Is adoptive T-cell therapy for solid tumors coming of age

Bone Marrow Transplantation

Volumn 47, Issue 8, 2012, Pages 1013-1019

  Pedrazzoli, P ^a   Comoli, P ^b   Montagna, D ^c   Demirer, T ^d   Bregni, M ^e  

^a Department of Oncology Hematology ^*  (Italy)

^b FONDAZIONE IRCCS POLICLINICO SAN MATTEO   (Italy)

^c UNIVERSITY OF PAVIA   (Italy)

^d ULUDAG UNIVERSITY   (Turkey)

^e SAN RAFFAELE HOSPITAL   (Italy)

Author keywords

immunotherapy; solid tumors; T cells

Indexed keywords

CHIMERIC PROTEIN; TUMOR ANTIGEN; VIRUS ANTIGEN;

ADOPTIVE T CELL THERAPY; ALLOGENEIC HEMATOPOIETIC STEM CELL TRANSPLANTATION; CANCER CONTROL; CELL SPECIFICITY; CELL THERAPY; CELL TRANSFER; CLINICAL EFFECTIVENESS; CYTOKINE INDUCED KILLER CELL; HUMAN; IMMUNOSURVEILLANCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SOLID TUMOR; T LYMPHOCYTE; TUMOR ASSOCIATED LEUKOCYTE;

ADOPTIVE TRANSFER; EPSTEIN-BARR VIRUS INFECTIONS; HERPESVIRUS 4, HUMAN; HUMANS; IMMUNITY, CELLULAR; MELANOMA; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTES; TRANSDUCTION, GENETIC; TUMOR ESCAPE;

EID: 84864866991     PISSN: 02683369     EISSN: 14765365     Source Type: Journal    
DOI: 10.1038/bmt.2011.155     Document Type: Review

References (64)

