Efficient and reproducible generation of tumour-infiltrating lymphocytes for renal cell carcinoma

British Journal of Cancer

Volumn 112, Issue 9, 2015, Pages 1510-1518

  Baldan, V ^a   Griffiths, R ^a,b   Hawkins, R E ^a   Gilham, D E ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b CLATTERBRIDGE CENTRE FOR ONCOLOGY   (United Kingdom)

Author keywords

adoptive cell therapy; disaggregation; lymphocyte, culture; mitogen; renal cell carcinoma; T cell; TIL; tumour

Indexed keywords

ADULT; AGED; ANTINEOPLASTIC ACTIVITY; ARTICLE; CELL COUNT; CELL EXPANSION; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; KIDNEY CARCINOMA; LEUKOCYTE ACTIVATION; MALE; MIDDLE AGED; PRIORITY JOURNAL; T LYMPHOCYTE; TUMOR ASSOCIATED LEUKOCYTE; TUMOR BIOPSY; CARCINOMA, RENAL CELL; CYTOTOXICITY; FOLLOW UP; IMMUNOLOGY; KIDNEY NEOPLASMS; PROGNOSIS; TUMOR CELL CULTURE;

AGED; CARCINOMA, RENAL CELL; CYTOTOXICITY, IMMUNOLOGIC; FEMALE; FOLLOW-UP STUDIES; HUMANS; KIDNEY NEOPLASMS; LYMPHOCYTES, TUMOR-INFILTRATING; MALE; MIDDLE AGED; PROGNOSIS; T-LYMPHOCYTES; TUMOR CELLS, CULTURED;

EID: 84928763657     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/bjc.2015.96     Document Type: Article

References (34)

