Trial Watch: Adoptive cell transfer immunotherapy

Lorenzo Galluzzi, Erika Vacchelli, Alexander Eggermont, Wolf Herve Fridman, Jerome Galon, Catherine Sautès-Fridman, Eric Tartour, Laurence Zitvogel, Guido Kroemer, Lorenzo Galluzzi, Erika Vacchelli, Alexander Eggermont, Wolf Herve Fridman, Jerome Galon, Catherine Sautès-Fridman, Eric Tartour, Laurence Zitvogel, Guido Kroemer

Abstract

During the last two decades, several approaches for the activation of the immune system against cancer have been developed. These include rather unselective maneuvers such as the systemic administration of immunostimulatory agents (e.g., interleukin-2) as well as targeted interventions, encompassing highly specific monoclonal antibodies, vaccines and cell-based therapies. Among the latter, adoptive cell transfer (ACT) involves the selection of autologous lymphocytes with antitumor activity, their expansion/activation ex vivo, and their reinfusion into the patient, often in the context of lymphodepleting regimens (to minimize endogenous immunosuppression). Such autologous cells can be isolated from tumor-infiltrating lymphocytes or generated by manipulating circulating lymphocytes for the expression of tumor-specific T-cell receptors. In addition, autologous lymphocytes can be genetically engineered to prolong their in vivo persistence, to boost antitumor responses and/or to minimize side effects. ACT has recently been shown to be associated with a consistent rate of durable regressions in melanoma and renal cell carcinoma patients and holds great promises in several other oncological settings. In this Trial Watch, we will briefly review the scientific rationale behind ACT and discuss the progress of recent clinical trials evaluating the safety and effectiveness of adoptive cell transfer as an anticancer therapy.

References

    1. de Visser KE, Korets LV, Coussens LM. De novo carcinogenesis promoted by chronic inflammation is B lymphocyte dependent. Cancer Cell. 2005;7:411–23. doi: 10.1016/j.ccr.2005.04.014.
    1. Doedens AL, Stockmann C, Rubinstein MP, Liao D, Zhang N, DeNardo DG, et al. Macrophage expression of hypoxia-inducible factor-1 alpha suppresses T-cell function and promotes tumor progression. Cancer Res. 2010;70:7465–75. doi: 10.1158/0008-5472.CAN-10-1439.
    1. Schioppa T, Moore R, Thompson RG, Rosser EC, Kulbe H, Nedospasov S, et al. B regulatory cells and the tumor-promoting actions of TNF-α during squamous carcinogenesis. Proc Natl Acad Sci U S A. 2011;108:10662–7. doi: 10.1073/pnas.1100994108.
    1. Zitvogel L, Tesniere A, Kroemer G. Cancer despite immunosurveillance: immunoselection and immunosubversion. Nat Rev Immunol. 2006;6:715–27. doi: 10.1038/nri1936.
    1. Galluzzi L, Senovilla L, Zitvogel L, Kroemer G. The secrete ally: immunostimulation by anticancer drugs. Nat Rev Drug Discov. 2012;11:215–33. doi: 10.1038/nrd3626.
    1. Pagès F, Berger A, Camus M, Sanchez-Cabo F, Costes A, Molidor R, et al. Effector memory T cells, early metastasis, and survival in colorectal cancer. N Engl J Med. 2005;353:2654–66. doi: 10.1056/NEJMoa051424.
    1. Galon J, Costes A, Sanchez-Cabo F, Kirilovsky A, Mlecnik B, Lagorce-Pagès C, et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science. 2006;313:1960–4. doi: 10.1126/science.1129139.
    1. Mlecnik B, Tosolini M, Kirilovsky A, Berger A, Bindea G, Meatchi T, et al. Histopathologic-based prognostic factors of colorectal cancers are associated with the state of the local immune reaction. J Clin Oncol. 2011;29:610–8. doi: 10.1200/JCO.2010.30.5425.
