Attenuation of the glucocorticoid response during Ad5iL-12 adenovirus vector treatment enhances natural killer cell-mediated killing of MHC class I-negative LNCaP prostate tumors

Cancer Research

Volumn 67, Issue 5, 2007, Pages 2290-2297

  Gabaglia, Claudia Raja ^a   De Durana, Yaiza Diaz ^a   Graham, Frank L ^b   Gauldie, Jack ^b   Sercarz, Eli E ^a   Braciak, Todd A ^a  

^a TORREY PINES INSTITUTE FOR MOLECULAR STUDIES   (United States)

^b MCMASTER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; GLUCOCORTICOID; INTERLEUKIN 12; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MICA; MITOTANE; NATURAL KILLER CELL RECEPTOR NKG2D;

ADRENALECTOMY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; CARCINOGENESIS; CARCINOGENICITY; CELL ACTIVITY; CELL STRAIN LNCAP; CONTROLLED STUDY; DRUG MECHANISM; DRUG POTENTIATION; FLUORESCENCE ACTIVATED CELL SORTING; GENE TARGETING; GENETIC TRANSDUCTION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOSURVEILLANCE; IMMUNOTHERAPY; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROSTATE TUMOR; VIRUS STRAIN;

ADENOVIRIDAE; ANIMALS; ANTINEOPLASTIC AGENTS, HORMONAL; COMBINED MODALITY THERAPY; GENE THERAPY; GENES, MHC CLASS I; GENETIC VECTORS; HUMANS; HYDROCORTISONE; IMMUNITY, CELLULAR; IMMUNOTHERAPY; INTERLEUKIN-12; KILLER CELLS, NATURAL; MALE; MICE; MICE, INBRED NOD; MICE, SCID; MITOTANE; PROSTATIC NEOPLASMS; TUMOR CELLS, CULTURED; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 33947263159     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-06-3399     Document Type: Article

References (49)

