At the Bench: Adoptive cell therapy for melanoma

Journal of Leukocyte Biology

Volumn 95, Issue 6, 2014, Pages 867-874

  Urba, Walter J ^a  

^a EARLE A CHILES RESEARCH INSTITUTE   (United States)

Author keywords

Cytokines; Lymphoid depletion; Murine; Transgenic

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 15; INTERLEUKIN 2; INTERLEUKIN 7; L SELECTIN; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MELAN A; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; TYROSINASE RELATED PROTEIN 1;

ADOPTIVE CELL THERAPY; ADOPTIVE IMMUNOTHERAPY; ADOPTIVE TRANSFER; ANTIGEN PRESENTATION; ARTICLE; CD8+ T LYMPHOCYTE; CELL THERAPY; HUMAN; LYMPHOCYTE DEPLETION; LYMPHOCYTE DIFFERENTIATION; LYMPHOKINE ACTIVATED KILLER CELL; MAJOR HISTOCOMPATIBILITY COMPLEX RESTRICTION; MELANOCYTE; MELANOMA; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION; THERAPY EFFECT;

CYTOKINES; LYMPHOID DEPLETION; MURINE; TRANSGENIC;

ANIMALS; COXSACKIE AND ADENOVIRUS RECEPTOR-LIKE MEMBRANE PROTEIN; HUMANS; IMMUNOTHERAPY, ADOPTIVE; INTERLEUKIN-2; KILLER CELLS, LYMPHOKINE-ACTIVATED; LYMPHOCYTE DEPLETION; MELANOMA; PROTEIN ENGINEERING; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTES;

EID: 84901705453     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.0513301     Document Type: Article

References (52)