    1. Mlecnik B, Bindea G, Pagès F, Galon J. Tumor immunosurveillance in human cancers. Cancer Metastasis Rev. 2011;30:5–12. doi: 10.1007/s10555-011-9270-7.
    1. Rosenberg SA, Yang JC, Restifo NP. Cancer immunotherapy: moving beyond current vaccines. Nat Med. 2004;10:909–15. doi: 10.1038/nm1100.
    1. Rosenberg SA. Cell transfer immunotherapy for metastatic solid cancer--what clinicians need to know. Nat Rev Clin Oncol. 2011;8:577–85. doi: 10.1038/nrclinonc.2011.116.
    1. Hodi FS, O’Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med. 2010;363:711–23. doi: 10.1056/NEJMoa1003466.
    1. Robert C, Thomas L, Bondarenko I, O’Day S, M D JW, Garbe C, et al. Ipilimumab plus dacarbazine for previously untreated metastatic melanoma. N Engl J Med. 2011;364:2517–26. doi: 10.1056/NEJMoa1104621.
    1. Rosenberg SA, Lotze MT, Muul LM, Leitman S, Chang AE, Ettinghausen SE, et al. Observations on the systemic administration of autologous lymphokine-activated killer cells and recombinant interleukin-2 to patients with metastatic cancer. N Engl J Med. 1985;313:1485–92. doi: 10.1056/NEJM198512053132327.
    1. Smith FO, Downey SG, Klapper JA, Yang JC, Sherry RM, Royal RE, et al. Treatment of metastatic melanoma using interleukin-2 alone or in conjunction with vaccines. Clin Cancer Res. 2008;14:5610–8. doi: 10.1158/1078-0432.CCR-08-0116.
    1. Tartour E, Pere H, Maillere B, Terme M, Merillon N, Taieb J, et al. Angiogenesis and immunity: a bidirectional link potentially relevant for the monitoring of antiangiogenic therapy and the development of novel therapeutic combination with immunotherapy. Cancer Metastasis Rev. 2011;30:83–95. doi: 10.1007/s10555-011-9281-4.
    1. Finn OJ. Cancer vaccines: between the idea and the reality. Nat Rev Immunol. 2003;3:630–41. doi: 10.1038/nri1150.
    1. Kantoff PW, Higano CS, Shore ND, Berger ER, Small EJ, Penson DF, et al. IMPACT Study Investigators Sipuleucel-T immunotherapy for castration-resistant prostate cancer. N Engl J Med. 2010;363:411–22. doi: 10.1056/NEJMoa1001294.
    1. Small EJ, Schellhammer PF, Higano CS, Redfern CH, Nemunaitis JJ, Valone FH, et al. Placebo-controlled phase III trial of immunologic therapy with sipuleucel-T (APC8015) in patients with metastatic, asymptomatic hormone refractory prostate cancer. J Clin Oncol. 2006;24:3089–94. doi: 10.1200/JCO.2005.04.5252.
    1. Beer TM, Bernstein GT, Corman JM, Glode LM, Hall SJ, Poll WL, et al. Randomized trial of autologous cellular immunotherapy with sipuleucel-T in androgen-dependent prostate cancer. Clin Cancer Res. 2011;17:4558–67. doi: 10.1158/1078-0432.CCR-10-3223.
    1. Kantoff PW, Schuetz TJ, Blumenstein BA, Glode LM, Bilhartz DL, Wyand M, et al. Overall survival analysis of a phase II randomized controlled trial of a Poxviral-based PSA-targeted immunotherapy in metastatic castration-resistant prostate cancer. J Clin Oncol. 2010;28:1099–105. doi: 10.1200/JCO.2009.25.0597.
    1. Schwartzentruber DJ, Lawson DH, Richards JM, Conry RM, Miller DM, Treisman J, et al. gp100 peptide vaccine and interleukin-2 in patients with advanced melanoma. N Engl J Med. 2011;364:2119–27. doi: 10.1056/NEJMoa1012863.
