Bone marrow stroma confers resistance to Apo2 ligand/TRAIL in multiple myeloma in part by regulating c-FLIP

Journal of Immunology

Volumn 180, Issue 3, 2008, Pages 1545-1555

  Perez, Lia Elena ^a,c   Parquet, Nancy ^a   Shain, Kenneth ^a   Nimmanapalli, Ramadevi ^b   Alsina, Melissa ^a   Anasetti, Claudio ^a   Dalton, William ^a  

^a H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

^b TUSKEGEE UNIVERSITY   (United States)

^c BMT Blood and Marrow Transplantation Program   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FIBRONECTIN; FLICE INHIBITORY PROTEIN; INTERLEUKIN 6; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROCASPASE 3; PROCASPASE 8; PROTEIN BCL 2; RNA; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND RECEPTOR; CFLAR PROTEIN, HUMAN; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; BONE MARROW CELL; CANCER CELL CULTURE; CANCER RESISTANCE; CELL ADHESION; CELL ASSAY; CELL LINE; CONTROLLED STUDY; CYTOTOXICITY; DOWN REGULATION; ENZYME REGULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; INTRACELLULAR TRANSPORT; MITOCHONDRIAL MEMBRANE POTENTIAL; MULTIPLE MYELOMA; MYELOMA CELL; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RNA INTERFERENCE; STROMA CELL; BONE MARROW; DRUG ANTAGONISM; GENETICS; IMMUNOLOGY; METABOLISM; TUMOR CELL LINE;

APOPTOSIS; BONE MARROW; CASP8 AND FADD-LIKE APOPTOSIS REGULATING PROTEIN; CELL ADHESION; CELL LINE, TUMOR; CYTOTOXICITY, IMMUNOLOGIC; HUMANS; INTERLEUKIN-6; MULTIPLE MYELOMA; RNA INTERFERENCE; STROMAL CELLS; TNF-RELATED APOPTOSIS-INDUCING LIGAND;

EID: 40749116017     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.180.3.1545     Document Type: Article

References (62)

