Bortezomib and TRAIL: A perfect match for apoptotic elimination of tumour cells?

Critical Reviews in Oncology/Hematology

Volumn 85, Issue 3, 2013, Pages 363-372

  de Wilt, L H A M ^a,b   Kroon, J ^a   Jansen, G ^a   de Jong, S ^b   Peters, G J ^a   Kruyt, F A E ^b  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

Bortezomib; Cancer stem cells; Primary cells; Proteasome inhibitor; Resistance; TRAIL; Ubiquitin

Indexed keywords

5 AMINO 8 HYDROXYQUINOLINE; ANTINEOPLASTIC AGENT; BORTEZOMIB; CARFILZOMIB; CASPASE 8; CONATUMUMAB; FLICE INHIBITORY PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INHIBITOR OF APOPTOSIS PROTEIN; LEXATUMUMAB; MAPATUMUMAB; MD 5 1; ONX 0914; OPROZOMIB; PHOSPHOTRANSFERASE; PROTEIN BCL 2; PROTEIN P21; PROTEIN P27; PROTEIN P53; RECOMBINANT TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; TIGATUZUMAB; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND RECEPTOR; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; BREAST CANCER; CANCER CELL CULTURE; CANCER STEM CELL; CELL STIMULATION; COCULTURE; CONCENTRATION RESPONSE; DRUG DISTRIBUTION; DRUG DOSE REDUCTION; DRUG EFFICACY; DRUG MECHANISM; DRUG PENETRATION; DRUG POTENCY; DRUG POTENTIATION; DRUG RESEARCH; DRUG TARGETING; DRUG UPTAKE; HODGKIN DISEASE; HUMAN; KIDNEY CANCER; LARGE CELL LYMPHOMA; LIVER CELL CARCINOMA; LUNG NON SMALL CELL CANCER; LYMPHOMA; MANTLE CELL LYMPHOMA; MULTIPLE MYELOMA; NONHUMAN; PHARMACODYNAMICS; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PROSTATE CANCER; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN PROTEIN INTERACTION; RECEPTOR UPREGULATION; REVIEW; SIGNAL TRANSDUCTION; SOLID TUMOR; SPHEROID CELL; STROMA CELL; SURVIVAL TIME; TUMOR CELL; TUMOR XENOGRAFT;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BORONIC ACIDS; DISEASE MODELS, ANIMAL; DRUG EVALUATION, PRECLINICAL; HUMANS; NEOPLASMS; PYRAZINES; SIGNAL TRANSDUCTION; TNF-RELATED APOPTOSIS-INDUCING LIGAND;

EID: 84873526407     PISSN: 10408428     EISSN: 18790461     Source Type: Journal    
DOI: 10.1016/j.critrevonc.2012.08.001     Document Type: Review

References (102)