    1. Rosenberg SA, Yang JC, Sherry RM, Kammula US, Hughes MS, Phan GQ, et al. Durable complete responses in heavily pretreated patients with metastatic melanoma using T-cell transfer immunotherapy. Clin Cancer Res. 2011;17:4550–7. doi: 10.1158/1078-0432.CCR-11-0116.
    1. Gattinoni L, Powell DJ, Jr., Rosenberg SA, Restifo NP. Adoptive immunotherapy for cancer: building on success. Nat Rev Immunol. 2006;6:383–93. doi: 10.1038/nri1842.
    1. Shlomchik WD. Graft-versus-host disease. Nat Rev Immunol. 2007;7:340–52. doi: 10.1038/nri2000.
    1. Tacken PJ, de Vries IJ, Torensma R, Figdor CG. Dendritic-cell immunotherapy: from ex vivo loading to in vivo targeting. Nat Rev Immunol. 2007;7:790–802. doi: 10.1038/nri2173.
    1. Bouquie´ R, Bonnin A, Bernardeau K, Khammari A, Dre´no B, Jotereau F, et al. A fast and efficient HLA multimer-based sorting procedure that induces little apoptosis to isolate clinical grade human tumor specific T lymphocytes. Cancer Immunol Immunother. 2009;58:553–66. doi: 10.1007/s00262-008-0578-2.
    1. Yun YS, Hargrove ME, Ting CC. In vivo antitumor activity of anti-CD3-induced activated killer cells. Cancer Res. 1989;49:4770–4.
    1. Aebersold P, Hyatt C, Johnson S, Hines K, Korcak L, Sanders M, et al. Lysis of autologous melanoma cells by tumor-infiltrating lymphocytes: association with clinical response. J Natl Cancer Inst. 1991;83:932–7. doi: 10.1093/jnci/83.13.932.
    1. Klebanoff CA, Gattinoni L, Torabi-Parizi P, Kerstann K, Cardones AR, Finkelstein SE, et al. Central memory self/tumor-reactive CD8+ T cells confer superior antitumor immunity compared with effector memory T cells. Proc Natl Acad Sci U S A. 2005;102:9571–6. doi: 10.1073/pnas.0503726102.
    1. Schwartzentruber DJ, Hom SS, Dadmarz R, White DE, Yannelli JR, Steinberg SM, et al. In vitro predictors of therapeutic response in melanoma patients receiving tumor-infiltrating lymphocytes and interleukin-2. J Clin Oncol. 1994;12:1475–83.
    1. Zhou J, Shen X, Huang J, Hodes RJ, Rosenberg SA, Robbins PF. Telomere length of transferred lymphocytes correlates with in vivo persistence and tumor regression in melanoma patients receiving cell transfer therapy. J Immunol. 2005;175:7046–52.
    1. Kalbasi A, Shrimali RK, Chinnasamy D, Rosenberg SA. Prevention of interleukin-2 withdrawal-induced apoptosis in lymphocytes retrovirally cotransduced with genes encoding an antitumor T-cell receptor and an antiapoptotic protein. J Immunother. 2010;33:672–83. doi: 10.1097/CJI.0b013e3181e475cd.
    1. Liu K, Rosenberg SA. Transduction of an IL-2 gene into human melanoma-reactive lymphocytes results in their continued growth in the absence of exogenous IL-2 and maintenance of specific antitumor activity. J Immunol. 2001;167:6356–65.
    1. Hinrichs CS, Borman ZA, Gattinoni L, Yu Z, Burns WR, Huang J, et al. Human effector CD8+ T cells derived from naive rather than memory subsets possess superior traits for adoptive immunotherapy. Blood. 2011;117:808–14. doi: 10.1182/blood-2010-05-286286.
    1. Zhang Q, Yang X, Pins M, Javonovic B, Kuzel T, Kim SJ, et al. Adoptive transfer of tumor-reactive transforming growth factor-beta-insensitive CD8+ T cells: eradication of autologous mouse prostate cancer. Cancer Res. 2005;65:1761–9. doi: 10.1158/0008-5472.CAN-04-3169.