1. Alcantar-Orozco EM, Gornall H, Baldan V, Hawkins RE, Gilham DE. (2013). Potential limitations of the NSG humanized mouse as a model system to optimize engineered human T cell therapy for cancer. Hum Gene Ther Methods 24: 310-320
2. Besser MJ, Shapira-Frommer R, Itzhaki O, Treves AJ, Zippel DB, Levy D, Kubi A, Shoshani N, Zikich D, Ohayon Y, Ohayon D, Shalmon B, Markel G, Yerushalmi R, Apter S, Ben-Nun A, Ben-Ami E, Shimoni A, Nagler A, Schachter J. (2013). Adoptive transfer of tumor-infiltrating lymphocytes in patients with metastatic melanoma: intent-To-Treat analysis and efficacy after failure to prior immunotherapies. Clin Cancer Res 19: 4792-4800
3. Besser MJ, Shapira-Frommer R, Treves AJ, Zippel D, Itzhaki O, Hershkovitz L, Levy D, Kubi A, Hovav E, Chermoshniuk N, Shalmon B, Hardan I, Catane R, Markel G, Apter S, Ben-Nun A, Kuchuk I, Shimoni A, Nagler A, Schachter J. (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
4. Bouet-Toussaint F, Genetel N, Rioux-Leclercq N, Bansard JY, Leveque J, Guille F, Patard JJ, Lesimple T, Catros-Quemener V. (2000). Interleukin-2 expanded lymphocytes from lymph node and tumor biopsies of human renal cell carcinoma, breast and ovarian cancer. Eur Cytokine Netw 11: 217-224
5. Danilova E, Skrindo I, Gran E, Hales BJ, Smith WA, Jahnsen J, Johansen FE, Jahnsen FL, Baekkevold ES. (2015). A role for CCL28-CCR3 in T-cell homing to the human upper airway mucosa. Mucosal Immunol 8(1): 107-114
6. Dillman R, Schiltz P, DePriest C, Barth N, Beutel L, de Leon C, OConnor A, Nayak S. (2004). Tumor-infiltrating lymphocytes and interleukin-2: dose and schedules of administration in the treatment of metastatic cancer. Cancer Biother Radiopharm 19: 730-737
7. Dudley ME, Gross CA, Langhan MM, Garcia MR, Sherry RM, Yang JC, Phan GQ, Kammula US, Hughes MS, Citrin DE, Restifo NP, Wunderlich JR, Prieto PA, Hong JJ, Langan RC, Zlott DA, Morton KE, White DE, Laurencot CM, Rosenberg SA. (2010). CD8+ enriched young tumor infiltrating lymphocytes can mediate regression of metastatic melanoma. Clin Cancer Res 16: 6122-6131
8. 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
9. Dudley ME, Yang JC, Sherry R, Hughes MS, Royal R, Kammula U, Robbins PF, Huang J, Citrin DE, Leitman SF, Wunderlich J, Restifo NP, Thomasian A, Downey SG, Smith FO, Klapper J, Morton K, Laurencot C, White DE, Rosenberg SA. (2008). Adoptive cell therapy for patients with metastatic melanoma: evaluation of intensive myeloablative chemoradiation preparative regimens. J Clin Oncol 26: 5233-5239
10. Figlin RA, Pierce WC, Kaboo R, Tso CL, Moldawer N, Gitlitz B, deKernion J, Belldegrun A. (1997). Treatment of metastatic renal cell carcinoma with nephrectomy, interleukin-2 and cytokine-primed or CD8(+) selected tumor infiltrating lymphocytes from primary tumor. J Urol 158: 740-745
11. Figlin RA, Thompson JA, Bukowski RM, Vogelzang NJ, Novick AC, Lange P, Steinberg GD, Belldegrun AS. (1999). Multicenter, randomized, phase III trial of CD8(+) tumor-infiltrating lymphocytes in combination with recombinant interleukin-2 in metastatic renal cell carcinoma. J Clin Oncol 17: 2521-2529
12. Gattinoni L, Klebanoff CA, Restifo NP. (2012). Paths to stemness: building the ultimate antitumour T cell. Nat Rev Cancer 12: 671-684
13. Gerlinger M, Quezada SA, Peggs KS, Furness AJ, Fisher R, Marafioti T, Shende VH, McGranahan N, Rowan AJ, Hazell S, Hamm D, Robins HS, Pickering L, Gore M, Nicol DL, Larkin J, Swanton C. (2013). Ultra-deep T cell receptor sequencing reveals the complexity and intratumour heterogeneity of T cell clones in renal cell carcinomas. J Pathol 231: 424-432
14. Goedegebuure PS, Douville LM, Li H, Richmond GC, Schoof DD, Scavone M, Eberlein TJ. (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
15. Gilham DE, ONeil A, Hughes C, Guest RD, Kirillova N, Lehane M, Hawkins RE. (2002). Primary polyclonal human T lymphocytes targeted to carcino-embryonic antigens and neural cell adhesion molecule tumor antigens by CD3zeta-based chimeric immune receptors. J Immunother 25(2): 139-151
16. Griffiths RW, Gilham DE, Dangoor A, Ramani V, Clarke NW, Stern PL, Hawkins RE. (2005). Expression of the 5T4 oncofoetal antigen in renal cell carcinoma: a potential target for T-cell-based immunotherapy. Br J Cancer 93(6): 670-677
