Tumor-specific CD8+ T cells expressing interleukin-12 eradicate established cancers in lymphodepleted hosts

Cancer Research

Volumn 70, Issue 17, 2010, Pages 6725-6734

  Kerkar, Sid P ^a   Muranski, Pawel ^a   Kaiser, Andrew ^a   Boni, Andrea ^a   Sanchez Perez, Luis ^a   Yu, Zhiya ^a   Palmer, Douglas C ^a   Reger, Robert N ^a   Borman, Zachary A ^a   Zhang, Ling ^a   Morgan, Richard A ^a   Gattinoni, Luca ^a   Rosenberg, Steven A ^a   Trinchieri, Giorgio ^b   Restifo, Nicholas P ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 12; RECOMBINANT INTERLEUKIN 12; RETROVIRUS VECTOR; T BOX TRANSCRIPTION FACTOR; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR FOXP3;

ADOPTIVE TRANSFER; ANIMAL EXPERIMENT; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER REGRESSION; CD8+ T LYMPHOCYTE; CELL INFILTRATION; CELL MIGRATION; CELL TRANSFER; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG EFFICACY; DRUG MEGADOSE; FEMALE; GENETIC ENGINEERING; MELANOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; SPLEEN CELL; TUMOR MICROENVIRONMENT; ADOPTIVE IMMUNOTHERAPY; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; FLOW CYTOMETRY; GENETIC TRANSDUCTION; GENETICS; IMMUNOLOGY; MELANOMA, EXPERIMENTAL; METABOLISM; PROCEDURES; PROTEIN ENGINEERING; RETROVIRUS; TRANSGENIC MOUSE; TUMOR ASSOCIATED LEUKOCYTE;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; FEMALE; FLOW CYTOMETRY; IMMUNOTHERAPY, ADOPTIVE; INTERLEUKIN-12; LYMPHOCYTES, TUMOR-INFILTRATING; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PROTEIN ENGINEERING; RETROVIRIDAE; TRANSDUCTION, GENETIC;

EID: 77956280888     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-10-0735     Document Type: Article

References (50)