    1. Gross G, Waks T, Eshhar Z. Expression of immunoglobulin-T-cell receptor chimeric molecules as functional receptors with antibody-type specificity. Proc Natl Acad Sci U S A. 1989;86:10024–8. doi: 10.1073/pnas.86.24.10024.
    1. Li LP, Lampert JC, Chen X, Leitao C, Popovicá J, Müller W, et al. Transgenic mice with a diverse human T cell antigen receptor repertoire. Nat Med. 2010;16:1029–34. doi: 10.1038/nm.2197.
    1. Chhabra A, Yang L, Wang P, Comin-Anduix B, Das R, Chakraborty NG, et al. CD4+CD25- T cells transduced to express MHC class I-restricted epitope-specific TCR synthesize Th1 cytokines and exhibit MHC class I-restricted cytolytic effector function in a human melanoma model. J Immunol. 2008;181:1063–70.
    1. Ray S, Chhabra A, Chakraborty NG, Hegde U, Dorsky DI, Chodon T, et al. UCLA-CALTECH-CHLA-USC-UCONN Consortium on Translational Program in Engineered Immunity MHC-I-restricted melanoma antigen specific TCR-engineered human CD4+ T cells exhibit multifunctional effector and helper responses, in vitro. Clin Immunol. 2010;136:338–47. doi: 10.1016/j.clim.2010.04.013.
    1. Godet Y, Moreau-Aubry A, Guilloux Y, Vignard V, Khammari A, Dreno B, et al. MELOE-1 is a new antigen overexpressed in melanomas and involved in adoptive T cell transfer efficiency. J Exp Med. 2008;205:2673–82. doi: 10.1084/jem.20081356.
    1. Godet Y, Desfrançois J, Vignard V, Schadendorf D, Khammari A, Dreno B, et al. Frequent occurrence of high affinity T cells against MELOE-1 makes this antigen an attractive target for melanoma immunotherapy. Eur J Immunol. 2010;40:1786–94. doi: 10.1002/eji.200940132.
    1. 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;314:126–9. doi: 10.1126/science.1129003.
    1. Morgan RA, Dudley ME, Yu YY, Zheng Z, Robbins PF, Theoret MR, 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;171:3287–95.
    1. Parkhurst MR, Yang JC, Langan RC, Dudley ME, Nathan DA, Feldman SA, et al. T cells targeting carcinoembryonic antigen can mediate regression of metastatic colorectal cancer but induce severe transient colitis. Mol Ther. 2011;19:620–6. doi: 10.1038/mt.2010.272.
    1. Simpson AJ, Caballero OL, Jungbluth A, Chen YT, Old LJ. Cancer/testis antigens, gametogenesis and cancer. Nat Rev Cancer. 2005;5:615–25. doi: 10.1038/nrc1669.
    1. Robbins PF, Morgan RA, Feldman SA, Yang JC, Sherry RM, Dudley ME, et al. Tumor regression in patients with metastatic synovial cell sarcoma and melanoma using genetically engineered lymphocytes reactive with NY-ESO-1. J Clin Oncol. 2011;29:917–24. doi: 10.1200/JCO.2010.32.2537.
    1. Hunder NN, Wallen H, Cao J, Hendricks DW, Reilly JZ, Rodmyre R, et al. Treatment of metastatic melanoma with autologous CD4+ T cells against NY-ESO-1. N Engl J Med. 2008;358:2698–703. doi: 10.1056/NEJMoa0800251.
    1. Willemsen R, Ronteltap C, Heuveling M, Debets R, Bolhuis R. Redirecting human CD4+ T lymphocytes to the MHC class I-restricted melanoma antigen MAGE-A1 by TCR alphabeta gene transfer requires CD8alpha. Gene Ther. 2005;12:140–6. doi: 10.1038/sj.gt.3302388.
    1. Chinnasamy N, Wargo JA, Yu Z, Rao M, Frankel TL, Riley JP, et al. A TCR targeting the HLA-A*0201-restricted epitope of MAGE-A3 recognizes multiple epitopes of the MAGE-A antigen superfamily in several types of cancer. J Immunol. 2011;186:685–96. doi: 10.4049/jimmunol.1001775.