1. Balagula Y, Lacouture ME, Cotliar JA. Dermatologic toxicities of targeted anticancer therapies. J Support Oncol 2010; 8: 149-161.
2. Chintalgattu V, Khakoo AY. Review: cardiovascular toxicities due to molecularly targeted cancer therapeutics. Clin Adv Hematol Oncol 2010; 8: 133-135.
3. Dranitsaris G, Truter I, Lubbe MS, Amir E, Evans W. Advances in cancer therapeutics and patient access to new drugs. Pharmacoeconomics 2011; 29: 213-224.
4. Rosenberg SA, Yang JC, White DE, Steinberg SM. Durability of complete responses in patients with metastatic cancer treated with high-dose interleukin-2: Identification of the antigens mediating response. Ann Surg 1998; 228: 307-319. (Pubitemid 30191694)
5. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011; 144: 646-674.
6. Demirer T, Barkholt L, Blaise D, Pedrazzoli P, Aglietta M, Carella AM et al. on behalf of the EBMT Solid Tumors Working Party. Transplantation of allogeneic hematopoietic stem cells: an emerging treatment modality for solid tumors. Nature Clin Pract Oncol 2008; 5: 256-267. (Pubitemid 351596043)
7. Takahashi Y, Harashima N, Kajigaya S, Yokoyama H, Cherkasova E, McCoy JP et al. Regression of human kidney cancer following allogeneic stem cell transplantation is associated with recognition of an HERV-E antigen by T cells. J Clin Invest 2008; 118: 1099-1109. (Pubitemid 351364617)
8. Hutson TE. Targeted therapies for the treatment of metastatic renal cell carcinoma: clinical evidence. Oncologist 2011; 16: 14-22.
9. Grimm EA, Mazumder A, Zhang HZ, Rosenberg SA. Lymphokine-activated killer cell phenomenon. Lysis of natural killer-resistant fresh solid tumor cells by interleukin 2-activated autologous human peripheral blood lymphocytes. J Exp Med 1982; 155: 1823-1841. (Pubitemid 12074218)
10. Mazumder A, Rosenberg SA. Successful immunotherapy of natural killer-resistant established pulmonary melanoma metastases by the intravenous adoptive transfer of syngeneic lymphocytes activated in vitro by interleukin 2. J Exp Med 1984; 159: 495-507. (Pubitemid 14193991)
11. Lafreniere R, Rosenberg SA. Successful immunotherapy of murine experimental hepatic metastases with lymphokineactivated killer cells and recombinant interleukin 2. Cancer Res 1985; 45: 3735-3374.
12. Rosenberg SA, Lotze MT, Muul LM. 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. New Engl J Med 1987; 316: 889-897. (Pubitemid 17041979)
13. Takayama T, Sekine T, Makuuchi M, Yamasaki S, Kosuge T, Yamamoto J et al. Adoptive immunotherapy to lower postsurgical recurrence rates of hepatocellular carcinoma: a randomised trial. Lancet 2000; 356: 802-807.
14. Linn YC, Hui KM. Cytokine-induced NK-like T cells: from bench to bedside. J Biomed Biotechnol 2010; 2010: 435745.
15. Lu PH, Negrin RS. A novel population of expanded human CD3+CD56+ cells derived from T cells with potent in vivo antitumor activity in mice with severe combined immunodeficiency. J Immunol 1994; 153: 1687-1696. (Pubitemid 24251113)
16. Schmidt-Wolf IGH, Lefterova P, Mehta BA, Fernandez LP, Huhn D, Blume KG et al. Phenotypic characterization and identification of effector cells involved in tumor cell recognition of cytokine-induced killer cells. Exp Hematol 1993; 21: 1673-1679. (Pubitemid 24223014)
17. Wang Y, Dai H, Li H, Lv H, Wang T, Fu X et al. Growth of human colorectal cancer SW1116 cells is inhibited by cytokine-induced killer cells. Clin Dev Immunol 2011; 2011: 621414.
18. Hontscha C, Borck Y, Zhou H, Messmer D, Schmidt-Wolf IGH. Clinical trials on CIK cells: first report of the international registry on CIK cells (IRCC). J Cancer Res Clin Oncol 2011; 137: 305-310.
19. Baker J, Verneris MR, Ito M, Shizuru JA, Negrin RS. Expansion of cytolytic CD8(+) natural killer T cells with limited capacity for graft-versus-host disease induction due to interferon gamma production. Blood 2001; 97: 2923-2931.
20. Kuçi S, Rettinger E, Voss B, Weber G, Stais M, Kreyenberg H et al. Efficient lysis of rhabdomyosarcoma cells by cytokineinduced killer cells: implications for adoptive immunotherapy after allogeneic stem cell transplantation. Haematologica 2010; 95: 1579-1586.
21. Sangiolo D, Mesiano G, Carnevale-Schianca F, Piacibello W, Aglietta M, Cignetti A. Cytokine induced killer cells as adoptive immunotherapy strategy to augment graft versus tumor after hematopoietic cell transplantation. Expert Opin Biol Ther 2009; 9: 831-740.