1. Oettgen, H. F., Old, L. J. (1991) The history of cancer immunotherapy. In Biologic Therapy of Cancer (V. T. DeVita Jr., Hellman, S. and S. A. Rosenberg, eds.), J. B. Lippincott, Philadelphia, 87-119.
2. Rosenberg, S. A., Restifo, N. P., Yang, J. C., Morgan, R. A., Dudley, M. E. (2008) Adoptive cell transfer: a clinical path to effective cancer immunotherapy. Nat. Rev. Cancer 8, 299-308.
3. Cheever, M. A., Kempf, R. A., Fefer, A. (1977) Tumor neutralization, immunotherapy, and chemoimmmunotherapy of a Friend leukemia with cells secondarily sensitized in vitro. J. Immunol. 119, 714-718.
4. Morgan, D. A., Ruscetti, F. W., Gallo, R. (1976) Selective in vitro growth of T lymphocytes from normal human bone marrows. Science 193, 1007-1008.
5. Rosenberg, S. A., Mule, J. J., Spiess, P. J., Reichert, C. M., Schwarz, S. L. (1985) Regression of established pulmonary metastases and subcutaneous tumor mediated by the systemic administration of high-dose recombinant interleukin 2. J. Exp. Med. 161, 1169-1188.
6. Lotze, M. T., Grimm, E. A., Mazumder, A., Strausser, J. L., Rosenberg, S. A. (1981) Lysis of fresh and cultured autologous tumor by human lymphocytes cultured in T-cell growth factor. Cancer Res. 41, 4420-4425.
7. Restifo, N. P., Dudley, M. E., Rosenberg, S. A. (2012) Adoptive immunotherapy for cancer: harnessing the T cell response. Nat. Rev. Immunol. 12, 269-281.
8. Cheever, M. A., Chen, W. (1997) Therapy with cultured T cells: principles revisited. Immunol. Rev. 157, 177-194.
9. Rosenberg, S. A., Spiess, P., Lafreniere, R. (1986) A new approach to the adoptive immunotherapy of cancer with tumor-infiltrating lymphocytes. Science 233, 1318-1321.
10. North, R. J. (1982) Cyclophosphamide-facilitated adoptive immunotherapy of an established tumor depends on elimination of tumor-induced suppressor T cells. J. Exp. Med. 155, 1063-1074.
11. Dummer, W., Niethammer, A. G., Baccala, R., Lawson, B. R., Wagner, N., Reisfeld, R. A., Theofilopoulos, A. N. (2002) T cell homeostatic proliferation elicits effective antitumor autoimmunity. J. Clin. Invest. 110, 185-192.
12. Hu, H. M., Poehlein, C. H., Urba, W. J., Fox, B. A. (2002) Development of antitumor immune responses in reconstituted lymphopenic hosts. Cancer Res. 62, 3914-3919.
13. Klebanoff, C. A., Khong, H. T., Antony, P. A., Palmer, D. C., Restifo, N. P. (2005) Sinks, suppressors and antigen presenters: how lymphodepletion enhances T cell-mediated tumor immunotherapy. Trends Immunol. 26, 111-117.
14. Overwijk, W. W., Theoret, M. R., Finkelstein, S. E., Surman, D. R., de Jong, L. A., Vyth-Dreese, F. A., Dellemijn, T. A., Antony, P. A., Spiess, P. J., Palmer, D. C., Heimann, D. M., Klebanoff, C. A., Yu, Z., Hwang, L. N., Feigenbaum, L., Kruisbeek, A. M., Rosenberg, S. A., Restifo, N. P. (2003) Tumor regression and autoimmunity after reversal of a functionally tolerant state of self-reactive CD8+ T cells. J. Exp. Med. 198, 569-580.
15. Antony, P. A., Piccirillo, C. A., Akpinarli, A., Finkelstein, S. E., Speiss, P. J., Surman, D. R., Palmer, D. C., Chan, C. C., Klebanoff, C. A., Overwijk, W. W., Rosenberg, S. A., Restifo, N. P. (2005) CD8+ T cell immunity against a tumor/self-antigen is augmented by CD4+ T helper cells and hindered by naturally occurring T regulatory cells. J. Immunol. 174, 2591-2601.
16. Gattinoni, L., Finkelstein, S. E., Klebanoff, C. A., Antony, P. A., Palmer, D. C., Spiess, P. J., Hwang, L. N., Yu, Z., Wrzesinski, C., Heimann, D. M., Surh, C. D., Rosenberg, S. A., Restifo, N. P. (2005) Removal of homeostatic cytokine sinks by lymphodepletion enhances the efficacy of adoptively transferred tumor-specific CD8+ T cells. J. Exp. Med. 202, 907-912.
