In vivo proof of concept of adoptive immunotherapy for hepatocellular carcinoma using allogeneic suicide gene-modified killer cells

Molecular Therapy

Volumn 22, Issue 3, 2014, Pages 634-644

  Leboeuf, Céline ^a,b,j   Mailly, Laurent ^a,b   Wu, Tao ^a,b,c   Bour, Gaetan ^d   Durand, Sarah ^a,b   Brignon, Nicolas ^a,b   Ferrand, Christophe ^e,f,g   Borg, Christophe ^e,f,g   Tiberghien, Pierre ^e,f,g   Thimme, Robert ^h   Pessaux, Patrick ^a,b,i   Marescaux, Jacques ^b,d,i   Baumert, Thomas F ^a,b,i   Robinet, Eric ^a,b  

^a INSERM   (France)

^b UNIVERSITÉ DE STRASBOURG   (France)

^c KUNMING MEDICAL UNIVERSITY   (China)

^d IRCAD   (France)

^e ETABLISSEMENT FRANÇAIS DU SANG   (France)

^f France   (France)

^g UNIVERSITÉ DE FRANCHE COMTÉ   (France)

^h UNIVERSITY OF FREIBURG   (Germany)

ⁱ HÔPITAL CIVIL   (France)

^j UNIVERSITY OF BASEL   (Switzerland)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOSPORIN A; INTERLEUKIN 2; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1;

ALLOGENEIC SUICIDE GENE MODIFIED KILLER CELL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER IMMUNOTHERAPY; CELL ISOLATION; CELL THERAPY; CLINICAL EFFECTIVENESS; CONTROLLED STUDY; CYTOTOXICITY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; KILLER CELL; LIVER CELL CARCINOMA; MOUSE; NATURAL KILLER CELL; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PHENOTYPE; SAFETY; THERAPY EFFECT; TUMOR REJECTION;

ANIMALIA; MURINAE;

ANIMALS; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; CYTOTOXICITY, IMMUNOLOGIC; HELA CELLS; HUMANS; IMMUNOTHERAPY, ADOPTIVE; LIVER NEOPLASMS; MICE; MICE, INBRED C57BL; MICE, SCID; NEOPLASM TRANSPLANTATION; T-LYMPHOCYTES; TRANSPLANTATION, HOMOLOGOUS;

EID: 84895475681     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2013.277     Document Type: Article

References (38)