1. Trinchieri G, Wysocka M, D'Andrea A, et al. Natural killer cell stimulatory factor (NKSF) or interleukin-12 is a key regulator of immune response and inflammation. Prog Growth Factor Res 1992;4:355-68.
2. Watanabe M, Fenton RG, Wigginton JM, et al. Intradermal delivery of IL-12 naked DNA induces systemic NK cell activation and Th1 response in vivo that is independent of endogenous IL-12 production. J Immunol 1999;163:1943-50.
3. Kim S, Iizuka K, Aguila HL, Weissman IL, Yokoyama WM. In vivo natural killer cell activities revealed by natural killer cell-deficient mice. Proc Natl Acad Sci U S A 2000;97:2731-6.
4. Moretta L, Moretta A. Unravelling natural killer cell function: triggering and inhibitory human NK receptors. EMBO J 2004;23:255-9.
5. Bauer S, Groh V, Wu J, et al. Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science 1999;285:727-9.
6. Groh V, Rhinehart R, Randolph-Habecker J, Topp MS, Riddell SR, Spies T. Costimulation of CD8αβ T cells by NKG2D via engagement by MIC induced on virus-infected cells. Nat Immunol 2001;2:255-60.
7. Jinushi M, Takehara T, Tatsumi T, et al. Expression and role of MICA and MICBin human hepatocellular carcinomas and their regulation by retinoic acid. Int J Cancer 2003;104:354-61.
8. Groh V, Bahram S, Bauer S, Herman A, Beauchamp M, Spies T. Cell stress-regulated human major histocompatibility complex class I gene expressed in gastrointestinal epithelium. Proc Natl Acad Sci U S A 1996; 93:12445-50.
9. Trinchieri G, Pflanz S, Kastelein RA. The IL-12 family of heterodimeric cytokines: new players in the regulation of T cell responses. Immunity 2003;19:641-4.
10. Trinchieri G. Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat Rev Immunol 2003;3:133-46.
11. Colombo MP, Trinchieri G. Interleukin-12 in antitumor immunity and immunotherapy. Cytokine Growth Factor Rev 2002;13:155-68.
12. Atkins MB, Robertson MJ, Gordon M, et al. Phase 1 evaluation of intravenous recombinant human interleukin 12 in patients with advanced malignancies. Clin Cancer Res 1997;3:409-17.
13. 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.
14. Sangro B, Mazzolini G, Ruiz J, et al. Phase I trial of intratumoral injection of an adenovirus encoding interleukin-12 for advanced digestive tumors. J Clin Oncol 2004;22:1389-97.
15. Mazzolini G, Prieto J, Melero I. Gene therapy of cancer with interleukin-12. Curr Pharm Des 2003;9:1981-91.
16. Gabaglia CR, Pedersen B, Hitt M, et al. A single intramuscular injection with an adenovirus-expressing IL-12 protects BALB/c mice against Leishmania major infection, while treatment with an IL-4-expressing vector increases disease susceptibility in B10.D2 mice. J Immunol 1999;162:753-60.
17. Gabaglia CR, Sercarz EE, Diaz-De-Durana Y, et al. Life-long systemic protection in mice vaccinated with L. major and adenovirus IL-12 vector requires active infection, macrophages and intact lymph nodes. Vaccine 2004;23:247-57.
18. Bramson JL, Hitt M, Addison CL, Muller WJ, Gauldie J, Graham FL. Direct intratumoral injection of an adenovirus expressing interleukin-12 induces regression and long-lasting immunity that is associated with highly localized expression of interleukin-12. Hum Gene Ther 1996;7:1995-2002.
19. Addison CL, Bramson JL, Hitt MM, Muller WJ, Gauldie J, Graham FL. Intratumoral coinjection of adenoviral vectors expressing IL-2 and IL-12 results in enhanced frequency of regression of injected and untreated distal tumors. Gene Ther 1998;5:1400-9.
20. Braciak TA, Mittal SK, Graham FL, Richards CD, Gauldie J. Construction of recombinant human type 5 adenoviruses expressing rodent IL-6 genes. An approach to investigate in vivo cytokine function. J Immunol 1993; 151:5145-53.
21. Addison CL, Braciak T, Ralston R, Muller WJ, Gauldie J, Graham FL. Intratumoral injection of an adenovirus expressing interleukin 2 induces regression and immunity in a murine breast cancer model. Proc Natl Acad Sci U S A 1995;92:8522-6.
22. Bramson JL, Hitt M, Gauldie J, Graham FL. Preexisting immunity to adenovirus does not prevent tumor regression following intratumoral administration of a vector expressing IL-12 but inhibits virus dissemination. Gene Ther 1997;4:1069-76.
23. Breuner CW, Jennings DH, Moore MC, Orchinik M. Pharmacological adrenalectomy with mitotane. Gen Comp Endocrinol 2000;120:27.
24. Hahner S, Fassnacht M. Mitotane for adrenocortical carcinoma treatment. Curr Opin Investig Drugs 2005;6:386-94.