    1. Brentjens RJ, Rivière I, Park JH, Davila ML, Wang X, Stefanski J, et al. Safety and persistence of adoptively transferred autologous CD19-targeted T cells in patients with relapsed or chemotherapy refractory B-cell leukemias. Blood. 2011;118:4817–28. doi: 10.1182/blood-2011-04-348540.
    1. 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. doi: 10.1182/blood-2010-04-281931.
    1. 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. doi: 10.1056/NEJMoa1103849.
    1. 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. doi: 10.1172/JCI43490.
    1. Rosenberg SA, Packard BS, Aebersold PM, Solomon D, Topalian SL, Toy ST, 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;319:1676–80. doi: 10.1056/NEJM198812223192527.
    1. 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;202:907–12. doi: 10.1084/jem.20050732.
    1. Klebanoff CA, Khong HT, Antony PA, Palmer DC, Restifo NP. Sinks, suppressors and antigen presenters: how lymphodepletion enhances T cell-mediated tumor immunotherapy. Trends Immunol. 2005;26:111–7. doi: 10.1016/j.it.2004.12.003.
    1. Wrzesinski C, Paulos CM, Kaiser A, Muranski P, Palmer DC, Gattinoni L, et al. Increased intensity lymphodepletion enhances tumor treatment efficacy of adoptively transferred tumor-specific T cells. J Immunother. 2010;33:1–7. doi: 10.1097/CJI.0b013e3181b88ffc.
    1. Tartour E, Latour S, Mathiot C, Thiounn N, Mosseri V, Joyeux I, et al. Variable expression of CD3-zeta chain in tumor-infiltrating lymphocytes (TIL) derived from renal-cell carcinoma: relationship with TIL phenotype and function. Int J Cancer. 1995;63:205–12. doi: 10.1002/ijc.2910630210.
    1. Tartour E, Mathiot C, Fridman WH. Current status of interleukin-2 therapy in cancer. Biomed Pharmacother. 1992;46:473–84. doi: 10.1016/0753-3322(92)90005-R.
    1. Ahmadzadeh M, Rosenberg SA. IL-2 administration increases CD4+ CD25(hi) Foxp3+ regulatory T cells in cancer patients. Blood. 2006;107:2409–14. doi: 10.1182/blood-2005-06-2399.
    1. Saadoun D, Rosenzwajg M, Joly F, Six A, Carrat F, Thibault V, et al. Regulatory T-cell responses to low-dose interleukin-2 in HCV-induced vasculitis. N Engl J Med. 2011;365:2067–77. doi: 10.1056/NEJMoa1105143.
    1. Koreth J, Matsuoka K, Kim HT, McDonough SM, Bindra B, Alyea EP, 3rd, et al. Interleukin-2 and regulatory T cells in graft-versus-host disease. N Engl J Med. 2011;365:2055–66. doi: 10.1056/NEJMoa1108188.
    1. Mignot G, Ullrich E, Bonmort M, Me´nard C, Apetoh L, Taieb J, et al. The critical role of IL-15 in the antitumor effects mediated by the combination therapy imatinib and IL-2. J Immunol. 2008;180:6477–83.
    1. Ullrich E, Bonmort M, Mignot G, Jacobs B, Bosisio D, Sozzani S, et al. Trans-presentation of IL-15 dictates IFN-producing killer dendritic cells effector functions. J Immunol. 2008;180:7887–97.
    1. Liu DL, Håkansson CH, Seifert J. Immunotherapy in liver tumors: II. Intratumoral injection with activated tumor-infiltrating lymphocytes, intrasplenic administration of recombinant interleukin-2 and interferon alpha causes tumor regression and lysis. Cancer Lett. 1994;85:39–46. doi: 10.1016/0304-3835(94)90236-4.
    1. Helms MW, Prescher JA, Cao YA, Schaffert S, Contag CH. IL-12 enhances efficacy and shortens enrichment time in cytokine-induced killer cell immunotherapy. Cancer Immunol Immunother. 2010;59:1325–34. doi: 10.1007/s00262-010-0860-y.