1. Cretney, E., K. Takeda, H. Yagita, M. Glaccum, J. J. Peschon, and M. J. Smyth. 2002. Increased susceptibility to tumor initiation and metastasis in TNF-related apoptosis-inducing ligand-deficient mice. J. Immunol. 168: 1356-1361.
2. Sedger, L. M., M. B. Glaccum, J. C. Schuh, S. T. Kanaly, E. Williamson, N. Kayagaki, T. Yun, P. Smolak, T. Le, R. Goodwin, and B. Gliniak. 2002. Characterization of the in vivo function of TNF-α-related apoptosis-inducing ligand, TRAIL/Apo2L, using TRAIL/Apo2L gene-deficient mice. Eur. J. Immunol. 32: 2246-2254.
3. -/- mice. Nat. Immunol. 4: 255-260.
4. Bouralexis, S., D. M. Findlay, and A. Evdokiou. 2005. Death to the bad guys: targeting cancer via Apo2L/TRAIL. Apoptosis 10: 35-51.
5. Wiley, S. R., K. Schooley, P. J. Smolak, W. S. Din, C. P. Huang, J. K. Nicholl, G. R. Sutherland, T. D. Smith, C. Rauch, C. A. Smith, et al. 1995. Identification and characterization of a new member of the TNF family that induces apoptosis. Immunity 3: 673-682.
6. Walczak, H., R. E. Miller, K. Ariail, B. Gliniak, T. S. Griffith, M. Kubin, W. Chin, J. Jones, A. Woodward, T. Le, et al. 1999. Tumoricidal activity of tumor necrosis factor-related apoptosis-inducing ligand in vivo. Nat. Med. 5: 157-163.
7. Mitsiades, C. S., S. P. Treon, N. Mitsiades, Y. Shima, P. Richardson, R. Schlossman, T. Hideshima, and K. C. Anderson. 2001. TRAIL/Apo2L ligand selectively induces apoptosis and overcomes drug resistance in multiple myeloma: therapeutic applications. Blood 98: 795-804.
8. Younes, A., J. M. Vose, A. D. Zelenetz, M. R. Smith, H. Burris, S. Ansell, J. Klein, E. Kumm, and M. Czuczman. 2005. Results of a phase 2 trial of HGS-ETR1 (agonistic human monoclonal antibody to TRAIL receptor 1) in subjects with relapsed/refractory non-Hodgkin's lymphoma (NHL). Blood 106: 489a.
9. Fesik, S. W. 2005. Promoting apoptosis as a strategy for cancer drug discovery. Nat. Rev. Cancer 5: 876-885.
10. Schmaltz, C., O. Alpdogan, B. J. Kappel, S. J. Muriglan, J. A. Rotolo, J. Ongchin, L. M. Willis, A. S. Greenberg, J. M. Eng, J. M. Crawford, et al. 2002. T cells require TRAIL for optimal graft-versus-tumor activity. Nat. Med. 8: 1433-1437.
11. Zhang, L., and B. Fang. 2005. Mechanisms of resistance to TRAIL-induced apoptosis in cancer. Cancer Gene Ther. 12: 228-237.
12. Nefedova, Y., T. H. Landowski, and W. S. Dalton. 2003. Bone marrow stromal-derived soluble factors and direct cell contact contribute to de novo drug resistance of myeloma cells by distinct mechanisms. Leukemia 17: 1175-1182.
13. Hazlehurst, L. A., R. F. Argilagos, M. Emmons, D. Boulware, C. A. Beam, D. M. Sullivan, and W. S. Dalton. 2006. Cell adhesion to fibronectin (CAM-DR) influences acquired mitoxantrone resistance in U937 cells. Cancer Res. 66: 2338-2345.
14. Shain, K. H., T. H. Landowski, and W. S. Dalton. 2002. Adhesion-mediated intracellular redistribution of c-Fas-associated death domain-like IL-1-converting enzyme-like inhibitory protein-long confers resistance to CD95-induced apoptosis in hematopoietic cancer cell lines. J. Immunol. 168: 2544-2553.
15. Yanamandra, N., N. M. Colaco, N. A. Parquet, R. W. Buzzeo, D. Boulware, G. Wright, L. E. Perez, W. S. Dalton, and D. M. Beaupre. 2006. Tipifarnib and bortezomib are synergistic and overcome cell adhesion-mediated drug resistance in multiple myeloma and acute myeloid leukemia. Clin. Cancer Res. 12: 591-599.
16. Dalton, W. S., L. Hazlehurst, K. Shain, T. Landowski, and M. Alsina. 2004. Targeting the bone marrow microenvironment in hematologic malignancies. Semin. Hematol. 41: 1-5.
