Expansion and characterization of human melanoma tumor-infiltrating lymphocytes (TILs)

PLoS ONE

Volumn 5, Issue 11, 2010, Pages

  Nguyen, Linh T ^a   Yen, Pei Hua ^a   Nie, Jessica ^a   Liadis, Nicole ^a   Ghazarian, Danny ^b   Al Habeeb, Ayman ^b   Easson, Alexandra ^b   Leong, Wey ^b   Lipa, Joan ^b   McCready, David ^b   Reedijk, Michael ^b   Hogg, David ^b   Joshua, Anthony M ^b   Quirt, Ian ^b   Messner, Hans ^b   Shaw, Patricia ^b   Crump, Michael ^b   Sharon, Eran ^b   Ohashi, Pamela S ^a,c  

^a PRINCESS MARGARET HOSPITAL   (Canada)

^b UNIVERSITY HEALTH NETWORK   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON;

ADOPTIVE IMMUNOTHERAPY; ADULT; AGED; ARTICLE; CD3+ T LYMPHOCYTE; CD4 CD8 RATIO; CELL EXPANSION; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOTOXICITY; FEMALE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOREACTIVITY; LYMPHOCYTE CULTURE; LYMPHOCYTE PROLIFERATION; MALE; MELANOMA; TUMOR ASSOCIATED LEUKOCYTE; CELL CULTURE; CELL PROLIFERATION; COCULTURE; IMMUNOLOGY; IMMUNOPHENOTYPING; METABOLISM; METHODOLOGY; MIDDLE AGED; PATHOLOGY; TRANSPLANTATION; TUMOR CELL CULTURE; TUMOR CELL LINE;

ADULT; AGED; AGED, 80 AND OVER; CELL LINE, TUMOR; CELL PROLIFERATION; CELLS, CULTURED; COCULTURE TECHNIQUES; CYTOTOXICITY, IMMUNOLOGIC; FEMALE; FLOW CYTOMETRY; HUMANS; IMMUNOPHENOTYPING; IMMUNOTHERAPY, ADOPTIVE; INTERFERON-GAMMA; LYMPHOCYTES, TUMOR-INFILTRATING; MALE; MELANOMA; MIDDLE AGED; TUMOR CELLS, CULTURED;

EID: 78649756275     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0013940     Document Type: Article

References (49)

