Increased susceptibility to immune destruction of B16BL6 tumor cells engineered to express a novel pro-Smac fusion protein

Journal of Immunotherapy

Volumn 31, Issue 1, 2008, Pages 43-51

  Rüttinger, Dominik ^a   Li, Rui ^a   Poehlein, Christian H ^a   Haley, Dan ^a   Walker, Edwin B ^a   Hu, Hong Ming ^a,b   Fox, Bernard A ^a,b,c,d  

^a PROVIDENCE PORTLAND MEDICAL CENTER   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^d EARLE A CHILES RESEARCH INSTITUTE   (United States)

Author keywords

Adoptive immunotherapy; Cancer vaccines; Cellular immunotherapy; Effectors of apoptosis; Granzyme B; Smac

Indexed keywords

GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; INHIBITOR OF APOPTOSIS PROTEIN; PERFORIN; SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE; CARRIER PROTEIN; CASPASE 3; DIABLO PROTEIN, MOUSE; GRANZYME; GZMB PROTEIN, MOUSE; MITOCHONDRIAL PROTEIN; PERFORIN, MOUSE; PORE FORMING CYTOTOXIC PROTEIN; UNCLASSIFIED DRUG;

ADOPTIVE IMMUNOTHERAPY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOENGINEERING; CANCER CELL CULTURE; CELL DESTRUCTION; CELL KILLING; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; FEMALE; GENETIC CODE; MELANOMA CELL; MOLECULAR CLONING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SENSITIZATION; T LYMPHOCYTE; TUMOR CELL; WILD TYPE; ANIMAL; C57BL MOUSE; CYTOPLASM; CYTOTOXICITY TEST; DRUG EFFECT; EXPERIMENTAL MELANOMA; FLOW CYTOMETRY; GENETIC TRANSFECTION; GENETICS; IMMUNOLOGY; LUNG TUMOR; METABOLISM; METASTASIS; METHODOLOGY; MOUSE MUTANT; PATHOLOGY; TRANSPLANTATION; TUMOR CELL LINE; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CARRIER PROTEINS; CASPASE 3; CELL LINE, TUMOR; CYTOPLASM; CYTOTOXICITY TESTS, IMMUNOLOGIC; FEMALE; FLOW CYTOMETRY; GRANZYMES; GREEN FLUORESCENT PROTEINS; IMMUNOTHERAPY, ADOPTIVE; LUNG NEOPLASMS; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOCHONDRIAL PROTEINS; PORE FORMING CYTOTOXIC PROTEINS; RECOMBINANT FUSION PROTEINS; T-LYMPHOCYTES, CYTOTOXIC; TRANSFECTION;

EID: 40749129635     PISSN: 15249557     EISSN: None     Source Type: Journal    
DOI: 10.1097/CJI.0b013e318158fd16     Document Type: Article

References (49)