17. Landowski, T. H., N. E. Olashaw, D. Agrawal, and W. S. Dalton. 2003. Cell adhesion-mediated drug resistance (CAM-DR) is associated with activation of NF-kB (RelB/p50) in myeloma cells. Oncogene 22: 2417-2421.
18. Damiano, J. S., A. E. Cress, L. A. Hazlehurst, A. A. Shtil, and W. S. Dalton. 1999. Cell adhesion mediated drug resistance (CAM-DR): role of integrins and resistance to apoptosis in human myeloma cell lines. Blood 93: 1658-1667.
19. Shain, K. H., and W. S. Dalton. 2001. Cell adhesion is a key determinant in de novo multidrug resistance (MDR): new targets for the prevention of acquired MDR. Mol. Cancer Ther. 1: 69-78.
20. Abdollahi, T., N. M. Robertson, A. Abdollahi, and G. Litwack. 2003. Identification of interleukin 8 as an inhibitor of tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis in the ovarian carcinoma cell line OVCAR3. Cancer Res. 63: 4521-4526.
21. Ahonen, M., M. Poukkula, A. H. Baker, M. Kashiwagi, H. Nagase, J. E. Eriksson, and V. M. Kahari. 2003. Tissue inhibitor of metalloproteinases-3 induces apoptosis in melanoma cells by stabilization of death receptors. Oncogene 22: 2121-2134.
22. Kyle, R. A., and S. V. Rajkumar. 2004. Multiple myeloma. N. Engl. J. Med. 351: 1860-1873.
23. Spencer, A., S.-L. Yeh, K. Koutrevelis, C. Baulch-Brown, N. Mitsiades, C. Mitsiades, K. C. Anderson, and S. P. Treon. 2002. TRAIL-induced apoptosis of authentic myeloma cells does not correlate with the procaspase-8/cFLIP ratio. Blood 100: 3049-3050.
24. Roecklein, B. A., and B. Torok-Storb. 1995. Functionally distinct human marrow stromal cell lines immortalized by transduction with the human papilloma virus E6/E7 genes. Blood 85: 997-1005.
25. Iwata, M., L. Graf, N. Awaya, and B. Torok-Storb. 2002. Functional interleukin-7 receptors (IL-7Rs) are expressed by marrow stromal cells: binding of IL-7 increases levels of IL-6 mRNA and secreted protein. Blood 100: 1318-1325.
26. Garrido, S. M., F. R. Appelbaum, C. L. Willman, and D. E. Banker. 2001. Acute myeloid leukemia cells are protected from spontaneous and drug-induced apoptosis by direct contact with a human bone marrow stromal cell line (HS-5). Exp. Hematol. 29: 448-457.
27. Hazlehurst, L. A., N. Valkov, L. Wisner, J. A. Storey, D. Boulware, D. M. Sullivan, and W. S. Dalton. 2001. Reduction in drug-induced DNA double-strand breaks associated with β1 integrin-mediated adhesion correlates with drug resistance in U937 cells. Blood 98: 1897-1903.
28. Shin, M. S., H. S. Kim, S. H. Lee, W. S. Park, S. Y. Kim, J. Y. Park, J. H. Lee, S. K. Lee, S. N. Lee, S. S. Jung, et al. 2001. Mutations of tumor necrosis factor-related apoptosis-inducing ligand receptor 1 (TRAIL-R1) and receptor 2 (TRAIL-R2) genes in metastatic breast cancers. Cancer Res. 61: 4942-4946.
29. Lee, S. H., M. S. Shin, H. S. Kim, H. K. Lee, W. S. Park, S. Y. Kim, J. H. Lee, S. Y. Han, J. Y. Park, R. R. Oh, et al. 2001. Somatic mutations of TRAIL-receptor 1 and TRAIL-receptor 2 genes in non-Hodgkin's lymphoma. Oncogene 20: 399-403.
30. Degli-Esposti, M. A., W. C. Dougall, P. J. Smolak, J. Y. Waugh, C. A. Smith, and R. G. Goodwin. 1997. The novel receptor TRAIL-R4 induces NF-κB and protects against TRAIL-mediated apoptosis, yet retains an incomplete death domain. Immunity 7: 813-820.
31. Sheridan, J. P., S. A. Marsters, R. M. Pitti, A. Gurney, M. Skubatch, D. Baldwin, L. Ramakrishnan, C. L. Gray, K. Baker, W. I. Wood, et al. 1997. Control of TRAIL-induced apoptosis by a family of signaling and decoy receptors. Science 277: 818-821.