25. Hitt MM, Addison CL, Graham FL. Human adenovirus vectors for gene transfer into mammalian cells. Adv Pharmacol 1997;40:137-206.
26. Shankaran V, Ikeda H, Bruce AT, et al. IFNγ and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature 2001;410:1107-11.
27. Sunamura M, Sun L, Lozonschi L, et al. The antiangiogenesis effect of interleukin 12 during early growth of human pancreatic cancer in SCID mice. Pancreas 2000;20:227-33.
28. Shultz LD, Schweitzer PA, Christianson SW, et al. Multiple defects in innate and adaptive immunologic function in NOD/LtSz-scid mice. J Immunol 1995; 154:180-91.
29. Callewaert DM, Moudgil VK, Radcliff G, Waite R. Hormone specific regulation of natural killer cells by cortisol. Direct inactivation of the cytotoxic function of cloned human NK cells without an effect on cellular proliferation. FEBS Lett 1991;285:108-10.
30. Liu Z, Guo BL, Gehrs BC, Nan L, Lopez RD. Ex vivo expanded human Vγ9Vδ2+ γδ-T cells mediate innate antitumor activity against human prostate cancer cells in vitro. J Urol 2005;173:1552-6.
31. Leitch J, Fraser K, Lane C, et al. CTL-dependent and -independent antitumor immunity is determined by the tumor not the vaccine. J Immunol 2004;172:5200-5.
32. Ayyoub M, Migliaccio M, Guillaume P, et al. Lack of tumor recognition by hTERT peptide 540-548-specific CD8(+) T cells from melanoma patients reveals inefficient antigen processing. Eur J Immunol 2001;31:2642-51.
33. Chang CC, Ogino T, Mullins DW, et al. Defective human leukocyte antigen class I-associated antigen presentation caused by a novel β2-microglobulin loss-of-function in melanoma cells. J Biol Chem 2006;281: 18763-73.
34. Gavioli R, Vertuani S, Masucci MG. Proteasome inhibitors reconstitute the presentation of cytotoxic T-cell epitopes in Epstein-Barr virus-associated tumors. Int J Cancer 2002;101:532-8.
35. Dunn GP, Bruce AT, Ikeda H, Old LJ, Schreiber RD. Cancer immunoediting: from immunosurveillance to tumor escape. Nat Immunol 2002;3:991-8.
36. Winter CC, Gumperz JE, Parham P, Long EO, Wagtmann N. Direct binding and functional transfer of NK cell inhibitory receptors reveal novel patterns of HLA-C allotype recognition. J Immunol 1998;161:571-7.
37. Parham P, McQueen KL. Alloreactive killer cells: hindrance and help for haematopoietic transplants. Nat Rev Immunol 2003;3:108-22.
38. Satoh M, Miyamura K, Yamada M, Ishidoya S, Childs RW, Arai Y. Haploidentical, non-myeloablative stem-cell transplantation for advanced renal-cell carcinoma. Lancet Oncol 2004;5:125-6.
39. Bucy RP. The effects of immunosuppressive pharmacological agents on the induction of cytotoxic and suppressor T lymphocytes in vitro. Immunopharmacology 1988;15:65-72.
40. de Jong EC, Vieira PL, Kalinski P, Kapsenberg ML. Corticosteroids inhibit the production of inflammatory mediators in immature monocyte-derived DC and induce the development of tolerogenic DC3. J Leukoc Biol 1999;66:201-4.
41. Nair MP, Schwartz SA. Immunomodulatory effects of corticosteroids on natural killer and antibody-dependent cellular cytotoxic activities of human lymphocytes. J Immunol 1984;132:2876-82.
42. Zhou J, Olsen S, Moldovan J, et al. Glucocorticoid regulation of natural cytotoxicity: effects of cortisol on the phenotype and function of a cloned human natural killer cell line. Cell Immunol 1997;178:108-16.
43. Cohen N, Mouly E, Hamdi H, et al. GILZ expression in human dendritic cells redirects their maturation and prevents antigen-specific T lymphocyte response. Blood 2006;107:2037-44.
44. Berrebi D, Bruscoli S, Cohen N, et al. Synthesis of glucocorticoid- induced leucine zipper (GILZ) by macrophages: an anti-inflammatory and immunosuppressive mechanism shared by glucocorticoids and IL 10. Blood 2003;101:729-38.
45. Russell ST, Tisdale MJ. The role of glucocorticoids in the induction of zinc-α2-glycoprotein expression in adipose tissue in cancer cachexia. Br J Cancer 2005; 92:876-81.
46. Groh V, Smythe K, Dai Z, Spies T. Fas ligand-mediated paracrine T cell regulation by the receptor NKG2D in tumor immunity. Nat Immunol 2006;7:755-62.
47. Galon J, Franchimont D, Hiroi N, et al. Gene profiling reveals unknown enhancing and suppressive actions of glucocorticoids on immune cells. FASEB J 2002;16:61-71.
48. Adam C, King S, Allgeier T, et al. DC-NK cell cross talk as a novel CD4+ T-cell-independent pathway for antitumor CTL induction. Blood 2005;106:338-44.
49. Kalinski P, Mailliard RB, Giermasz A, et al. Natural killer-dendritic cell crosstalk in cancer immunotherapy. Expert Opin Biol Ther 2005;5:1303-15.