17. Burnette, B., Fu, Y. X., Weichselbaum, R. R. (2012) The confluence of radiotherapy and immunotherapy. Front. Oncol. 2, 143.
18. Zitvogel, L., Kepp, O., Kroemer, G. (2010) Decoding cell death signals in inflammation and immunity. Cell 140, 798-804.
19. Gabrilovich, D. I., Nagaraj, S. (2009) Myeloid-derived suppressor cells as regulators of the immune system. Nat. Rev. Immunol. 9, 162-174.
20. Mok, S., Koya, R. C., Tsui, C., Xu, J., Robert, L., Wu, L., Graeber, T. G., West, B. L., Bollag, G., Ribas, A. (2013) Inhibition of CSF-1 receptor improves the antitumor efficacy of adoptive cell transfer immunotherapy. Cancer Res. 74, 153-161.
21. Wrzesinski, C., Paulos, C. M., Gattinoni, L., Palmer, D. C., Kaiser, A., Yu, Z., Rosenberg, S. A., Restifo, N. P. (2007) Hematopoietic stem cells promote the expansion and function of adoptively transferred antitumor CD8 T cells. J. Clin. Invest. 117, 492-501.
22. Dudley, M. E., Yang, J. C., Sherry, R., Hughes, M. S., Royal, R., Kammula, U., Robbins, P. F., Huang, J., Citrin, D. E., Leitman, S. F., Wunderlich, J., Restifo, N. P., Thomasian, A., Downey, S. G., Smith, F. O., Klapper, J., Morton, K., Laurencot, C., White, D. E., Rosenberg, S. A. (2008) Adoptive cell therapy for patients with metastatic melanoma: evaluation of intensive myeloablative chemoradiation preparative regimens. J. Clin. Oncol. 26, 5233-5239.
23. Sallusto, F., Geginat, J., Lanzavecchia, A. (2004) Central memory and effector memory T cell subsets: function, generation, and maintenance. Annu. Rev. Immunol. 22, 745-763.
24. Gattinoni, L., Klebanoff, C. A., Palmer, D. C., Wrzesinski, C., Kerstann, K., Yu, Z., Finkelstein, S. E., Theoret, M. R., Rosenberg, S. A., Restifo, N. P. (2005) Acquisition of full effector function in vitro paradoxically impairs the in vivo antitumor efficacy of adoptively transferred CD8+ T cells. J. Clin. Invest. 115, 1616-1626.
25. Klebanoff, C. A., Gattinoni, L., Restifo, N. P. (2012) Sorting through subsets: which T-cell populations mediate highly effective adoptive immunotherapy? J. Immunother. 35, 651-660.
26. Hinrichs, C. S., Borman, Z. A., Cassard, L., Gattinoni, L., Spolski, R., Yu, Z., Sanchez-Perez, L., Muranski, P., Kern, S. J., Logun, C., Palmer, D. C., Ji, Y., Reger, R. N., Leonard, W. J., Danner, R. L., Rosenberg, S. A., Restifo, N. P. (2009) Adoptively transferred effector cells derived from naive rather than central memory CD8+ T cells mediate superior antitumor immunity. Proc. Natl. Acad. Sci. USA 106, 17469-17474.
27. Gattinoni, L., Klebanoff, C. A., Restifo, N. P. (2012) Paths to stemness: building the ultimate antitumour T cell. Nat. Rev. Cancer 12, 671-684.
28. Berger, C., Jensen, M. C., Lansdorp, P. M., Gough, M., Elliott, C., Riddell, S. R. (2008) Adoptive transfer of effector CD8+ T cells derived from central memory cells establishes persistent T cell memory in primates. J. Clin. Invest. 118, 294-305.
29. Wang, X., Berger, C., Wong, C. W., Forman, S. J., Riddell, S. R., Jensen, M. C. (2012) Engraftment of human central memory-derived effector CD8+ T cells in immunodeficient mice. Blood 117, 1888-1898.
30. Butler, M. O., Lee, J. S., Ansen, S., Neuberg, D., Hodi, F. S., Murray, A. P., Drury, L., Berezovskaya, A., Mulligan, R. C., Nadler, L. M., Hirano, N. (2007) Long-lived antitumor CD8+ lymphocytes for adoptive therapy generated using an artificial antigen-presenting cell. Clin. Cancer Res. 13, 1857-1867.