1. + T cell cytotoxic activity during adoptive T cell therapy in mice. J Clin Invest 2008;118:1390-7.
2. Boissonnas A, Fetler L, Zeelenberg IS, Hugues S, Amigorena S. In vivo imaging of cytotoxic T cell infiltration and elimination of a solid tumor. J Exp Med 2007;204:345-56.
3. Marigo I, Dolcetti L, Serafini P, Zanovello P, Bronte V. Tumor-induced tolerance and immune suppression by myeloid derived suppressor cells. Immunol Rev 2008;222:162-79. (Pubitemid 351430364)
4. Hwu P, Du MX, Lapointe R, Do M, Taylor MW, Young HA. Indoleamine 2,3-dioxygenase production by human dendritic cells results in the inhibition of T cell proliferation. J Immunol 2000;164:3596-9.
5. Srivastava MK, Sinha P, Clements VK, Rodriguez P, Ostrand- Rosenberg S. Myeloid-derived suppressor cells inhibit T-cell activation by depleting cystine and cysteine. Cancer Res 2010;70:68-77.
6. Gabrilovich DI, Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 2009;9:162-74.
7. + cells. J Immunol 1998;161:5313-20.
8. Zhang B, Bowerman NA, Salama JK, et al. Induced sensitization of tumor stroma leads to eradication of established cancer by T cells. J Exp Med 2007;204:49-55.
9. Drake CG, Jaffee E, Pardoll DM. Mechanisms of immune evasion by tumors. Adv Immunol 2006;90:51-81.
10. Zou W. Immunosuppressive networks in the tumour environment and their therapeutic relevance. Nat Rev Cancer 2005;5:263-74. (Pubitemid 40488632)
11. Kobayashi M, Fitz L, Ryan M, et al. Identification and purification of natural killer cell stimulatory factor (NKSF), a cytokine with multiple biologic effects on human lymphocytes. J Exp Med 1989;170:827-45.
12. Colombo MP, Trinchieri G. Interleukin-12 in anti-tumor immunity and immunotherapy. Cytokine Growth Factor Rev 2002;13:155-68.
13. Gerosa F, Paganin C, Peritt D, et al. Interleukin-12 primes human CD4 and CD8 T cell clones for high production of both interferon-γ and interleukin-10. J Exp Med 1996;183:2559-69.
14. + T cells through IL-12 produced by Listeria-induced macrophages. Science 1993;260:547-9.
15. Manetti R, Gerosa F, Giudizi MG, et al. Interleukin 12 induces stable priming for interferon γ (IFN-γ) production during differentiation of human T helper (Th) cells and transient IFN-γ production in established Th2 cell clones. J Exp Med 1994;179:1273-83.
16. Mitola S, Strasly M, Prato M, Ghia P, Bussolino F. IL-12 regulates an endothelial cell-lymphocyte network: effect on metalloproteinase-9 production. J Immunol 2003;171:3725-33. (Pubitemid 37264926)
17. Ogawa M, Yu WG, Umehara K, et al. Multiple roles of interferon-γ in the mediation of interleukin 12-induced tumor regression. Cancer Res 1998;58:2426-32.
18. Strasly M, Cavallo F, Geuna M, et al. IL-12 inhibition of endothelial cell functions and angiogenesis depends on lymphocyte-endothelial cell cross-talk. J Immunol 2001;166:3890-9.
19. Szabo SJ, Sullivan BM, Stemmann C, Satoskar AR, Sleckman BP, Glimcher LH. Distinct effects of T-bet in TH1 lineage commitment and IFN-γ production in CD4 and CD8 T cells. Science 2002;295:338-42.
20. Voest EE, Kenyon BM, O'Reilly MS, Truitt G, D'Amato RJ, Folkman J. Inhibition of angiogenesis in vivo by interleukin 12. J Natl Cancer Inst 1995;87:581-6.
21. Brunda MJ, Luistro L, Warrier RR, et al. Antitumor and antimetastatic activity of interleukin 12 against murine tumors. J Exp Med 1993;178: 1223-30.
22. Markiewicz MA, Wise EL, Buchwald ZS, et al. IL-12 enhances CTL synapse formation and induces self-reactivity. J Immunol 2009;182: 1351-61.
23. Smyth MJ, Taniguchi M, Street SE. The anti-tumor activity of IL-12: mechanisms of innate immunity that are model and dose dependent. J Immunol 2000;165:2665-70. (Pubitemid 30660715)
24. Weiss JM, Subleski JJ, Wigginton JM, Wiltrout RH. Immunotherapy of cancer by IL-12-based cytokine combinations. Expert Opin Biol Ther 2007;7:1705-21.
25. Wigginton JM, Wiltrout RH. IL-12/IL-2 combination cytokine therapy for solid tumours: translation from bench to bedside. Expert Opin Biol Ther 2002;2:513-24.