    1. Dings RP, Vang KB, Castermans K, Popescu F, Zhang Y, Oude Egbrink MG, et al. Enhancement of T-cell-mediated antitumor response: angiostatic adjuvant to immunotherapy against cancer. Clin Cancer Res. 2011;17:3134–45. doi: 10.1158/1078-0432.CCR-10-2443.
    1. Yang Y, Huang CT, Huang X, Pardoll DM. Persistent Toll-like receptor signals are required for reversal of regulatory T cell-mediated CD8 tolerance. Nat Immunol. 2004;5:508–15. doi: 10.1038/ni1059.
    1. North RJ. Cyclophosphamide-facilitated adoptive immunotherapy of an established tumor depends on elimination of tumor-induced suppressor T cells. J Exp Med. 1982;155:1063–74. doi: 10.1084/jem.155.4.1063.
    1. Li Q, Lao X, Pan Q, Ning N, Yet J, Xu Y, et al. Adoptive transfer of tumor reactive B cells confers host T-cell immunity and tumor regression. Clin Cancer Res. 2011;17:4987–95. doi: 10.1158/1078-0432.CCR-11-0207.
    1. Pegram HJ, Jackson JT, Smyth MJ, Kershaw MH, Darcy PK. Adoptive transfer of gene-modified primary NK cells can specifically inhibit tumor progression in vivo. J Immunol. 2008;181:3449–55.
    1. Ruggeri L, Capanni M, Urbani E, Perruccio K, Shlomchik WD, Tosti A, et al. Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science. 2002;295:2097–100. doi: 10.1126/science.1068440.
    1. Velardi A, Ruggeri L, Mancusi A, Aversa F, Christiansen FT. Natural killer cell allorecognition of missing self in allogeneic hematopoietic transplantation: a tool for immunotherapy of leukemia. Curr Opin Immunol. 2009;21:525–30. doi: 10.1016/j.coi.2009.07.015.
    1. Parkhurst MR, Riley JP, Dudley ME, Rosenberg SA. Adoptive transfer of autologous natural killer cells leads to high levels of circulating natural killer cells but does not mediate tumor regression. Clin Cancer Res. 2011;17:6287–97. doi: 10.1158/1078-0432.CCR-11-1347.
    1. Geller MA, Cooley S, Judson PL, Ghebre R, Carson LF, Argenta PA, et al. A phase II study of allogeneic natural killer cell therapy to treat patients with recurrent ovarian and breast cancer. Cytotherapy. 2011;13:98–107. doi: 10.3109/14653249.2010.515582.
    1. Besser MJ, Shapira-Frommer R, Treves AJ, Zippel D, Itzhaki O, Hershkovitz L, et al. Clinical responses in a phase II study using adoptive transfer of short-term cultured tumor infiltration lymphocytes in metastatic melanoma patients. Clin Cancer Res. 2010;16:2646–55. doi: 10.1158/1078-0432.CCR-10-0041.
    1. Donia M, Junker N, Ellebaek E, Andersen MH, Straten PT, Svane IM. Characterization and comparison of “Standard” and “Young” tumor infiltrating lymphocytes for adoptive cell therapy at a Danish Translational Research Institution. Scand J Immunol. 2011 in press.
    1. Dudley ME, Gross CA, Langhan MM, Garcia MR, Sherry RM, Yang JC, et al. CD8+ enriched “young” tumor infiltrating lymphocytes can mediate regression of metastatic melanoma. Clin Cancer Res. 2010;16:6122–31. doi: 10.1158/1078-0432.CCR-10-1297.
    1. Vignard V, Lemercier B, Lim A, Pandolfino MC, Guilloux Y, Khammari A, et al. Adoptive transfer of tumor-reactive Melan-A-specific CTL clones in melanoma patients is followed by increased frequencies of additional Melan-A-specific T cells. J Immunol. 2005;175:4797–805.