17. Griffiths RW, Elkord E, Gilham DE, Ramani V, Clarke N, Stern PL, Hawkins RE. (2007). Frequency of regulatory T cells in renal cell carcinoma patients and investigation of correlation with survival. Cancer Immunol Immunother 56: 1743-1753
18. Gros A, Robbins PF, Yao X, Li YF, Turcotte S, Tran E, Wunderlich JR, Mixon A, Farid S, Dudley ME, Hanada K, Almeida JR, Darko S, Douek DC, Yang JC, Rosenberg SA. (2014). PD-1 identifies the patient-specific CD8(+) tumor-reactive repertoire infiltrating human tumors. J Clin Invest 124: 2246-2259
19. Igarashi T, Takahashi H, Tobe T, Suzuki H, Mizoguchi K, Nakatsu HO, Ito H. (2002). Effect of tumor-infiltrating lymphocyte subsets on prognosis and susceptibility to interferon therapy in patients with renal cell carcinoma. Urol Int 69: 51-56
20. Malone CC, Schiltz PM, Mackintosh AD, Beutel LD, Heinemann FS, Dillman RO. (2001). Characterization of human tumor-infiltrating lymphocytes expanded in hollow-fiber bioreactors for immunotherapy of cancer. Cancer Biother Radiopharm 16: 381-390
21. Markel G, Cohen-Sinai T, Besser MJ, Oved K, Itzhaki O, Seidman R, Fridman E, Treves AJ, Keisari Y, Dotan Z, Ramon J, Schachter J. (2009). Preclinical evaluation of adoptive cell therapy for patients with metastatic renal cell carcinoma. Anticancer Res 29: 145-154
22. Mautner J, Jaffee EM, Pardoll DM. (2005). Tumor-specific CD4+ T cells from a patient with renal cell carcinoma recognize diverse shared antigens. Int J Cancer 115: 752-759
23. McLoughlin RM, Lee JC, Kasper DL, Tzianabos AO. (2008). IFN-gamma regulated chemokine production determines the outcome of Staphylococcus aureus infection. J Immunol 181(2): 1323-1332
24. Rosenberg SA, Yang JC, Sherry RM, Kammula US, Hughes MS, Phan GQ, Citrin DE, Restifo NP, Robbins PF, Wunderlich JR, Morton KE, Laurencot CM, Steinberg SM, White DE, Dudley ME. (2011). Durable complete responses in heavily pretreated patients with metastatic melanoma using T-cell transfer immunotherapy. Clin Cancer Res 17: 4550-4557
25. Sittig SP, Kollgaard T, Gronbaek K, Idorn M, Hennenlotter J, Stenzl A, Gouttefangeas C, Thor Straten P. (2013). Clonal expansion of renal cell carcinoma-infiltrating T lymphocytes. Oncoimmunology 2: e26014
26. Takahara M, Miyai M, Tomiyama M, Mutou M, Nicol AJ, Nieda M. (2008). Copulsing tumor antigen-pulsed dendritic cells with zoledronate efficiently enhance the expansion of tumor antigen-specific CD8+ T cells via Vgamma9 gamma delta T cell activation. J Leukoc Biol 83(3): 742-754
27. Takeuchi M, Inoue T, Otani T, Yamasaki F, Nakamura S, Kibata M. (2010). Cell-in-cell structures formed between human cancer cell lines and the cytotoxic regulatory T-cell line HOZOT. J Mol Cell Biol 2(3): 139-151
28. Tassi E, Facchinetti V, Seresini S, Borri A, Dellantonio G, Garavaglia C, Casorati G, Protti MP. (2006). Peptidome from renal cell carcinoma contains antigens recognized by CD4+ T cells and shared among tumors of different histology. Clin Cancer Res 12: 4949-4957
29. Thompson JA, Figlin RA, Sifri-Steele C, Berenson RJ, Frohlich MW. (2003). 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 9: 3562-3570
30. Tran KQ, Zhou J, Durflinger KH, Langhan MM, Shelton TE, Wunderlich JR, Robbins PF, Rosenberg SA, Dudley ME. (2008). Minimally cultured tumorinfiltrating lymphocytes display optimal characteristics for adoptive cell therapy. J Immunother 31: 742-751
31. Wang QJ, Hanada K, Robbins PF, Li YF, Yang JC. (2012). Distinctive features of the differentiated phenotype and infiltration of tumor-reactive lymphocytes in clear cell renal cell carcinoma. Cancer Res 72: 6119-6129
32. Yang S, Ji Y, Gattinoni L, Zhang L, Yu Z, Restifo NP, Rosenberg SA, Morgan RA. (2013). Modulating the differentiation status of ex vivo-cultured antitumor T cells using cytokine cocktails. Cancer Immunol Immunother 62: 727-736
33. Yannelli JR, Hyatt C, McConnell S, Hines K, Jacknin L, Parker L, Sanders M, Rosenberg SA. (1996). Growth of tumor-infiltrating lymphocytes from human solid cancers: summary of a 5-year experience. Int J Cancer 65: 413-421
34. Ye Q, Song DG, Poussin M, Yamamoto T, Best A, Li C, Coukos G, Powell Jr. DJ. (2014). CD137 accurately identifies and enriches for naturally occurring tumor-reactive T cells in tumor. Clin Cancer Res 20: 44-55