1. Ashkenazi A., Pai R.C., Fong S., et al. Safety and antitumor activity of recombinant soluble Apo2 ligand. Journal of Clinical Investigation 1999, 104:155-162.
2. Wang S., El-Deiry W.S. TRAIL and apoptosis induction by TNF-family death receptors. Oncogene 2003, 22:8628-8633.
3. Ashkenazi A. Directing cancer cells to self-destruct with pro-apoptotic receptor agonists. Nature Reviews Drug Discovery 2008, 7:1001-1012.
4. Mahalingam D., Szegezdi E., Keane M., de Jong S., Samali A. TRAIL receptor signalling and modulation: are we on the right TRAIL?. Cancer Treatment Reviews 2009, 35:280-288.
5. Reis C.R., van der Sloot A.M., Natoni A., et al. Rapid and efficient cancer cell killing mediated by high-affinity death receptor homotrimerizing TRAIL variants. Cell Death & Disease 2010, 1:e83.
6. Kruyt F.A. TRAIL and cancer therapy. Cancer Letters 2008, 263:14-25.
7. Sprick M.R., Weigand M.A., Rieser E., et al. FADD/MORT1 and caspase-8 are recruited to TRAIL receptors 1 and 2 and are essential for apoptosis mediated by TRAIL receptor 2. Immunity 2000, 12:599-609.
8. Falschlehner C., Emmerich C.H., Gerlach B., Walczak H. TRAIL signalling: decisions between life and death. International Journal of Biochemistry and Cell Biology 2007, 39:1462-1475.
9. Stegehuis J.H., de Wilt L.H., de Vries E.G., Groen H.J., de Jong S., Kruyt F.A. TRAIL receptor targeting therapies for non-small cell lung cancer: current status and perspectives. Drug Resistance Updates 2010, 13:2-15.
10. Varfolomeev E., Maecker H., Sharp D., et al. Molecular determinants of kinase pathway activation by Apo2 ligand/tumor necrosis factor-related apoptosis-inducing ligand. Journal of Biological Chemistry 2005, 280:40599-40608.
11. Vucic D., Dixit V.M., Wertz I.E. Ubiquitylation in apoptosis: a post-translational modification at the edge of life and death. Nature Reviews Molecular Cell Biology 2011, 12:439-452.
12. Orlowski R.Z., Kuhn D.J. Proteasome inhibitors in cancer therapy: lessons from the first decade. Clinical Cancer Research 2008, 14:1649-1657.
13. Raab M.S., Podar K., Breitkreutz I., Richardson P.G., Anderson K.C. Multiple myeloma. Lancet 2009, 374:324-339.
14. Adams J. The proteasome: structure, function, and role in the cell. Cancer Treatment Reviews 2003, 29(Suppl. 1):3-9.
15. Mitsiades C.S., Treon S.P., Mitsiades N., et al. TRAIL/Apo2L ligand selectively induces apoptosis and overcomes drug resistance in multiple myeloma: therapeutic applications. Blood 2001, 98:795-804.
16. Brooks A.D., Jacobsen K.M., Li W., Shanker A., Sayers T.J. Bortezomib sensitizes human renal cell carcinomas to TRAIL apoptosis through increased activation of caspase-8 in the death-inducing signaling complex. Molecular Cancer Research 2010, 8:729-738.
17. Chen K.F., Yeh P.Y., Hsu C., et al. Bortezomib overcomes tumor necrosis factor-related apoptosis-inducing ligand resistance in hepatocellular carcinoma cells in part through the inhibition of the phosphatidylinositol 3-kinase/Akt pathway. Journal of Biological Chemistry 2009, 284:11121-11133.
18. Conticello C., Adamo L., Giuffrida R., et al. Proteasome inhibitors synergize with tumor necrosis factor-related apoptosis-induced ligand to induce anaplastic thyroid carcinoma cell death. Journal of Clinical Endocrinology and Metabolism 2007, 92:1938-1942.
19. Koschny R., Holland H., Sykora J., et al. Bortezomib sensitizes primary human astrocytoma cells of WHO grades I to IV for tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis. Clinical Cancer Research 2007, 13:3403-3412.
20. Liu J., Qu X.J., Xu L., et al. Bortezomib synergizes TRAIL-induced apoptosis in gastric cancer cells. Digestive Diseases and Sciences 2010, 55:3361-3368.