22. Introna M, Pievani A, Borleri G, Capelli C, Algarotti A, Mic C et al. Feasibility and safety of adoptive immunotherapy with CIK cells after cord blood transplantation. Biol Blood Marrow Transplant 2010; 16: 1603-1607.
23. 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. Preliminary report. N Engl J Med 1988; 319: 1676-1680. (Pubitemid 19015247)
24. Rosenberg SA, Dudley ME. Adoptive cell therapy for the treatment of patients with metastatic melanoma. Curr Opin Immunol 2009; 21: 233-240.
25. Rosenberg SA, Yang JC, Sherry RM, Kammula US, Hughes MS, Phan GQ et al. Durable complete responses in heavily pretreted patients with metastatic melanoma using t cell transfer immunotherapy. Clin Cancer Res 2011 (e-pub of print 15 April 2011).
26. 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: 4892-4298.
27. Klapper JA, Thomasian AA, Smith DM, Gorgas GC, Wunderlich JR, Smith FO et al. Single-pass, closed-system rapid expansion of lymphocyte cultures for adoptive cell therapy. J Immunol Methods 2009; 345: 90-99.
28. Weber J, Atkins M, Hwu P, Radvanyi L, Sznol M, Yee C. White Paper on adoptive cell therapy for cancer with tumorinfiltrating lymphocytes: a report of the CTEP subcommittee on adoptive cell therapy. Clin Cancer Res 2011; 17: 1664-1673.
29. Yee C, Thompson JA, Byrd D, Riddell SR, Roche P, Celis E et al. Adoptive T cell therapy using antigen-specific CD8+ 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 USA 2002; 99: 16168-16173. (Pubitemid 35462767)
30. 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: 5060-5069. (Pubitemid 46631410)
31. 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: 2698-2703. (Pubitemid 351860862)
32. Osman Y, Takahashi M, Zheng Z, Toba K, Liu A, Furukawa T et al. Activation of autologous or HLA identical sibling cytotoxic T lymphocytes by blood derived dendritic cells pulsed with tumor cell extract. Oncol Rep 1999; 6: 1057-1063.
33. Hoffmann TK, Meidenbauer N, Dworacki G, Kanaya H, Whiteside T. Generation of tumor-specific T lymphocytes by cross-priming with human dendritic cells ingesting apoptotic tumor cells. Cancer Res 2000; 60: 3542-3549. (Pubitemid 30482175)
34. Kurokawa T, Oelke M, Mackensen A. Induction and clonal expansion of tumor specific cytotoxic lymphocytes from renal cell carcinoma patients after stimulation with autologous dendritic cells loaded with tumor cells. Int J Cancer 2001; 91: 749-756. (Pubitemid 32178640)
35. Montagna D, Schiavo R, Gibelli N, Pedrazzoli P, Tonelli R, Pagani S et al. Ex vivo generation and expansion of anti-tumor cytotoxic T-cell lines derived from patients or their HLAidentical sibling. Int J Cancer 2004; 110: 76-86. (Pubitemid 38507206)
36. Montagna D, Turin I, Schiavo R, Montini E, Zaffaroni N, Villa R et al. Feasibility and safety with ex vivo generated autologous ex vivo cytotoxic T lymphocytes in patients with solid tumor. Cytotherapy 2011 (in press).
37. Nimaco M, Fiander AN, Wilkinson GWG, Borysiewicz LK, Man S. Human papillomavirus-specific cytotoxic T lymphocytes in patients with cervical intraepithelial neoplasia grade III. Cancer Res 1997; 57: 4855-4861. (Pubitemid 27468994)
38. Shablak A, Hawkins RE, Rothwell DG, Elkord E. T cell-based immunotherapy of metastatic renal cell carcinoma: modest success and future perspective. Clin Cancer Res 2009; 15: 6503-6510.
39. Straathof KC, Bollard CM, Popat U, Huls MH, Lopez T, Morriss MC et al. Treatment of nasopharyngeal carcinoma with Epstein-Barr virus-specific T lymphocytes. Blood 2005; 105: 1898-1904. (Pubitemid 40731770)
40. Comoli P, Pedrazzoli P, Maccario R, Basso S, Carminati O, Labirio M et al. Cell therapy of stage IV nasopharyngeal carcinoma with autologous EBV-targeted cytotoxic T-lymphocytes. J Clin Oncol 2005; 23: 8942-8949. (Pubitemid 46211479)
41. Rooney CM, Smith CA, Ng CY, Loftin S, Li C, Krance RA et al. Use of gene-modified virus specific T lymphocytes to control Epstein-Barr-virus-related lymphoproliferation. Lancet 1995; 345: 9-13.
42. Heslop HE, Slobod KS, Pule MA, Hale GA, Rousseau A, Smith CA et al. Long term outcome of EBV specific T-cell infusions to prevent or treat EBV-related lymphoproliferative disease in transplant recipients. Blood 2010; 4: 115 925-935.
43. Haque T, Wilkie GM, Jones MM, Higgins CD, Urquhart G, Wingate P et al. Allogeneic cytotoxic T-cell therapy for EBV-positive posttransplantation lymphoproliferative disease: results of a phase 2 multicenter clinical trial. Blood 2007; 110: 1123-1131. (Pubitemid 47281407)