    1. Anders K, Buschow C, Herrmann A, Milojkovic A, Loddenkemper C, Kammertoens T, et al. Oncogene-targeting T cells reject large tumors while oncogene inactivation selects escape variants in mouse models of cancer. Cancer Cell. 2011;20:755–67. doi: 10.1016/j.ccr.2011.10.019.
    1. Johnson LA, Morgan RA, Dudley ME, Cassard L, Yang JC, Hughes MS, et al. Gene therapy with human and mouse T-cell receptors mediates cancer regression and targets normal tissues expressing cognate antigen. Blood. 2009;114:535–46. doi: 10.1182/blood-2009-03-211714.
    1. 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;18:666–8. doi: 10.1038/mt.2010.31.
    1. 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;18:843–51. doi: 10.1038/mt.2010.24.
    1. Bendle GM, Linnemann C, Hooijkaas AI, Bies L, de Witte MA, Jorritsma A, et al. Lethal graft-versus-host disease in mouse models of T cell receptor gene therapy. Nat Med 2010; 16:565-70, 1p following 70.
    1. Dudley ME, Wunderlich JR, Yang JC, Sherry RM, Topalian SL, Restifo NP, 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;23:2346–57. doi: 10.1200/JCO.2005.00.240.
    1. Mackensen A, Meidenbauer N, Vogl S, Laumer M, Berger J, Andreesen R. Phase I study of adoptive T-cell therapy using antigen-specific CD8+ T cells for the treatment of patients with metastatic melanoma. J Clin Oncol. 2006;24:5060–9. doi: 10.1200/JCO.2006.07.1100.
    1. Heemskerk B, Liu K, Dudley ME, Johnson LA, Kaiser A, Downey S, et al. Adoptive cell therapy for patients with melanoma, using tumor-infiltrating lymphocytes genetically engineered to secrete interleukin-2. Hum Gene Ther. 2008;19:496–510. doi: 10.1089/hum.2007.0171.
    1. 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;26:5233–9. doi: 10.1200/JCO.2008.16.5449.
    1. Disis ML, Bernhard H, Jaffee EM. Use of tumour-responsive T cells as cancer treatment. Lancet. 2009;373:673–83. doi: 10.1016/S0140-6736(09)60404-9.
    1. Khammari A, Labarrière N, Vignard V, Nguyen JM, Pandolfino MC, Knol AC, et al. Treatment of metastatic melanoma with autologous Melan-A/MART-1-specific cytotoxic T lymphocyte clones. J Invest Dermatol. 2009;129:2835–42. doi: 10.1038/jid.2009.144.
    1. Hong JJ, Rosenberg SA, Dudley ME, Yang JC, White DE, Butman JA, et al. Successful treatment of melanoma brain metastases with adoptive cell therapy. Clin Cancer Res. 2010;16:4892–8. doi: 10.1158/1078-0432.CCR-10-1507.
    1. Verdegaal EM, Visser M, Ramwadhdoebe´ TH, van der Minne CE, van Steijn JA, Kapiteijn E, et al. Successful treatment of metastatic melanoma by adoptive transfer of blood-derived polyclonal tumor-specific CD4+ and CD8+ T cells in combination with low-dose interferon-alpha. Cancer Immunol Immunother. 2011;60:953–63. doi: 10.1007/s00262-011-1004-8.
    1. Butler MO, Friedlander P, Milstein MI, Mooney MM, Metzler G, Murray AP, et al. Establishment of antitumor memory in humans using in vitro-educated CD8+ T cells. Sci Transl Med. 2011;3:80ra34. doi: 10.1126/scitranslmed.3002207.
    1. Chang AE, Li Q, Jiang G, Sayre DM, Braun TM, Redman BG. Phase II trial of autologous tumor vaccination, anti-CD3-activated vaccine-primed lymphocytes, and interleukin-2 in stage IV renal cell cancer. J Clin Oncol. 2003;21:884–90. doi: 10.1200/JCO.2003.08.023.
