A novel inhibitor of proteasome deubiquitinating activity renders tumor cells sensitive to TRAIL-mediated apoptosis by natural killer cells and T cells

Cancer Immunology, Immunotherapy

Volumn 62, Issue 8, 2013, Pages 1359-1368

  Sarhan, Dhifaf ^a   Wennerberg, Erik ^a   D'Arcy, Padraig ^a   Gurajada, Deepthy ^a   Linder, Stig ^a   Lundqvist, Andreas ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Immunotherapy; Natural killer cells; Proteasome inhibitor; T cells; TRAIL

Indexed keywords

3,5 BIS[(4 NITROPHENYL)METHYLIDENE] 1 PROP 2 ENOYLPIPERIDIN 4 ONE; B AP15; DEATH RECEPTOR 5; FLICE INHIBITORY PROTEIN; PROTEASOME INHIBITOR; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNCLASSIFIED DRUG;

ADOPTIVE IMMUNOTHERAPY; ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER IMMUNOTHERAPY; CANCER INHIBITION; CELL MEDIATED CYTOTOXICITY; CONTROLLED STUDY; HUMAN; HUMAN CELL; LONG TERM SURVIVAL; MOUSE; NATURAL KILLER CELL; NEOPLASM; NONHUMAN; PRIORITY JOURNAL; SURVIVAL TIME; T LYMPHOCYTE; TUMOR CELL;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CELL LINE, TUMOR; CELLS, CULTURED; COMBINED MODALITY THERAPY; CYTOKINES; CYTOTOXICITY, IMMUNOLOGIC; HCT116 CELLS; HELA CELLS; HUMANS; IMMUNOTHERAPY, ADOPTIVE; K562 CELLS; KILLER CELLS, NATURAL; MCF-7 CELLS; MICE; MICE, INBRED BALB C; MICE, SCID; NEOPLASMS; PIPERIDONES; PROTEASE INHIBITORS; PROTEASOME ENDOPEPTIDASE COMPLEX; T-LYMPHOCYTES; TNF-RELATED APOPTOSIS-INDUCING LIGAND; UBIQUITINATION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84880910575     PISSN: 03407004     EISSN: 14320851     Source Type: Journal    
DOI: 10.1007/s00262-013-1439-1     Document Type: Article

References (32)