21. Liu X., Yue P., Chen S., et al. 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 Research 2007, 67:4981-4988.
22. Delmas D., Rebe C., Micheau O., et al. Redistribution of CD95, DR4 and DR5 in rafts accounts for the synergistic toxicity of resveratrol and death receptor ligands in colon carcinoma cells. Oncogene 2004, 23:8979-8986.
23. Song J.H., Tse M.C., Bellail A., et al. Lipid rafts and nonrafts mediate tumor necrosis factor related apoptosis-inducing ligand induced apoptotic and nonapoptotic signals in non small cell lung carcinoma cells. Cancer Research 2007, 67:6946-6955.
24. Xu L., Qu X., Zhang Y., et al. Oxaliplatin enhances TRAIL-induced apoptosis in gastric cancer cells by CBL-regulated death receptor redistribution in lipid rafts. FEBS Letters 2009, 583:943-948.
25. Seki N., Toh U., Sayers T.J., et al. Bortezomib sensitizes human esophageal squamous cell carcinoma cells to TRAIL-mediated apoptosis via activation of both extrinsic and intrinsic apoptosis pathways. Molecular Cancer Therapeutics 2010, 9:1842-1851.
26. Ganten T.M., Koschny R., Haas T.L., et al. Proteasome inhibition sensitizes hepatocellular carcinoma cells, but not human hepatocytes, to TRAIL. Hepatology 2005, 42:588-597.
27. Koschny R., Holland H., Sykora J., et al. Bortezomib sensitizes primary human esthesioneuroblastoma cells to TRAIL-induced apoptosis. Journal of Neuro-Oncology 2010, 97:171-185.
28. Jin Z., Li Y., Pitti R., et al. Cullin3-based polyubiquitination and p62-dependent aggregation of caspase-8 mediate extrinsic apoptosis signaling. Cell 2009, 137:721-735.
29. Micheau O. Cellular FLICE-inhibitory protein: an attractive therapeutic target?. Expert Opinion on Therapeutic Targets 2003, 7:559-573.
30. Yu J.W., Shi Y. FLIP and the death effector domain family. Oncogene 2008, 27:6216-6227.
31. Zhao X., Qiu W., Kung J., et al. 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. Leukemia Research 2008, 32:275-285.
32. An J., Sun Y., Fisher M., Rettig M.B. Antitumor effects of bortezomib (PS-341) on primary effusion lymphomas. Leukemia 2004, 18:1699-1704.
33. Shanker A., Brooks A.D., Tristan C.A., et al. Treating metastatic solid tumors with bortezomib and a tumor necrosis factor-related apoptosis-inducing ligand receptor agonist antibody. Journal of the National Cancer Institute 2008, 100:649-662.
34. Thorpe J.A., Christian P.A., Schwarze S.R. Proteasome inhibition blocks caspase-8 degradation and sensitizes prostate cancer cells to death receptor-mediated apoptosis. Prostate 2008, 68:200-209.
35. Voortman J., Resende T.P., Abou El Hassan M.A., Giaccone G., Kruyt F.A. TRAIL therapy in non-small cell lung cancer cells: sensitization to death receptor-mediated apoptosis by proteasome inhibitor bortezomib. Molecular Cancer Therapeutics 2007, 6:2103-2112.
36. Roue G., Perez-Galan P., Lopez-Guerra M., Villamor N., Campo E., Colomer D. Selective inhibition of IkappaB kinase sensitizes mantle cell lymphoma B cells to TRAIL by decreasing cellular FLIP level. Journal of Immunology 2007, 178:1923-1930.
37. Balsas P., Lopez-Royuela N., Galan-Malo P., Anel A., Marzo I., Naval J. Cooperation between Apo2L/TRAIL and bortezomib in multiple myeloma apoptosis. Biochemical Pharmacology 2009, 77:804-812.
38. Johnson T.R., Stone K., Nikrad M., et al. The proteasome inhibitor PS-341 overcomes TRAIL resistance in Bax and caspase 9-negative or Bcl-xL overexpressing cells. Oncogene 2003, 22:4953-4963.
39. Sohn D., Totzke G., Essmann F., Schulze-Osthoff K., Levkau B., Janicke R.U. The proteasome is required for rapid initiation of death receptor-induced apoptosis. Molecular and Cellular Biology 2006, 26:1967-1978.