    1. Thompson JA, Figlin RA, Sifri-Steele C, Berenson RJ, Frohlich MW. A phase I trial of CD3/CD28-activated T cells (Xcellerated T cells) and interleukin-2 in patients with metastatic renal cell carcinoma. Clin Cancer Res. 2003;9:3562–70.
    1. Zhou P, Liang P, Dong B, Yu X, Han Z, Xu Y. Phase I clinical study of combination therapy with microwave ablation and cellular immunotherapy in hepatocellular carcinoma. Cancer Biol Ther. 2011;11:450–6. doi: 10.4161/cbt.11.5.14669.
    1. Kershaw MH, Westwood JA, Parker LL, Wang G, Eshhar Z, Mavroukakis SA, et al. A phase I study on adoptive immunotherapy using gene-modified T cells for ovarian cancer. Clin Cancer Res. 2006;12:6106–15. doi: 10.1158/1078-0432.CCR-06-1183.
    1. Pule MA, Savoldo B, Myers GD, Rossig C, Russell HV, Dotti G, et al. Virus-specific T cells engineered to coexpress tumor-specific receptors: persistence and antitumor activity in individuals with neuroblastoma. Nat Med. 2008;14:1264–70. doi: 10.1038/nm.1882.
    1. Yamasaki K, Horiguchi S, Kurosaki M, Kunii N, Nagato K, Hanaoka H, et al. Induction of NKT cell-specific immune responses in cancer tissues after NKT cell-targeted adoptive immunotherapy. Clin Immunol. 2011;138:255–65. doi: 10.1016/j.clim.2010.11.014.
    1. Curti BD, Ochoa AC, Powers GC, Kopp WC, Alvord WG, Janik JE, et al. Phase I trial of anti-CD3-stimulated CD4+ T cells, infusional interleukin-2, and cyclophosphamide in patients with advanced cancer. J Clin Oncol. 1998;16:2752–60.
    1. Laport GG, Levine BL, Stadtmauer EA, Schuster SJ, Luger SM, Grupp S, et al. Adoptive transfer of costimulated T cells induces lymphocytosis in patients with relapsed/refractory non-Hodgkin lymphoma following CD34+-selected hematopoietic cell transplantation. Blood. 2003;102:2004–13. doi: 10.1182/blood-2003-01-0095.
    1. Berdeja JG, Hess A, Lucas DM, O’Donnell P, Ambinder RF, Diehl LF, et al. Systemic interleukin-2 and adoptive transfer of lymphokine-activated killer cells improves antibody-dependent cellular cytotoxicity in patients with relapsed B-cell lymphoma treated with rituximab. Clin Cancer Res. 2007;13:2392–9. doi: 10.1158/1078-0432.CCR-06-1860.
    1. Wallen H, Thompson JA, Reilly JZ, Rodmyre RM, Cao J, Yee C. Fludarabine modulates immune response and extends in vivo survival of adoptively transferred CD8 T cells in patients with metastatic melanoma. PLoS One. 2009;4:e4749. doi: 10.1371/journal.pone.0004749.
    1. Rapoport AP, Aqui NA, Stadtmauer EA, Vogl DT, Fang HB, Cai L, et al. Combination immunotherapy using adoptive T-cell transfer and tumor antigen vaccination on the basis of hTERT and survivin after ASCT for myeloma. Blood. 2011;117:788–97. doi: 10.1182/blood-2010-08-299396.
    1. Kochenderfer JN, Dudley ME, Feldman SA, Wilson WH, Spaner DE, Maric I, et al. B-cell depletion and remissions of malignancy along with cytokine-associated toxicity in a clinical trial of anti-CD19 chimeric-antigen-receptor-transduced T cells. Blood. 2011 doi: 10.1182/blood-2011-10-384388. in press.
    1. Sangiolo D. Cytokine induced killer cells as promising immunotherapy for solid tumors. J Cancer. 2011;2:363–8. doi: 10.7150/jca.2.363.

Source: PubMed

Sponsorer og samarbeidspartnere

Medisinsk tilstand

Legemiddelintervensjoner

3
Abonnere