1. Shankaran V, Ikeda H, Bruce AT, White JM, Swanson PE, et al. (2001) IFNgamma and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature 410: 1107-1111.
2. Dunn GP, Old LJ, Schreiber RD (2004) The immunobiology of cancer immunosurveillance and immunoediting. Immunity 21: 137-148.
3. Romero P, Dunbar PR, Valmori D, Pittet MJ, Ogg GS, et al. (1998) Ex vivo staining of metastatic lymph nodes by class I major histocompatibility complex tetramers reveals high numbers of antigen-experienced tumor-specific cytotoxic T lymphocytes. J Exp Med 188: 1641-1650.
4. Pittet MJ, Valmori D, Dunbar PR, Speiser DE, Lienard D, et al. (1999) High frequencies of naive Melan-A/MART-1-specific CD8(+) T cells in a large proportion of human histocompatibility leukocyte antigen (HLA)-A2 individuals. J Exp Med 190: 705-715.
5. Kawakami Y, Dang N, Wang X, Tupesis J, Robbins PF, et al. (2000) Recognition of shared melanoma antigens in association with major HLA-A alleles by tumor infiltrating T lymphocytes from 123 patients with melanoma. J Immunother 23: 17-27.
6. Boon T, Coulie PG, Van den Eynde BJ, van der Bruggen P (2006) Human T cell responses against melanoma. Annu Rev Immunol 24: 175-208.
7. Speiser DE, Lienard D, Rufer N, Rubio-Godoy V, Rimoldi D, et al. (2005) Rapid and strong human CD8+ T cell responses to vaccination with peptide, IFA, and CpG oligodeoxynucleotide 7909. J Clin Invest 115: 739-746.
8. Schwartzentruber DJ, Lawson D, Richards J, Conry RM, Miller D, et al. (2009) A phase III multi-institutional randomized study of immunization with the gp100:209-217(210 M) peptide followed by high-dose IL-2 compared with high-dose IL-2 alone in patients with metastatic melanoma. J Clin Oncol 27: 18s.
9. Weber J (2008) Overcoming immunologic tolerance to melanoma: targeting CTLA-4 with ipilimumab (MDX-010). Oncologist 13(Suppl 4): 16-25.
10. Ribas A (2008) Overcoming immunologic tolerance to melanoma: targeting CTLA-4 with tremelimumab (CP-675,206). Oncologist 13(Suppl 4): 10-15.: 10-15.
11. Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, et al. (2010) Improved Survival with Ipilimumab in Patients with Metastatic Melanoma. N Engl J Med 363: 711-723.
12. Blank C, Gajewski TF, Mackensen A (2005) Interaction of PD-L1 on tumor cells with PD-1 on tumor-specific T cells as a mechanism of immune evasion: implications for tumor immunotherapy. Cancer Immunol Immunother 54: 307-314.
13. Berger R, Rotem-Yehudar R, Slama G, Landes S, Kneller A, et al. (2008) Phase I safety and pharmacokinetic study of CT-011, a humanized antibody interacting with PD-1, in patients with advanced hematologic malignancies. Clin Cancer Res 14: 3044-3051.
14. Brahmer JR, Drake CG, Wollner I, Powderly JD, Picus J, et al. (2010) Phase I Study of Single-Agent Anti-Programmed Death-1 (MDX-1106) in Refractory Solid Tumors: Safety, Clinical Activity, Pharmacodynamics, and Immunologic Correlates. J Clin Oncol 28: 3167-3175.
15. Dudley ME, Wunderlich J, Nishimura MI, Yu D, Yang JC, et al. (2001) Adoptive transfer of cloned melanoma-reactive T lymphocytes for the treatment of patients with metastatic melanoma. J Immunother 24: 363-373.
16. Yee C, Thompson JA, Byrd D, Riddell SR, Roche P, et al. (2002) 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 U S A 99: 16168-16173.
17. Vignard V, Lemercier B, Lim A, Pandolfino MC, Guilloux Y, et al. (2005) 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 175: 4797-4805.
18. Hunder NN, Wallen H, Cao J, Hendricks DW, Reilly JZ, et al. (2008) Treatment of metastatic melanoma with autologous CD4+ T cells against NY-ESO-1. N Engl J Med 358: 2698-2703.
19. Rosenberg SA, Packard BS, Aebersold PM, Solomon D, Topalian SL, et al. (1988) Use of tumor-infiltrating lymphocytes and interleukin-2 in the immunotherapy of patients with metastatic melanoma. A preliminary report. N Engl J Med 319: 1676-1680.
20. Kradin RL, Kurnick JT, Lazarus DS, Preffer FI, Dubinett SM, et al. (1989) Tumour-infiltrating lymphocytes and interleukin-2 in treatment of advanced cancer. Lancet 1: 577-580.
21. Baars JW, Fonk JC, Scheper RJ, von Blomberg-van der Flier BM, Bril H, et al. (1992) Treatment with tumour infiltrating lymphocytes and interleukin-2 in patients with metastatic melanoma: a pilot study. Biotherapy 4: 289-297.
22. Dillman RO, Church C, Oldham RK, West WH, Schwartzberg L, et al. (1993) Inpatient continuous-infusion interleukin-2 in 788 patients with cancer. The National Biotherapy Study Group experience. Cancer 71: 2358-2370.
23. Rosenberg SA, Yannelli JR, Yang JC, Topalian SL, Schwartzentruber DJ, et al. (1994) Treatment of patients with metastatic melanoma with autologous tumor-infiltrating lymphocytes and interleukin 2. J Natl Cancer Inst 86: 1159-1166.
24. Ravaud A, Legrand E, Delaunay MM, Bussieres E, Coulon V, et al. (1995) A phase I trial of repeated tumour-infiltrating lymphocyte (TIL) infusion in metastatic melanoma. Br J Cancer 71: 331-336.
25. Goedegebuure PS, Douville LM, Li H, Richmond GC, Schoof DD, et al. (1995) Adoptive immunotherapy with tumor-infiltrating lymphocytes and interleukin-2 in patients with metastatic malignant melanoma and renal cell carcinoma: a pilot study. J Clin Oncol 13: 1939-1949.
26. Reali UM, Martini L, Borgognoni L, Semino C, Pietra G, et al. (1998) Infusion of in vitro expanded tumour-infiltrating lymphocytes and recombinant interleukin-2 in patients with surgically resected lymph node metastases of malignant melanoma: a pilot study. Melanoma Res 8: 77-82.