32. Irmler, M., M. Thome, M. Hahne, P. Schneider, K. Hofmann, V. Steiner, J. L. Bodmer, M. Schroter, K. Burns, C. Mattmann, et al. 1997. Inhibition of death receptor signals by cellular FLIP. Nature 388: 190-195.
33. Rasper, D. M., J. P. Vaillancourt, S. Hadano, V. M. Houtzager, I. Seiden, S. L. Keen, P. Tawa, S. Xanthoudakis, J. Nasir, D. Martindale, et al. 1998. Cell death attenuation by "Usurpin," a mammalian DED-caspase homologue that precludes caspase-8 recruitment and activation by the CD-95 (Fas, APO-1) receptor complex. Cell Death Differ. 5: 271-288.
34. Mitsiades, N., C. S. Mitsiades, V. Poulaki, K. C. Anderson, and S. P. Treon. 2002. Intracellular regulation of tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis in human multiple myeloma cells. Blood 99: 2162-2171.
35. Graf, L., M. Iwata, and B. Torok-Storb. 2002. Gene expression profiling of the functionally distinct human bone marrow stromal cell lines HS-5 and HS-27a. Blood 100: 1509-1511.
36. Chen, Q., S. Ray, M. A. Hussein, G. Srkalovic, and A. Almasan. 2003. Role of Apo2L/TRAIL and Bcl-2-family proteins in apoptosis of multiple myeloma. Leuk. Lymphoma 44: 1209-1214.
37. Catlett-Falcone, R., T. H. Landowski, M. M. Oshiro, J. Turkson, A. Levitzki, R. Savino, G. Ciliberto, L. Moscinski, J. L. Fernandez-Luna, G. Nunez, et al. 1999. Constitutive activation of Stat3 signaling confers resistance to apoptosis in human U266 myeloma cells. Immunity 10: 105-115.
38. Hazlehurst, L. A., T. H. Landowski, and W. S. Dalton. 2003. Role of the tumor microenvironment in mediating de novo resistance to drugs and physiological mediators of cell death. Oncogene 22: 7396-7402.
39. Yasui, H., T. Hideshima, P. G. Richardson, and K. C. Anderson. 2006. Novel therapeutic strategies targeting growth factor signalling cascades in multiple myeloma. Br. J. Haematol. 132: 385-397.
40. Sze, D. M., R. Brown, S. Yang, P. J. Ho, J. Gibson, and D. Joshua. 2006. The use of thalidomide in myeloma therapy as an effective anticancer drug. Curr. Cancer Drug Targets 6: 325-331.
41. Richardson, P. G., E. Blood, C. S. Mitsiades, S. Jagannath, S. R. Zeldenrust, M. Alsina, R. L. Schlossman, S. V. Rajkumar, K. R. Desikan, T. Hideshima, et al. 2006. A randomized phase 2 study of lenalidomide therapy for patients with relapsed or relapsed and refractory multiple myeloma. Blood 108: 3458-3464.
42. Richardson, P., S. Jagannath, and K. Colson. 2006. Optimizing the efficacy and safety of bortezomib in relapsed multiple myeloma. Clin. Adv. Hematol. Oncol. 4: 1, 8, 13.
43. Mitsiades, N., C. S. Mitsiades, V. Poulaki, K. C. Anderson, and S. P. Treon. 2002. Intracellular regulation of tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis in human multiple myeloma cells. Blood 99: 2162-2171.
44. Dutton, A., A. T. Burns, L. S. Young, and P. G. Murray. 2006. Targeting cellular FLICE-like inhibitory protein as a novel approach to the treatment of Hodgkin's lymphoma. Expert Rev. Anticancer Ther. 6: 911-919.
45. Dutton, A., L. S. Young, and P. G. Murray. 2006. The role of cellular FLICE inhibitory protein (c-FLIP) in the pathogenesis and treatment of cancer. Expert Opin. Ther. Targets 10: 27-35.
46. Valente, G., F. Manfroi, C. Peracchio, G. Nicotra, R. Castino, G. Nicosia, S. Kerim, and C. Isidoro. 2006. cFLIP expression correlates with tumour progression and patient outcome in non-Hodgkin lymphomas of low grade of malignancy. Br. J. Haematol. 132: 560-570.