26. Zitvogel L, Tahara H, Robbins PD, et al. Cancer immunotherapy of established tumors with IL-12. Effective delivery by genetically engineered fibroblasts. J Immunol 1995;155:1393-403.
27. Curti A, Parenza M, Colombo MP. Autologous and MHC class I-negative allogeneic tumor cells secreting IL-12 together cure disseminated A20 lymphoma. Blood 2003;101:568-75.
28. Kang WK, Park C, Yoon HL, et al. Interleukin 12 gene therapy of cancer by peritumoral injection of transduced autologous fibroblasts: outcome of a phase I study. Hum Gene Ther 2001;12:671-84.
29. van Herpen CM, van der Laak JA, de Vries IJ, et al. Intratumoral recombinant human interleukin-12 administration in head and neck squamous cell carcinoma patients modifies locoregional lymph node architecture and induces natural killer cell infiltration in the primary tumor. Clin Cancer Res 2005;11:1899-909.
30. Rook AH, Wood GS, Yoo EK, et al. Interleukin-12 therapy of cutaneous T-cell lymphoma induces lesion regression and cytotoxic T-cell responses. Blood 1999;94:902-8.
31. Tahara H, Zitvogel L, Storkus WJ, et al. Effective eradication of established murine tumors with IL-12 gene therapy using a polycistronic retroviral vector. J Immunol 1995;154:6466-74.
32. Tatsumi T, Huang J, Gooding WE, et al. Intratumoral delivery of dendritic cells engineered to secrete both interleukin (IL)-12 and IL-18 effectively treats local and distant disease in association with broadly reactive Tc1-type immunity. Cancer Res 2003;63:6378-86.
33. Mazzolini G, Alfaro C, Sangro B, et al. Intratumoral injection of dendritic cells engineered to secrete interleukin-12 by recombinant adenovirus in patients with metastatic gastrointestinal carcinomas. J Clin Oncol 2005;23:999-1010.
34. Rodolfo M, Colombo MP. Interleukin-12 as an adjuvant for cancer immunotherapy. Methods 1999;19:114-20.
35. + T cells. J Exp Med 2003;198:569-80.
36. + T cells. J Exp Med 2005;202:907-12.
37. + T cells mediate superior antitumor immunity. Proc Natl Acad Sci U S A 2009; 106:17469-74.
38. + memory stem cells. Nat Med 2009;15:808-13.
39. Hughes MS, Yu YY, Dudley ME, et al. Transfer of a TCR gene derived from a patient with a marked antitumor response conveys highly active T-cell effector functions. Hum Gene Ther 2005;16:457-72.
40. Anderson R, Macdonald I, Corbett T, Hacking G, Lowdell MW, Prentice HG. Construction and biological characterization of an interleukin-12 fusion protein (Flexi-12): delivery to acute myeloid leukemic blasts using adeno-associated virus. Hum Gene Ther 1997;8: 1125-35. (Pubitemid 27308210)
41. Lieschke GJ, Rao PK, Gately MK, Mulligan RC. Bioactive murine and human interleukin-12 fusion proteins which retain antitumor activity in vivo. Nat Biotechnol 1997;15:35-40. (Pubitemid 127747490)
42. Wagner HJ, Bollard CM, Vigouroux S, et al. A strategy for treatment of Epstein-Barr virus-positive Hodgkin's disease by targeting interleukin 12 to the tumor environment using tumor antigen-specific T cells. Cancer Gene Ther 2004;11:81-91.
43. + T cell differentiation. J Immunol 2006;177:7515-9.
44. Leonard JP, Sherman ML, Fisher GL, et al. Effects of single-dose interleukin-12 exposure on interleukin-12-associated toxicity and interferon-γ production. Blood 1997;90:2541-8.
45. + T cells via TLR4 signaling. J Clin Invest 2007; 117:2197-204.
46. + T helper cells and hindered by naturally occurring T regulatory cells. J Immunol 2005;174:2591-601.
47. Wrzesinski C, Paulos CM, Kaiser A, et al. Increased intensity lymphodepletion enhances tumor treatment efficacy of adoptively transferred tumor-specific T cells. J Immunother 33:1-7.
48. Dudley ME, Yang JC, Sherry R, et al. Adoptive cell therapy for patients with metastatic melanoma: evaluation of intensive myeloablative chemoradiation preparative regimens. J Clin Oncol 2008;26: 5233-9.
49. Rossig C, Brenner MK. Genetic modification of T lymphocytes for adoptive immunotherapy. Mol Ther 2004;10:5-18. (Pubitemid 38878144)
50. Bendle GM, Linnemann C, Hooijkaas AI, et al. Lethal graft-versus-host disease in mouse models of T cell receptor gene therapy. Nat Med 16:565-70, 1p following 70.