1. Thomas, MB, Jaffe, D, Choti, MM, Belghiti, J, Curley, S, Fong, Y et al. (2010). Hepatocellular carcinoma: consensus recommendations of the National Cancer Institute Clinical Trials Planning Meeting. J Clin Oncol 28: 3994-4005.
2. Padhya, KT, Marrero, JA and Singal, AG (2013). Recent advances in the treatment of hepatocellular carcinoma. Curr Opin Gastroenterol 29: 285-292.
3. El-Serag, HB, Marrero, JA, Rudolph, L and Reddy, KR (2008). Diagnosis and treatment of hepatocellular carcinoma. Gastroenterology 134: 1752-1763.
4. Brenner, MK and Heslop, HE (2010). Adoptive T cell therapy of cancer. Curr Opin Immunol 22: 251-257.
5. Velardi, A, Ruggeri, L, Mancusi, A, Aversa, F and Christiansen, FT (2009). Natural killer cell allorecognition of missing self in allogeneic hematopoietic transplantation: a tool for immunotherapy of leukemia. Curr Opin Immunol 21: 525-530.
6. Welniak, LA, Blazar, BR and Murphy, WJ (2007). Immunobiology of allogeneic hematopoietic stem cell transplantation. Annu Rev Immunol 25: 139-170.
7. Mailly, L, Leboeuf, C, Tiberghien, P, Baumert, T and Robinet, E (2010). Genetically engineered T-cells expressing a ganciclovir-sensitive HSV-tk suicide gene for the prevention of GvHD. Curr Opin Investig Drugs 11: 559-570.
8. Di Stasi, A, Tey, SK, Dotti, G, Fujita, Y, Kennedy-Nasser, A, Martinez, C et al. (2011). Inducible apoptosis as a safety switch for adoptive cell therapy. N Engl J Med 365: 1673-1683.
9. Tiberghien, P, Ferrand, C, Lioure, B, Milpied, N, Angonin, R, Deconinck, E et al. (2001). Administration of herpes simplex-thymidine kinase-expressing donor T cells with a T-cell-depleted allogeneic marrow graft. Blood 97: 63-72.
10. Bonini, C, Ferrari, G, Verzeletti, S, Servida, P, Zappone, E, Ruggieri, L et al. (1997). HSV-TK gene transfer into donor lymphocytes for control of allogeneic graft-versusleukemia. Science 276: 1719-1724.
11. Sauce, D, Tonnelier, N, Duperrier, A, Petracca, B, de Carvalho Bittencourt, M, Saadi, M et al. (2002). Influence of ex vivo expansion and retrovirus-mediated gene transfer on primary T lymphocyte phenotype and functions. J Hematother Stem Cell Res 11: 929-940.
12. Coito, S, Sauce, D, Duperrier, A, Certoux, JM, Bonyhadi, M, Collette, A et al. (2004). Retrovirus-mediated gene transfer in human primary T lymphocytes induces an activation- and transduction/selection-dependent TCR-B variable chain repertoire skewing of gene-modified cells. Stem Cells Dev 13: 71-81.
13. Marktel, S, Magnani, Z, Ciceri, F, Cazzaniga, S, Riddell, SR, Traversari, C et al. (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.
14. Mercier-Letondal, P, Montcuquet, N, Sauce, D, Certoux, JM, Jeanningros, S, Ferrand, C et al. (2008). Alloreactivity of ex vivo-expanded T cells is correlated with expansion and CD4/CD8 ratio. Cytotherapy 10: 275-288.
15. Montcuquet, N, Mercier-Letondal, P, Perruche, S, Duperrier, A, Couturier, M, Bouchekioua, A et al. (2008). Regulatory T-cell expansion and function do not account for the impaired alloreactivity of ex vivo-expanded T cells. Immunology 125: 320-330.
16. Contassot, E, Murphy, W, Angonin, R, Pavy, JJ, Bittencourt, MC, Robinet, E et al. (1998). In vivo alloreactive potential of ex vivo-expanded primary T lymphocytes. Transplantation 65: 1365-1370.
17. van Rijn, RS, Simonetti, ER, Hagenbeek, A, Bonyhadi, M, Storm, G, Martens, AC et al. (2007). Quantitative assessment of human T lymphocytes in RAG2(-/-)gammac(-/-) mice: the impact of ex vivo manipulation on in vivo functionality. Exp Hematol 35: 117-127.
18. Contassot, E, Robinet, E, Angonin, R, Laithier, V, Bittencourt, M, Pavy, JJ et al. (1998). Differential effects of cyclosporin A on the alloreactivity of fresh and ex vivo-expanded T lymphocytes. Bone Marrow Transplant 22: 1097-1102.
19. Marin, V, Cribioli, E, Philip, B, Tettamanti, S, Pizzitola, I, Biondi, A et al. (2012). Comparison of different suicide-gene strategies for the safety improvement of genetically manipulated T cells. Hum Gene Ther Methods 23: 376-386.
20. Paczesny, S, Hanauer, D, Sun, Y and Reddy, P (2010). New perspectives on the biology of acute GVHD. Bone Marrow Transplant 45: 1-11.