1. Kageshita T, Hirai S, Ono T, et al. Down-regulation of HLA class I antigen-processing molecules in malignant melanoma: association with disease progression. Am J Pathol. 1999;154:745-754.
2. Khong HT, Restifo NP. Natural selection of tumor variants in the generation of "tumor escape" phenotypes. Nat Immunol. 2002;3:999-1005.
3. Gajewski TF. Overcoming immune resistance in the tumor microenvironment by blockade of indoleamine 2,3-dioxygenase and programmed death ligand 1. Curr Opin Investig Drugs. 2004;5:1279-1283.
4. Ahmad M, Rees RC, Ali SA. Escape from immunotherapy: possible mechanisms that influence tumor regression/progression. Cancer Immunol Immunother. 2004;53:844-854.
5. Zou W. Immunosuppressive networks in the tumour environment and their therapeutic relevance. Nat Rev Cancer. 2005;5:263-274.
6. Campoli M, Ferrone S, Zea AH, et al. Mechanisms of tumor evasion. Cancer Treat Res. 2005;123:61-88.
7. Hersey P, Zhang XD. How melanoma cells evade trail-induced apoptosis. Nat Rev Cancer. 2001;1:142-150.
8. Ivanov VN, Bhoumik A, Ronai Z. Death receptors and melanoma resistance to apoptosis. Oncogene. 2003;22:3152-3161.
9. Lowin B, Hahne M, Mattmann C, et al. Cytolytic T-cell cytotoxicity is mediated through perforin and Fas lytic pathways. Nature. 1994;370:650-652.
10. Andrade F, Roy S, Nicholson D, et al. Granzyme B directly and efficiently cleaves several downstream caspase substrates: implications for CTL-induced apoptosis. Immunity. 1998;8:451-460.
11. MacDonald G, Shi L, Van de Velde C, et al. Mitochondria-dependent and independent regulation of Granzyme B-induced apoptosis. J Exp Med. 1999;189:131-144.
12. Pinkoski MJ, Heibein JA, Barry M, et al. Nuclear translocation of granzyme B in target cell apoptosis. Cell Death Differ. 2000;7:17-24.
13. Herr I, Debatin KM. Cellular stress response and apoptosis in cancer therapy. Blood. 2001;98:2603-2614.
14. Ambrosini G, Adida C, Altieri DC. A novel anti-apoptosis gene, survivin, expressed in cancer and lymphoma. Nat Med. 1997;3:917-921.
15. Wagenknecht B, Glaser T, Naumann U, et al. Expression and biological activity of X-linked inhibitor of apoptosis (XIAP) in human malignant glioma. Cell Death Differ. 1999;6:370-376.
16. Schimmer AD, Dalili S, Batey RA, et al. Targeting XIAP for the treatment of malignancy. Cell Death Differ. 2006;13:179-188.
17. Ravi R, Fuchs EJ, Jain A, et al. Resistance of cancers to immunologic cytotoxicity and adoptive immunotherapy via X-linked inhibitor of apoptosis protein expression and coexisting defects in mitochondrial death signaling. Cancer Res. 2006;66:1730-1739.
18. Du C, Fang M, Li Y, et al. Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell. 2000;102:33-42.
19. Verhagen AM, Ekert PG, Pakusch M, et al. Identification of DIABLO, a mammalian protein that promotes apoptosis by binding to and antagonizing IAP proteins. Cell. 2000;102:43-53.
20. Zhang XD, Zhang XY, Gray CP, et al. Tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis of human melanoma is regulated by smac/DIABLO release from mitochondria. Cancer Res. 2001;61:7339-7348.
21. Guo F, Nimmanapalli R, Paranawithana S, et al. Ectopic overexpression of second mitochondria-derived activator of caspases (Smac/DIABLO) or cotreatment with N-terminus of Smac/DIABLO peptide potentiates epothilone B derivative-(BMS 247550) and Apo-2L/TRAIL-induced apoptosis. Blood. 2002;99:3419-3426.
22. Fulda S, Wick W, Weller M, et al. Smac agonists sensitize for Apo2L/TRAIL- or anticancer drug-induced apoptosis and induce regression of malignant glioma in vivo. Nat Med. 2002;8:808-815.
23. Li L, Thomas RM, Suzuki H, et al. A small molecule Smac mimic potentiates TRAIL- and TNFalpha-mediated cell death. Science. 2004;305:1471-1474.
24. Li R, Rüttinger D, Urba WJ, et al. Targeting and amplification of immune killing of tumor cells by pro-Smac. Int J Cancer. 2004;109:85-94.
25. Arca MJ, Krauss JC, Aruga A, et al. Therapeutic efficacy of T cells derived from lymph nodes draining a poorly immunogenic tumor transduced to secrete granulocyte-macrophage colony-stimulating factor. Cancer Gene Ther. 1996;3:39-47.
26. Hu HM, Winter H, Urba WJ, et al. Divergent roles for CD4+ T cells in the priming and effector/memory phases of adoptive immunotherapy. J Immunol. 2000;165:4246-4253.