31. Butler, M. O., Friedlander, P., Milstein, M. I., Mooney, M. M., Metzler, G., Murray, A. P., Tanaka, M., Berezovskaya, A., Imataki, O., Drury, L., Brennan, L., Flavin, M., Neuberg, D., Stevenson, K., Lawrence, D., Hodi, F. S., Velazquez, E. F., Jaklitsch, M. T., Russell, S. E., Mihm, M., Nadler, L. M., Hirano, N. (2011) Establishment of antitumor memory in humans using in vitro-educated CD8+ T cells. Sci. Transl. Med. 3, 80ra34.
32. Wang, A., Chandran, S., Shah, S. A., Chiu, Y., Paria, B. C., Aghamolla, T., Alvarez-Downing, M. M., Lee, C. C., Singh, S., Li, T., Dudley, M. E., Restifo, N. P., Rosenberg, S. A., Kammula, U. S. (2012) The stoichiometric production of IL-2 and IFN-α mRNA defines memory T cells that can self-renew after adoptive transfer in humans. Sci. Transl. Med. 4, 149ra120.
33. Quezada, S. A., Simpson, T. R., Peggs, K. S., Merghoub, T., Vider, J., Fan, X., Blasberg, R., Yagita, H., Muranski, P., Antony, P. A., Restifo, N. P., Allison, J. P. (2010) Tumor-reactive CD4(+) T cells develop cytotoxic activity and eradicate large established melanoma after transfer into lymphopenic hosts. J. Exp. Med. 207, 637-650.
34. Xie, Y., Akpinarli, A., Maris, C., Hipkiss, E. L., Lane, M., Kwon, E. K., Muranski, P., Restifo, N. P., Antony, P. A. (2010) Naive tumor-specific CD4(+) T cells differentiated in vivo eradicate established melanoma. J. Exp. Med. 207, 651-667.
35. Johnson, L. A., Morgan, R. A., Dudley, M. E., Cassard, L., Yang, J. C., Hughes, M. S., Kammula, U. S., Royal, R. E., Sherry, R. M., Wunderlich, J. R., Lee, C. C., Restifo, N. P., Schwarz, S. L., Cogdill, A. P., Bishop, R. J., Kim, H., Brewer, C. C., Rudy, S. F., VanWaes, C., Davis, J. L., Mathur, A., Ripley, R. T., Nathan, D. A., Laurencot, C. M., Rosenberg, S. A. (2009) Gene therapy with human and mouse T-cell receptors mediates cancer regression and targets normal tissues expressing cognate antigen. Blood 114, 535-546.
36. Morgan, R. A., Chinnasamy, N., Abate-Daga, D., Gros, A., Robbins, P. F., Zheng, Z., Dudley, M. E., Feldman, S. A., Yang, J. C., Sherry, R. M., Phan, G. Q., Hughes, M. S., Kammula, U. S., Miller, A. D., Hessman, C. J., Stewart, A. A., Restifo, N. P., Quezado, M. M., Alimchandani, M., Rosenberg, A. Z., Nath, A., Wang, T., Bielekova, B., Wuest, S. C., Akula, N., McMahon, F. J., Wilde, S., Mosetter, B., Schendel, D. J., Laurencot, C. M., Rosenberg, S. A. (2013) Cancer regression and neurological toxicity following anti-MAGE-A3 TCR gene therapy. J. Immunother. 36, 133-151.
37. Parkhurst, M. R., Yang, J. C., Langan, R. C., Dudley, M. E., Nathan, D. A., Feldman, S. A., Davis, J. L., Morgan, R. A., Merino, M. J., Sherry, R. M., Hughes, M. S., Kammula, U. S., Phan, G. Q., Lim, R. M., Wank, S. A., Restifo, N. P., Robbins, P. F., Laurencot, C. M., Rosenberg, S. A. (2011) T cells targeting carcinoembryonic antigen can mediate regression of metastatic colorectal cancer but induce severe transient colitis. Mol. Ther. 19, 620-626.
38. Cameron, B. J., Gerry, A. B., Dukes, J., Harper, J. V., Kannan, V., Bianchi, F. C., Grand, F., Brewer, J. E., Gupta, M., Plesa, G., Bossi, G., Vuidepot, A., Powlesland, A. S., Legg, A., Adams, K. J., Bennett, A. D., Pumphrey, N. J., Williams, D. D., Binder-Scholl, G., Kulikovskaya, I., Levine, B. L., Riley, J. L., Varela-Rohena, A., Stadtmauer, E. A., Rapoport, A. P., Linette, G. P., June, C. H., Hassan, N. J., Kalos, M., Jakobsen, B. K. (2013) Identification of a titin-derived HLA-A1-presented peptide as a cross-reactive target for engineered MAGE A3-directed T cells. Sci. Transl. Med. 5, 197ra103.