40. Laussmann M.A., Passante E., Hellwig C.T., et al. Proteasome inhibition can impair caspase-8 activation upon submaximal stimulation of apoptotic tumor necrosis factor-related apoptosis inducing ligand (TRAIL) signaling. Journal of Biological Chemistry 2012, 287:14402-14411.
41. Chang L., Kamata H., Solinas G., et al. The E3 ubiquitin ligase itch couples JNK activation to TNFalpha-induced cell death by inducing c-FLIP(L) turnover. Cell 2006, 124:601-613.
42. Mitsiades N., Mitsiades C.S., Poulaki V., Anderson K.C., Treon S.P. Intracellular regulation of tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis in human multiple myeloma cells. Blood 2002, 99:2162-2171.
43. Spencer A., Yeh S.L., Koutrevelis K., Baulch-Brown C. TRAIL-induced apoptosis of authentic myeloma cells does not correlate with the procaspase-8/cFLIP ratio. Blood 2002, 100:3049-3051.
44. Baritaki S., Suzuki E., Umezawa K., Spandidos D.A., Berenson J., Daniels T.R. Inhibition of Yin Yang 1-dependent repressor activity of DR5 transcription and expression by the novel proteasome inhibitor NPI-0052 contributes to its TRAIL-enhanced apoptosis in cancer cells. Journal of Immunology 2008, 180:6199-6210.
45. Jane E.P., Premkumar D.R., Pollack I.F. Bortezomib sensitizes malignant human glioma cells to TRAIL, mediated by inhibition of the NF-{kappa}B signaling pathway. Molecular Cancer Therapeutics 2011, 10:198-208.
46. Orlowski R.Z., Baldwin A.S. NF-kappaB as a therapeutic target in cancer. Trends in Molecular Medicine 2002, 8:385-389.
47. Scagliotti G. Proteasome inhibitors in lung cancer. Critical Reviews in Oncology/Hematology 2006, 58:177-189.
48. Sayers T.J., Brooks A.D., Koh C.Y., et al. The proteasome inhibitor PS-341 sensitizes neoplastic cells to TRAIL-mediated apoptosis by reducing levels of c-FLIP. Blood 2003, 102:303-310.
49. Kreuz S., Siegmund D., Scheurich P., Wajant H. NF-kappaB inducers upregulate cFLIP, a cycloheximide-sensitive inhibitor of death receptor signaling. Molecular and Cellular Biology 2001, 21:3964-3973.
50. Khanbolooki S., Nawrocki S.T., Arumugam T., et al. Nuclear factor-kappaB maintains TRAIL resistance in human pancreatic cancer cells. Molecular Cancer Therapeutics 2006, 5:2251-2260.
51. Nagy K., Szekely-Szuts K., Izeradjene K., et al. Proteasome inhibitors sensitize colon carcinoma cells to TRAIL-induced apoptosis via enhanced release of Smac/DIABLO from the mitochondria. Pathology Oncology Research 2006, 12:133-142.
52. Vaux D.L., Silke J. IAPs, RINGs and ubiquitylation. Nature Reviews Molecular Cell Biology 2005, 6:287-297.
53. Suzuki Y., Nakabayashi Y., Takahashi R. Ubiquitin-protein ligase activity of X-linked inhibitor of apoptosis protein promotes proteasomal degradation of caspase-3 and enhances its anti-apoptotic effect in Fas-induced cell death. Proceedings of the National Academy of Sciences of the United States of America 2001, 98:8662-8667.
54. MacFarlane M., Merrison W., Bratton S.B., Cohen G.M. Proteasome-mediated degradation of Smac during apoptosis: XIAP promotes Smac ubiquitination in vitro. Journal of Biological Chemistry 2002, 277:36611-36616.
55. Silke J., Kratina T., Chu D., et al. Determination of cell survival by RING-mediated regulation of inhibitor of apoptosis (IAP) protein abundance. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:16182-16187.
56. Bruning A., Burger P., Vogel M., et al. Bortezomib treatment of ovarian cancer cells mediates endoplasmic reticulum stress, cell cycle arrest, and apoptosis. Investigational New Drugs 2008, 27:543-551.