47. Oyarzo, M. P., L. J. Medeiros, C. Atwell, M. Feretzaki, V. Leventaki, E. Drakos, H. M. Amin, and G. Z. Rassidakis. 2006. c-FLIP confers resistance to FAS-mediated apoptosis in anaplastic large-cell lymphoma. Blood 107: 2544-2547.
48. Longley, D. B., T. R. Wilson, M. McEwan, W. L. Allen, U. McDermott, L. Galligan, and P. G. Johnston. 2006. c-FLIP inhibits chemotherapy-induced colorectal cancer cell death. Oncogene 25: 838-848.
49. Pathil, A., S. Armeanu, S. Venturelli, P. Mascagni, T. S. Weiss, M. Gregor, U. M. Lauer, and M. Bitzer. 2006. HDAC inhibitor treatment of hepatoma cells induces both TRAIL-independent apoptosis and restoration of sensitivity to TRAIL. Hepatology 43: 425-434.
50. El-Zawahry, A., P. Lu, S. J. White, and C. Voelkel-Johnson. 2006. In vitro efficacy of AdTRAIL gene therapy of bladder cancer is enhanced by trichostatin A-mediated restoration of CAR expression and downregulation of cFLIP and Bcl-XL. Cancer Gene Ther. 13: 281-289.
51. Medema, J. P., J. de Jong, T. van Hall, C. J. Melief, and R. Offringa. 1999. Immune escape of tumors in vivo by expression of cellular FLICE-inhibitory protein. J. Exp. Med. 190: 1033-1038.
52. Djerbi, M., V. Screpanti, A. I. Catrina, B. Bogen, P. Biberfeld, and A. Grandien. 1999. The inhibitor of death receptor signaling, FLICE-inhibitory protein defines a new class of tumor progression factors. J. Exp. Med. 190: 1025-1032.
53. Kim, D. K., E. S. Cho, J. H. Yoo, and H. D. Um. 2000. FLIP is constitutively hyperexpressed in Fas-resistant U266 myeloma cells, but is not induced by IL-6 in Fas-sensitive RPM18226 cells. Mol. Cells 10: 552-556.
54. Zhang, S., H. M. Shen, and C. N. Ong. 2005. Down-regulation of c-FLIP contributes to the sensitization effect of 3,3′-diindolylmethane on TRAIL-induced apoptosis in cancer cells. Mol. Cancer Ther. 4: 1972-1981.
55. Kataoka, T. 2005. The caspase-8 modulator c-FLIP. Crit. Rev. Immunol. 25: 31-58.
56. Frassanito, M. A., A. Cusmai, G. Iodice, and F. Dammacco. 2001. Autocrine interleukin-6 production and highly malignant multiple myeloma: relation with resistance to drug-induced apoptosis. Blood 97: 483-489.
57. Hideshima, T., N. Nakamura, D. Chauhan, and K. C. Anderson. 2001. Biologic sequelae of interleukin-6 induced PI3-K/Akt signaling in multiple myeloma. Oncogene 20: 5991-6000.
58. Chauhan, D., P. Pandey, T. Hideshima, S. Treon, N. Raje, F. E. Davies, Y. Shima, Y. T. Tai, S. Rosen, S. Avraham, et al. 2000. SHP2 mediates the protective effect of interleukin-6 against dexamethasone-induced apoptosis in multiple myeloma cells. J. Biol. Chem. 275: 27845-27850.
59. Chauhan, D., S. Kharbanda, A. Ogata, M. Urashima, G. Teoh, M. Robertson, D. W. Kufe, and K. C. Anderson. 1997. Interleukin-6 inhibits Fas-induced apoptosis and stress-activated protein kinase activation in multiple myeloma cells. Blood 89: 227-234.
60. Hideshima, T., P. Richardson, D. Chauhan, V. J. Palombella, P. J. Elliott, J. Adams, and K. C. Anderson. 2001. The proteasome inhibitor PS-341 inhibits growth, induces apoptosis, and overcomes drug resistance in human multiple myeloma cells. Cancer Res. 61: 3071-3076.
61. Panka, D. J., T. Mano, T. Suhara, K. Walsh, and J. W. Mier. 2001. Phosphatidylinositol 3-kinase/Akt activity regulates c-FLIP expression in tumor cells. J. Biol. Chem. 276: 6893-6896.
62. Puduvalli, V. K., D. Sampath, J. M. Bruner, J. Nangia, R. Xu, and A. P. Kyritsis. 2005. TRAIL-induced apoptosis in gliomas is enhanced by Akt-inhibition and is independent of JNK activation. Apoptosis 10: 233-243.