl J Med 1988;319:1676-1680
31. Dudley ME, Wunderlich JR, Yang JC, et al. Adoptive cell transfer therapy following non-myeloablative but lymphodepleting chemotherapy for the treatment of patients with refractory metastatic melanoma. J Clin Oncol 2005;23:2346-2357
32. Rosenberg SA, Yang JC, Restifo NP. Cancer immunotherapy: moving beyond current vaccines. Nat Med 2004;10:909-915 (Pubitemid 39273730)
33. Powell DJ, Jr., Dudley ME, Hogan KA, Wunderlich JR, Rosenberg SA. Adoptive transfer of vaccine-induced peripheral blood mononuclear cells to patients with metastatic melanoma following lymphodepletion. J Immunol 2006;177:6527-6539
34. Morgan RA, Dudley ME, Yu YY, et al. High efficiency TCR gene transfer into primary human lymphocytes affords avid recognition of melanoma tumor antigen glycoprotein 100 and does not alter the recognition of autologous melanoma antigens. J Immunol 2003;171:3287-3295
35. + T lymphocytes to the MHC class I-restricted melanoma antigen MAGE-A1 by TCR αβ gene transfer requires CD8α. Gene Ther 2005;12:140-146
36. Alvarez-Vallina L, Hawkins RE. Antigen-specific targeting of CD28-mediated T cell co-stimulation using chimeric single-chain antibody variable fragment-CD28 receptors. Eur J Immunol 1996;26:2304-2309 (Pubitemid 26340928)
37. Finney HM, Lawson AD, Bebbington CR, Weir AN. Chimeric receptors providing both primary and costimulatory signaling in T cells from a single gene product. J Immunol 1998;161:2791-2797
38. Hombach A, Wieczarkowiecz A, Marquardt T, et al. Tumor-specific T cell activation by recombinant immunoreceptors: CD3ζ signaling and CD28 costimulation are simultaneously required for efficient IL-2 secretion and can be integrated into one combined CD28/CD3ζ signaling receptor molecule. J Immunol 2001;167:6123-6131 (Pubitemid 33081538)
39. Sullivan JA. Video 3.1 "lymphocytes attacking melanoma cells." Available from: http://cellsalive.com/stock3.htm.
40. Loskog A, Giandomenico V, Rossig C, Pule M, Dotti G, Brenner MK. Addition of the CD28 signaling domain to chimeric T-cell receptors enhances chimeric T-cell resistance to T regulatory cells. Leukemia 2006;20:1819-1828 (Pubitemid 44574993)
41. Wohlfert EA, Clark RB. Enhanced CD28 signaling may be a common mechanism underlying resistance to regulation. Leukemia 2007;21:175.
42. Mor F, Cohen IR. IL-2 rescues antigen-specific T cells from radiation or dexamethasone-induced apoptosis. Correlation with induction of Bcl-2. J Immunol 1996;156:515-522 (Pubitemid 26028910)
43. + helper T cells. A model for the long-term survival of memory cells. J Immunol 1996;156:1764-1771
44. Haynes NM, Trapani JA, Teng MW, et al. Single-chain antigen recognition receptors that costimulate potent rejection of established experimental tumors. Blood 2002;100:3155-3163
45. + helper T cells induces potent primary and secondary tumor rejection. Blood 2005;106:2995-3003.
46. Brocker T. Chimeric Fv-ζ or Fv-ε receptors are not sufficient to induce activation or cytokine production in peripheral T cells. Blood 2000;96:1999-2001. (Pubitemid 30661090)
47. Wang H, Wei H, Zhang R, et al. Genetically targeted T cells eradicate established breast cancer in syngeneic mice. Clin Cancer Res 2009;15:943-950
48. Savoldo B, Rooney CM, Di Stasi A, et al. Epstein Barr virus specific cytotoxic T lymphocytes expressing the anti-CD30ζ artificial chimeric T-cell receptor for immunotherapy of Hodgkin disease. Blood 2007;110:2620-2630 (Pubitemid 47523186)
49. + T cells. Cancer Res 2007;67:11428-11437
50. Schaafsma MR, Falkenburg JH, Landegent JE, et al. In vivo production of interleukin-5, granulocyte-macrophage colony-stimulating factor, macrophages colony-stimulating factor, and interleukin-6 during intravenous administration of high-dose interleukin-2 in cancer patients. Blood 1991;78:1981-1987
51. Lamers HJ, Gratama JW, van Putten WL, Stoter G, Bolhuis RL. Exogenous interleukin 2 recruits in vitro lymphokine-activated killer activity by in vivo activated lymphocytes. Cancer Res 1991;51:2324-2328
52. Beecham EJ, Ortiz-Pujols S, Junghans RP. Dynamics of tumor cell killing by human T lymphocytes armed with an anti-carcinoembryonic antigen chimeric immunoglobulin T-cell receptor. J Immunother 2000;23:332-343 (Pubitemid 30327368)
53. + T cell clones for the treatment of patients with metastatic melanoma: in vivo persistence, migration, and antitumor effect of transferred T cells. Proc Natl Acad Sci U S A 2002;99:16168-16173
54. Carpenito C, Milone MC, Hassan R, 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;106:3360-3365
55. Carroll RG, Carpenito C, Shan X, et al. Distinct effects of IL-18 on the engraftment and function of human effector CD8 T cells and regulatory T cells. PLoS One 2008;3:e3289.