27. Queirolo P, Ponte M, Gipponi M, Cafiero F, Peressini A, et al. (1999) Adoptive immunotherapy with tumor-infiltrating lymphocytes and subcutaneous recom-binant interleukin-2 plus interferon alfa-2a for melanoma patients with nonresectable distant disease: a phase I/II pilot trial. Melanoma Istituto Scientifico Tumori Group. Ann Surg Oncol 6: 272-278.
28. Dreno B, Nguyen JM, Khammari A, Pandolfino MC, Tessier MH, et al. (2002) Randomized trial of adoptive transfer of melanoma tumor-infiltrating lymphocytes as adjuvant therapy for stage III melanoma. Cancer Immunol Immunother 51: 539-546.
29. Dudley ME, Wunderlich JR, Robbins PF, Yang JC, Hwu P, et al. (2002) Cancer regression and autoimmunity in patients after clonal repopulation with antitumor lymphocytes. Science 298: 850-854.
30. Dudley ME, Wunderlich JR, Yang JC, Sherry RM, Topalian SL, et al. (2005) Adoptive cell transfer therapy following non-myeloablative but lymphodepleting chemotherapy for the treatment of patients with refractory metastatic melanoma. J Clin Oncol 23: 2346-2357.
31. Dudley ME, Yang JC, Sherry R, Hughes MS, Royal R, et al. (2008) Adoptive Cell Therapy for Patients With Metastatic Melanoma: Evaluation of Intensive Myeloablative Chemoradiation Preparative Regimens. J Clin Oncol 26: 5233-5239.
32. Besser MJ, Shapira-Frommer R, Treves AJ, Zippel D, Itzhaki O, et al. (2009) Minimally cultured or selected autologous tumor-infiltrating lymphocytes after a lympho-depleting chemotherapy regimen in metastatic melanoma patients. J Immunother 32: 415-423.
33. Morgan RA, Dudley ME, Wunderlich JR, Hughes MS, Yang JC, et al. (2006) Cancer Regression in Patients After Transfer of Genetically Engineered Lymphocytes. Science 314: 68-69.
34. Aoki Y, Takakuwa K, Kodama S, Tanaka K, Takahashi M, et al. (1991) Use of adoptive transfer of tumor-infiltrating lymphocytes alone or in combination with cisplatin-containing chemotherapy in patients with epithelial ovarian cancer. Cancer Res 51: 1934-1939.
35. Belldegrun A, Pierce W, Kaboo R, Tso CL, Shau H, et al. (1993) Interferon-alpha primed tumor-infiltrating lymphocytes combined with interleukin-2 and interferon-alpha as therapy for metastatic renal cell carcinoma. J Urol 150: 1384-1390.
36. Ratto GB, Melioli G, Zino P, Mereu C, Mirabelli S, et al. (1995) Immunotherapy with the use of tumor-infiltrating lymphocytes and interleu-kin-2 as adjuvant treatment in stage III non-small-cell lung cancer. A pilot study. J Thorac Cardiovasc Surg 109: 1212-1217.
37. Gardini A, Ercolani G, Riccobon A, Ravaioli M, Ridolfi L, et al. (2004) Adjuvant, adoptive immunotherapy with tumor infiltrating lymphocytes plus interleukin-2 after radical hepatic resection for colorectal liver metastases: 5-year analysis. J Surg Oncol 87: 46-52.
38. Atkins MB, Kunkel L, Sznol M, Rosenberg SA (2000) High-dose recombinant interleukin-2 therapy in patients with metastatic melanoma: long-term survival update. Cancer J Sci Am 6(Suppl 1): S11-4.: S11-S14.
39. Bedikian AY, Millward M, Pehamberger H, Conry R, Gore M, et al. (2006) Bcl-2 antisense (oblimersen sodium) plus dacarbazine in patients with advanced melanoma: the Oblimersen Melanoma Study Group. J Clin Oncol 24: 4738-4745.
40. Wallen H, Thompson JA, Reilly JZ, Rodmyre RM, Cao J, et al. (2009) Fludarabine modulates immune response and extends in vivo survival of adoptively transferred CD8 T cells in patients with metastatic melanoma. PLoS One 4: e4749.
41. Tran KQ, Zhou J, Durflinger KH, Langhan MM, Shelton TE, et al. (2008) Minimally cultured tumor-infiltrating lymphocytes display optimal characteristics for adoptive cell therapy. J Immunother 31: 742-751.
42. Besser MJ, Shapira-Frommer R, Treves AJ, Zippel D, Itzhaki O, et al. (2010) Clinical responses in a phase II study using adoptive transfer of short-term cultured tumor infiltration lymphocytes in metastatic melanoma patients. Clin Cancer Res 16: 2646-2655.
43. Clark WH, Jr., Elder DE, Van Horn M (1986) The biologic forms of malignant melanoma. Hum Pathol 17: 443-450.
44. Cao K, Hollenbach J, Shi X, Shi W, Chopek M, et al. (2001) Analysis of the frequencies of HLA-A, B, and C alleles and haplotypes in the five major ethnic groups of the United States reveals high levels of diversity in these loci and contrasting distribution patterns in these populations. Hum Immunol 62: 1009-1030.
45. Pittet MJ, Speiser DE, Valmori D, Cerottini JC, Romero P (2000) Cutting edge: cytolytic effector function in human circulating CD8+ T cells closely correlates with CD56 surface expression. J Immunol 164: 1148-1152.
46. Barrow C, Browning J, MacGregor D, Davis ID, Sturrock S, et al. (2006) Tumor antigen expression in melanoma varies according to antigen and stage. Clin Cancer Res 12: 764-771.
47. Bachmann MF, Sebzda E, Kündig TM, Shahinian A, Speiser DE, et al. (1996) T cell responses are governed by avidity and costimulatory thresholds. Eur J Immunol 26: 2017-2022.
48. Ohlen C, Kalos M, Cheng LE, Shur AC, Hong DJ, et al. (2002) CD8(+) T cell tolerance to a tumor-associated antigen is maintained at the level of expansion rather than effector function. J Exp Med 195: 1407-1418.
49. Dudley ME, Wunderlich JR, Shelton TE, Even J, Rosenberg SA (2003) Generation of tumor-infiltrating lymphocyte cultures for use in adoptive transfer therapy for melanoma patients. J Immunother 26: 332-342.