39. Linette, G. P., Stadtmauer, E. A., Maus, M. V., Rapoport, A. P., Levine, B. L., Emery, L., Litzky, L., Bagg, A., Carreno, B. M., Cimino, P. J., Binder-Scholl, G. K., Smethurst, D. P., Gerry, A. B., Pumphrey, N. J., Bennett, A. D., Brewer, J. E., Dukes, J., Harper, J., Tayton-Martin, H. K., Jakobsen, B. K., Hassan, N. J., Kalos, M., June, C. H. (2013) Cardiovascular toxicity and titin cross-reactivity of affinity-enhanced T cells in myeloma and melanoma. Blood 122, 863-871.
40. Porter, D. L., Levine, B. L., Kalos, M., Bagg, A., June, C. H. (2012) Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. N. Engl. J. Med. 365, 725-733.
41. Hwu, P., Yang, J. C., Cowherd, R., Treisman, J., Shafer, G. E., Eshhar, Z., Rosenberg, S. A. (1995) In vivo antitumor activity of T cells redirected with chimeric antibody/T-cell receptor genes. Cancer Res. 55, 3369-3373.
42. Chmielewski, M., Maliar, A., Eshhar, Z., Abken, H. (2012) CAR's made it to the pancreas. Oncoimmunology 1, 1387-1389.
43. Beatty, G. L., Haas, A. R., Maus, M. V., Torigian, D. A., Soulen, M. C., Plesa, G., Chew, A., Zhao, Y., Levine, B. L., Albelda, S. M., Kalos, M., June, C. H. (2013) Mesothelin-specific chimeric antigen receptor mRNA-engineered T cells induce antitumor activity in solid malignancies. Cancer Immunol. Res. 2, 1-9.
44. Yvon, E., Del Vecchio, M., Savoldo, B., Hoyos, V., Dutour, A., Anichini, A., Dotti, G., Brenner, M. K. (2009) Immunotherapy of metastatic melanoma using genetically engineered GD2-specific T cells. Clin. Cancer Res. 15, 5852-5860.
45. Lo, A. S., Ma, Q., Liu, D. L., Junghans, R. P. (2010) Anti-GD3 chimeric sFv-CD28/T-cell receptor α designer T cells for treatment of metastatic melanoma and other neuroectodermal tumors. Clin. Cancer Res. 16, 2769-2780.
46. Burns, W. R., Zhao, Y., Frankel, T. L., Hinrichs, C. S., Zheng, Z., Xu, H., Feldman, S. A., Ferrone, S., Rosenberg, S. A., Morgan, R. A. (2010) A high molecular weight melanoma-associated antigen-specific chimeric antigen receptor redirects lymphocytes to target human melanomas. Cancer Res. 70, 3027-3033.
47. Marktel, S., Magnani, Z., Ciceri, F., Cazzaniga, S., Riddell, S. R., Traversari, C., Bordignon, C., Bonini, C. (2003) Immunologic potential of donor lymphocytes expressing a suicide gene for early immune reconstitution after hematopoietic T-cell-depleted stem cell transplantation. Blood 101, 1290-1298.
48. Kieback, E., Charo, J., Sommermeyer, D., Blankenstein, T., Uckert, W. (2008) A safeguard eliminates T cell receptor gene-modified autoreactive T cells after adoptive transfer. Proc. Natl. Acad. Sci. USA 105, 623-628.
49. Di Stasi, A., Tey, S. K., Dotti, G., Fujita, Y., Kennedy-Nasser, A., Martinez, C., Straathof, K., Liu, E., Durett, A. G., Grilley, B., Liu, H., Cruz, C. R., Savoldo, B., Gee, A. P., Schindler, J., Krance, R. A., Heslop, H. E., Spencer, D. M., Rooney, C. M., Brenner, M. K. (2011) Inducible apoptosis as a safety switch for adoptive cell therapy. N. Engl. J. Med. 365, 1673-1683.
50. Barrett, D. M., Zhao, Y., Liu, X., Jiang, S., Carpenito, C., Kalos, M., Carroll, R. G., June, C. H., Grupp, S. A. (2011) Treatment of advanced leukemia in mice with mRNA engineered T cells. Hum. Gene Ther. 22, 1575-1586.
51. Fedorov, V. D., Themeli, M., Sadelain, M. (2013) PD-1-and CTLA-4-based inhibitory chimeric antigen receptors (iCARs) divert off-target immunotherapy responses. Sci. Transl. Med. 5, 215ra172.
52. Vonderheide, R. H., June, C. H. (2014) Engineering T cells for cancer: our synthetic future. Immunol. Rev. 257, 7-13.