27. Winter H, Hu HM, Urba WJ, et al. Tumor regression after adoptive transfer of effector T cells is independent of perforin or Fas ligand (APO-1L/CD95L). J Immunol. 1999;163:4462-4472.
28. Talanian RV, Yang X, Turbov J, et al. Granule-mediated killing: pathways for granzyme B-initiated apoptosis. J Exp Med. 1997;186:1323-1331.
29. Poehlein CH, Hu HM, Yamada J, et al. TNF plays an essential role in tumor regression after adoptive transfer of perforin/ IFN-gamma double knockout effector T cells. J Immunol. 2003;170:2004-2013.
30. Medema JP, de Jong J, Peltenburg LT, et al. Blockade of the granzyme B/perforin pathway through overexpression of the serine protease inhibitor PI-9/SPI-6 constitutes a mechanism for immune escape by tumors. Proc Natl Acad Sci USA. 2001;98:11515-11520.
31. Soengas MS, Lowe SW. Apoptosis and melanoma chemoresistance. Oncogene. 2003;22:3138-3151.
32. Wright CW, Duckett CS. Reawakening the cellular death program in neoplasia through the therapeutic blockade of IAP function. J Clin Invest. 2005;115:2673-2678.
33. Deng Y, Lin Y, Wu X. TRAIL-induced apoptosis requires Bax-dependent mitochondrial release of Smac/DIABLO. Genes Dev. 2002;16:33-45.
34. Dass CR, Su T. Particle-mediated intravascular delivery of oligonucleotides to tumors: associated biology and lessons from genotherapy. Drug Deliv. 2001;8:191-213.
35. Dass CR, Walker TL, Kalle WH, et al. A microsphere-liposome (microplex) vector for targeted gene therapy of cancer. II. In vivo biodistribution study in a solid tumor model. Drug Deliv. 2000;7:15-19.
36. Dass CR, Burton MA. A model for evaluating selective delivery of plasmid DNA to tumours via the vasculature. Cancer Biother Radiopharm. 2002;17:501-505.
37. Wittmann S, Bali P, Donapaty S, et al. Flavopiridol down-regulates antiapoptotic proteins and sensitizes human breast cancer cells to epothilone B-induced apoptosis. Cancer Res. 2003;63:93-99.
38. Wall NR, O'Connor DS, Plescia J, et al. Suppression of survivin phosphorylation on Thr34 by flavopiridol enhances tumor cell apoptosis. Cancer Res. 2003;63:230-235.
39. Plenchette S, Cheung HH, Fong WG, et al. The role of XAF1 in cancer. Curr Opin Investig Drugs. 2007;8:469-476.
40. Hu Y, Cherton-Horvat G, Dragowska V, et al. Antisense oligonucleotides targeting XIAP induce apoptosis and enhance chemotherapeutic activity against human lung cancer cells in vitro and in vivo. Clin Cancer Res. 2003;9:2826-2836.
41. Fulda S, Debatin K-M. Extrinsic versus intrinsic apoptosis pathways in anticancer chemotherapy. Oncogene. 2006;25:4798-4811.
42. Cummings J, Ward TH, LaCasse E, et al. Validation of pharmacodynamic assays to evaluate the clinical efficacy of an antisense compound (AEG 35156) targeted to the X-linked inhibitor of apoptosis protein XIAP. Br J Cancer. 2005;92:532-538.
43. Dudley ME, Wunderlich JR, Yang JC, et al. Adoptive cell transfer therapy following non-myeloablative but lymphodepleting chemotherapy for the treatment of patients with refractory metastatic melanoma. J Clin Oncol. 2005;23:2346-2357.
44. Zhou J, Dudley ME, Rosenberg SA, et al. Persistence of multiple tumor-specific T-cell clones is associated with complete tumor regression in a melanoma patient receiving adoptive cell transfer therapy. J Immunother. 2005;28:53-62.
45. Rosenberg SA, Yang JC, Restifo NP. Cancer immunotherapy: moving beyond current vaccines. Nat Med. 2004;10:909-915.
46. Romero P, Cerottini JC, Speiser DE. Monitoring tumor antigen specific T-cell responses in cancer patients and phase I clinical trials of peptide-based vaccination. Cancer Immunol Immunother. 2004;53:249-255.
47. Lonchay C, van der Bruggen P, Connerotte T, et al. Correlation between tumor regression and T cell responses in melanoma patients vaccinated with a MAGE antigen. Proc Natl Acad Sci USA. 2004;101:14631-14638.
48. Lurquin C, Lethe B, De Plaen E, et al. Contrasting frequencies of antitumor and anti-vaccine T cells in metastases of a melanoma patient vaccinated with a MAGE tumor antigen. J Exp Med. 2005;201:249-257.
49. Ma J, Poehlein CH, Jensen SM, et al. Manipulating the host response to autologous tumour vaccines. Dev Biol (Basel). 2004;116:93-107; discussion 133-143.