1. 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(13):4550-4557
2. June CH (2007) Adoptive T cell therapy for cancer in the clinic. J Clin Invest 117(6):1466-1476
3. Parkhurst MR, Riley JP, Dudley ME, Rosenberg SA (2011) Adoptive transfer of autologous natural killer cells leads to high levels of circulating natural killer cells but does not mediate tumor regression. Clin Cancer Res 17(19):6287-6297
4. Bubenik J (2003) Tumour MHC class I downregulation and immunotherapy (Review). Oncol Rep 10(6):2005-2008
5. Marincola FM, Jaffee EM, Hicklin DJ, Ferrone S (2000) Escape of human solid tumors from T-cell recognition: molecular mechanisms and functional significance. Adv Immunol 74:181-273
6. Al-Batran SE, Rafiyan MR, Atmaca A, Neumann A, Karbach J, Bender A, Weidmann E, Altmannsberger HM, Knuth A, Jager E (2005) Intratumoral T-cell infiltrates and MHC class I expression in patients with stage IV melanoma. Cancer Res 65(9):3937-3941
7. Milstein O, Hagin D, Lask A, Reich-Zeliger S, Shezen E, Ophir E, Eidelstein Y, Afik R, Antebi YE, Dustin ML, Reisner Y (2011) CTLs respond with activation and granule secretion when serving as targets for T-cell recognition. Blood 117(3):1042-1052
8. Arancia G, Malorni W, Donelli G (1990) Cellular mechanisms of lymphocyte-mediated lysis of tumor cells. Ann Ist Super Sanita 26(3-4):369-384
9. Jenne DE, Tschopp J (1988) Granzymes, a family of serine proteases released from granules of cytolytic T lymphocytes upon T cell receptor stimulation. Immunol Rev 103:53-71
10. Berke G (1994) The binding and lysis of target cells by cytotoxic lymphocytes: molecular and cellular aspects. Annu Rev Immunol 12:735-773
11. Yong AS, Keyvanfar K, Hensel N, Eniafe R, Savani BN, Berg M, Lundqvist A, Adams S, Sloand EM, Goldman JM, Childs R, Barrett AJ (2009) Primitive quiescent CD34 + cells in chronic myeloid leukemia are targeted by in vitro expanded natural killer cells, which are functionally enhanced by bortezomib. Blood 113(4):875-882
12. Liu X, Yue P, Chen S, Hu L, Lonial S, Khuri FR, Sun SY (2007) The proteasome inhibitor PS-341 (bortezomib) up-regulates DR5 expression leading to induction of apoptosis and enhancement of TRAIL-induced apoptosis despite up-regulation of c-FLIP and survivin expression in human NSCLC cells. Cancer Res 67(10):4981-4988
13. Shanker A, Brooks AD, Tristan CA, Wine JW, Elliott PJ, Yagita H, Takeda K, Smyth MJ, Murphy WJ, Sayers TJ (2008) Treating metastatic solid tumors with bortezomib and a tumor necrosis factor-related apoptosis-inducing ligand receptor agonist antibody. J Natl Cancer Inst 100(9):649-662
14. Lundqvist A, Su S, Rao S, Childs R (2010) Cutting edge: bortezomib-treated tumors sensitized to NK cell apoptosis paradoxically acquire resistance to antigen-specific T cells. J Immunol 184(3):1139-1142
15. Baumann P, Muller K, Mandl-Weber S, Leban J, Doblhofer R, Ammendola A, Baumgartner R, Oduncu F, Schmidmaier R (2009) The peptide-semicarbazone S-2209, a representative of a new class of proteasome inhibitors, induces apoptosis and cell growth arrest in multiple myeloma cells. Br J Haematol 144(6):875-886
16. D'Arcy P, Brnjic S, Olofsson MH, Fryknas M, Lindsten K, De Cesare M, Perego P, Sadeghi B, Hassan M, Larsson R, Linder S (2011) Inhibition of proteasome deubiquitinating activity as a new cancer therapy. Nat Med 17(12):1636-1640
17. Kang YJ, Kim IY, Kim EH, Yoon MJ, Kim SU, Kwon TK, Choi KS (2011) Paxilline enhances TRAIL-mediated apoptosis of glioma cells via modulation of c-FLIP, survivin and DR5. Exp Mol Med 43(1):24-34
18. Moon MH, Jeong JK, Seo JS, Seol JW, Lee YJ, Xue M, Jackson CJ, Park SY (2011) Bisphosphonate enhances TRAIL sensitivity to human osteosarcoma cells via death receptor 5 upregulation. Exp Mol Med 43(3):138-145
19. Lundqvist A, Abrams SI, Schrump DS, Alvarez G, Suffredini D, Berg M, Childs R (2006) Bortezomib and depsipeptide sensitize tumors to tumor necrosis factor-related apoptosis-inducing ligand: a novel method to potentiate natural killer cell tumor cytotoxicity. Cancer Res 66(14):7317-7325
20. Jazirehi AR, Economou JS (2012) Proteasome inhibition blocks NF-kappaB and ERK1/2 pathways, restores antigen expression, and sensitizes resistant human melanoma to TCR-engineered CTLs. Mol Cancer Ther 11(6):1332-1341
21. Zhao X, Qiu W, Kung J, Peng X, Yegappan M, Yen-Lieberman B, Hsi ED (2008) Bortezomib induces caspase-dependent apoptosis in Hodgkin lymphoma cell lines and is associated with reduced c-FLIP expression: a gene expression profiling study with implications for potential combination therapies. Leuk Res 32(2):275-285
22. White SJ, Lu P, Keller GM, Voelkel-Johnson C (2006) Targeting the short form of cFLIP by RNA interference is sufficient to enhance TRAIL sensitivity in PC3 prostate carcinoma cells. Cancer Biol Ther 5(12):1618-1623
23. Ganten TM, Koschny R, Haas TL, Sykora J, Li-Weber M, Herzer K, Walczak H (2005) Proteasome inhibition sensitizes hepatocellular carcinoma cells, but not human hepatocytes, to TRAIL. Hepatology 42(3):588-597
24. Hallett WH, Ames E, Motarjemi M, Barao I, Shanker A, Tamang DL, Sayers TJ, Hudig D, Murphy WJ (2008) Sensitization of tumor cells to NK cell-mediated killing by proteasome inhibition. J Immunol 180(1):163-170
25. Trivedi PP, Roberts PC, Wolf NA, Swanborg RH (2005) NK cells inhibit T cell proliferation via p21-mediated cell cycle arrest. J Immunol 174(8):4590-4597
26. Olson JA, Leveson-Gower DB, Gill S, Baker J, Beilhack A, Negrin RS (2010) NK cells mediate reduction of GVHD by inhibiting activated, alloreactive T cells while retaining GVT effects. Blood 115(21):4293-4301
27. Wang XJ, Hu J, Yuan J, Peng YM, Gui L, He WF, Tan J, Luo GX, Wu J (2009) Activated T cells inhibit NK cell-mediated tumour rejection. Scand J Immunol 69(4):337-341
28. Soria JC, Smit E, Khayat D, Besse B, Yang X, Hsu CP, Reese D, Wiezorek J, Blackhall F (2010) Phase 1b study of dulanermin (recombinant human Apo2L/TRAIL) in combination with paclitaxel, carboplatin, and bevacizumab in patients with advanced non-squamous non-small-cell lung cancer. J Clin Oncol 28(9):1527-1533
29. Mom CH, Verweij J, Oldenhuis CN, Gietema JA, Fox NL, Miceli R, Eskens FA, Loos WJ, de Vries EG, Sleijfer S (2009) Mapatumumab, a fully human agonistic monoclonal antibody that targets TRAIL-R1, in combination with gemcitabine and cisplatin: a phase I study. Clin Cancer Res 15(17):5584-5590
30. Leong S, Cohen RB, Gustafson DL, Langer CJ, Camidge DR, Padavic K, Gore L, Smith M, Chow LQ, von Mehren M, O'Bryant C, Hariharan S, Diab S, Fox NL, Miceli R, Eckhardt SG (2009) Mapatumumab, an antibody targeting TRAIL-R1, in combination with paclitaxel and carboplatin in patients with advanced solid malignancies: results of a phase I and pharmacokinetic study. J Clin Oncol 27(26):4413-4421
31. Duiker EW, Mom CH, de Jong S, Willemse PH, Gietema JA, van der Zee AG, de Vries EG (2006) The clinical trail of TRAIL. Eur J Cancer 42(14):2233-2240
32. Huang J, Khong HT, Dudley ME, El-Gamil M, Li YF, Rosenberg SA, Robbins PF (2005) Survival, persistence, and progressive differentiation of adoptively transferred tumor-reactive T cells associated with tumor regression. J Immunother 28(3):258-267