44. Comoli P, Basso S, Zecca M, Pagliara D, Baldanti F, Bernardo ME et al. Preemptive therapy of EBV-related lymphoproliferative disease after pediatric haploidentical stem cell transplantation. Am J Transplant 2007; 7: 1648-1655. (Pubitemid 46776261)
45. Khanna R, Bell S, Sherritt M, Galbraith A, Burrows SR, Rafter L et al. Activation and adoptive transfer of Epstein-Barr virus-specific cytotoxic T cells in solid organ transplant patients with posttransplant lymphoproliferative disease. Proc Natl Acad Sci USA 1999; 96: 10391-10396. (Pubitemid 29422568)
46. Comoli P, Maccario R, Locatelli F, Valente U, Basso S, Garaventa A et al. Treatment of EBV-related post-renal transplant lymphoproliferative disease with a tailored regimen including EBV-specific T cells. Am J Transplant 2005; 5: 1415-1422. (Pubitemid 40839433)
47. Rickinson AB, Moss DJ. Human cytotoxic T lymphocyte responses to Epstein-Barr virus infection. Annu Rev Immunol 1997; 15: 405-431. (Pubitemid 27169287)
48. Moss DJ, Schmidt C, Elliott S, Suhrbier A, Burrows S, Khanna R. Strategies involved in developing an effective vaccine for EBV-associated diseases. Adv Cancer Res 1996; 69: 213-245. (Pubitemid 126686832)
49. Merlo A, Turrini R, Dolcetti R, Martorelli D, Muraro E, Comoli P et al. The interplay between Epstein-Barr virus and the immune system: a rationale for adoptive cell therapy of EBV-related disorders. Haematologica 2010; 95: 1769-1777.
50. Bollard CM, Aguilar L, Straathof KC, Gahn B, Huls MH, Rousseau A et al. Cytotoxic T lymphocyte therapy for Epstein-Barr virus+ Hodgkin0s disease. J Exp Med 2004; 200: 1623-1633. (Pubitemid 40094186)
51. Louis CU, Straathof K, Bollard CM, Gerken C, Huls MH, Gresik MV et al. Enhancing the in vivo expansion of adoptively transferred EBV-specific CTL with lymphodepleting CD45 monoclonal antibodies in NPC patients. Blood 2009; 113: 2442-2450.
52. Secondino S, Zecca M, Licitra L, Gurrado A, Schiavetto IP, Bossi P et al. T-cell therapy for EBV-associated nasopharyngeal carcinoma: preparative lymphodepleting chemotherapy does not improve clinical results. Ann Oncol 2011 (e-pub ahead of print 17 May 2011).
53. Sadelain M, Riviere I, Brentjens R. Targeting tumours with genetically enhanced T lymphocytes. Nat Rev Cancer 2003; 3: 35-45. (Pubitemid 37328885)
54. Brentjens RJ, Latouche JB, Santos E, Marti F, Gong MC, Lyddane C et al. Eradication of systemic B-cell tumors by genetically targeted human T lymphocytes co-stimulated by CD80 and interleukin-15. Nat Med 2003; 9: 279-286. (Pubitemid 36362782)
55. Savoldo B, Rooney CM, Di SA, Abken H, Hombach A, Foster AE et al. Epstein Barr virus specific cytotoxic T lymphocytes expressing the anti-CD30zeta artificial chimeric T-cell receptor for immunotherapy of Hodgkin disease. Blood 2007; 110: 2620-2630. (Pubitemid 47523186)
56. 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: 6106-6115. (Pubitemid 44703776)
57. Lamers CH, Langeveld SC, Groot-van Ruijven CM, Debets R, Sleijfer S, Gratama JW. Gene-modified T cells for adoptive immunotherapy of renal cell cancer maintain transgene-specific immune functions in vivo. Cancer Immunol Immunother 2007; 56: 1875-1883. (Pubitemid 47512609)
58. Pule MA, Savoldo B, Myers GD, Rossig C, Russell HV, Dotti G et al. Virus-specific T cells engineered to coexpress tumorspecific receptors: persistence and antitumor activity in individuals with neuroblastoma. Nat Med 2008; 14: 1264-1270.
59. 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: 917-924.
60. 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: 1822-1826.
61. Drake CG, Jaffee E, Pardoll DM. Mechanisms of immune evasion by tumors. Adv Immunol 2006; 90: 51-81. (Pubitemid 43765799)
62. Bollard CM, Rossig C, Calonge MJ, Huls MH, Wagner HJ, Massague J et al. Adapting a transforming growth factor betarelated tumor protection strategy to enhance antitumor immunity. Blood 2002; 99: 3179-3187. (Pubitemid 34525296)
63. 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 meloablative chemoradiation preparative regimens. J Clin Oncol 2008; 26: 5233-5239.
64. Hawkins RE, Gilham DE, Debets R, Eshhar Z, Taylor N, Abken H et al. Development of adoptive cell therapy for cancer: a clinical perspective. Hum Gene Ther 2010; 21: 665-672.