21. Sun, FX, Tang, ZY, Liu, KD, Xue, Q, Gao, DM, Yu, YQ et al. (1996). Metastatic models of human liver cancer in nude mice orthotopically constructed by using histologically intact patient specimens. J Cancer Res Clin Oncol 122: 397-402.
22. Haque, T, Wilkie, GM, Taylor, C, Amlot, PL, Murad, P, Iley, A et al. (2002). Treatment of Epstein-Barr-virus-positive post-transplantation lymphoproliferative disease with partly HLA-matched allogeneic cytotoxic T cells. Lancet 360: 436-442.
23. Haque, T, Wilkie, GM, Jones, MM, Higgins, CD, Urquhart, G, Wingate, P et al. (2007). Allogeneic cytotoxic T-cell therapy for EBV-positive posttransplantation lymphoproliferative disease: results of a phase 2 multicenter clinical trial. Blood 110: 1123-1131.
24. Slavin, S, Ackerstein, A, Or, R, Shapira, MY, Gesundheit, B, Askenasy, N et al. (2010). Immunotherapy in high-risk chemotherapy-resistant patients with metastatic solid tumors and hematological malignancies using intentionally mismatched donor lymphocytes activated with rIL-2: a phase I study. Cancer Immunol Immunother 59: 1511-1519.
25. Hambach, L, Vermeij, M, Buser, A, Aghai, Z, van der Kwast, T and Goulmy, E (2008). Targeting a single mismatched minor histocompatibility antigen with tumor-restricted expression eradicates human solid tumors. Blood 112: 1844-1852.
26. Schmidt-Wolf, IG, Lefterova, P, Mehta, BA, Fernandez, LP, Huhn, D, Blume, KG et al. (1993). Phenotypic characterization and identification of effector cells involved in tumor cell recognition of cytokine-induced killer cells. Exp Hematol 21: 1673-1679.
27. Kim, HM, Lim, J, Yoon, YD, Ahn, JM, Kang, JS, Lee, K et al. (2007). Anti-tumor activity of ex vivo expanded cytokine-induced killer cells against human hepatocellular carcinoma. Int Immunopharmacol 7: 1793-1801.
28. Wang, FS, Liu, MX, Zhang, B, Shi, M, Lei, ZY, Sun, WB et al. (2002). Antitumor activities of human autologous cytokine-induced killer (CIK) cells against hepatocellular carcinoma cells in vitro and in vivo. World J Gastroenterol 8: 464-468.
29. Nishimura, R, Baker, J, Beilhack, A, Zeiser, R, Olson, JA, Sega, EI et al. (2008). In vivo trafficking and survival of cytokine-induced killer cells resulting in minimal GVHD with retention of antitumor activity. Blood 112: 2563-2574.
30. Takayama, T, Sekine, T, Makuuchi, M, Yamasaki, S, Kosuge, T, Yamamoto, J et al. (2000). Adoptive immunotherapy to lower postsurgical recurrence rates of hepatocellular carcinoma: a randomised trial. Lancet 356: 802-807.
31. Weng, DS, Zhou, J, Zhou, QM, Zhao, M, Wang, QJ, Huang, LX et al. (2008). Minimally invasive treatment combined with cytokine-induced killer cells therapy lower the shortterm recurrence rates of hepatocellular carcinomas. J Immunother 31: 63-71.
32. Horowitz, MM, Gale, RP, Sondel, PM, Goldman, JM, Kersey, J, Kolb, HJ et al. (1990). Graft-versus-leukemia reactions after bone marrow transplantation. Blood 75: 555-562.
33. Ciceri, F, Bonini, C, Marktel, S, Zappone, E, Servida, P, Bernardi, M et al. (2007). Antitumor effects of HSV-TK-engineered donor lymphocytes after allogeneic stem-cell transplantation. Blood 109: 4698-4707.
34. Introna, M, Borleri, G, Conti, E, Franceschetti, M, Barbui, AM, Broady, R et al. (2007). Repeated infusions of donor-derived cytokine-induced killer cells in patients relapsing after allogeneic stem cell transplantation: a phase I study. Haematologica 92: 952-959.
35. Fehse, B, Kustikova, OS, Li, Z, Wahlers, A, Bohn, W, Beyer, WR et al. (2002). A novel 'sort-suicide' fusion gene vector for T cell manipulation. Gene Ther 9: 1633-1638.
36. Roth, P, Hammer, C, Piguet, AC, Ledermann, M, Dufour, JF and Waelti, E (2007). Effects on hepatocellular carcinoma of doxorubicin-loaded immunoliposomes designed to target the VEGFR-2. J Drug Target 15: 623-631.
37. Kruschinski, A, Moosmann, A, Poschke, I, Norell, H, Chmielewski, M, Seliger, B et al. (2008). Engineering antigen-specific primary human NK cells against HER-2 positive carcinomas. Proc Natl Acad Sci USA 105: 17481-17486.
38. Cooke, KR, Kobzik, L, Martin, TR, Brewer, J, Delmonte, J Jr, Crawford, JM et al. (1996). An experimental model of idiopathic pneumonia syndrome after bone marrow transplantation: I. The roles of minor H antigens and endotoxin. Blood 88: 3230-3239.