57. Brunelle J.K., Letai A. Control of mitochondrial apoptosis by the Bcl-2 family. Journal of Cell Science 2009, 122:437-441.
58. Fahy B.N., Schlieman M.G., Mortenson M.M., Virudachalam S., Bold R.J. Targeting BCL-2 overexpression in various human malignancies through NF-kappaB inhibition by the proteasome inhibitor bortezomib. Cancer Chemotherapy and Pharmacology 2005, 56:46-54.
59. Koschny R., Ganten T.M., Sykora J., et al. TRAIL/bortezomib cotreatment is potentially hepatotoxic but induces cancer-specific apoptosis within a therapeutic window. Hepatology 2007, 45:649-658.
60. Naumann I., Kappler R., von Schweinitz D., Debatin K.M., Fulda S. Bortezomib primes neuroblastoma cells for TRAIL-induced apoptosis by linking the death receptor to the mitochondrial pathway. Clinical Cancer Research 2011, 17:3204-3218.
61. Yuan B.Z., Chapman J., Reynolds S.H. Proteasome inhibitors induce apoptosis in human lung cancer cells through a positive feedback mechanism and the subsequent Mcl-1 protein cleavage. Oncogene 2009, 28:3775-3786.
62. Luster T.A., Carrell J.A., McCormick K., Sun D., Humphreys R. Mapatumumab and lexatumumab induce apoptosis in TRAIL-R1 and TRAIL-R2 antibody-resistant NSCLC cell lines when treated in combination with bortezomib. Molecular Cancer Therapeutics 2009, 8:292-302.
63. Nikrad M., Johnson T., Puthalalath H., Coultas L., Adams J., Kraft A.S. The proteasome inhibitor bortezomib sensitizes cells to killing by death receptor ligand TRAIL via BH3-only proteins Bik and Bim. Molecular Cancer Therapeutics 2005, 4:443-449.
64. Zhu H., Guo W., Zhang L., et al. Proteasome inhibitors-mediated TRAIL resensitization and Bik accumulation. Cancer Biology and Therapy 2005, 4:781-786.
65. Tait S.W., de Vries E., Maas C., Keller A.M., D'Santos C.S., Borst J. Apoptosis induction by Bid requires unconventional ubiquitination and degradation of its N-terminal fragment. Journal of Cell Biology 2007, 179:1453-1466.
66. Brooks A.D., Ramirez T., Toh U., et al. The proteasome inhibitor bortezomib (Velcade) sensitizes some human tumor cells to Apo2L/TRAIL-mediated apoptosis. Annals of the New York Academy of Sciences 2005, 1059:160-167.
67. Hock A., Vousden K.H. Regulation of the p53 pathway by ubiquitin and related proteins. International Journal of Biochemistry and Cell Biology 2010, 42:1618-1621.
68. Zhao J., Lu Y., Shen H.M. Targeting p53 as a therapeutic strategy in sensitizing TRAIL-induced apoptosis in cancer cells. Cancer Letters 2012, 314:8-23.
69. Hori T., Kondo T., Kanamori M., et al. Nutlin-3 enhances tumor necrosis factor-related apoptosis-inducing ligand (TRAIL)-induced apoptosis through up-regulation of death receptor 5 (DR5) in human sarcoma HOS cells and human colon cancer HCT116 cells. Cancer Letters 2010, 287:98-108.
70. Hideshima T., Richardson P., Chauhan D., et al. The proteasome inhibitor PS-341 inhibits growth, induces apoptosis, and overcomes drug resistance in human multiple myeloma cells. Cancer Research 2001, 61:3071-3076.
71. Lashinger L.M., Zhu K., Williams S.A., Shrader M., Dinney C.P., McConkey D.J. Bortezomib abolishes tumor necrosis factor-related apoptosis-inducing ligand resistance via a p21-dependent mechanism in human bladder and prostate cancer cells. Cancer Research 2005, 65:4902-4908.
72. Okhrimenko H., Lu W., Xiang C., et al. Roles of tyrosine phosphorylation and cleavage of protein kinase Cdelta in its protective effect against tumor necrosis factor-related apoptosis inducing ligand-induced apoptosis. Journal of Biological Chemistry 2005, 280:23643-23652.
73. Kahana S., Finniss S., Cazacu S., et al. Proteasome inhibitors sensitize glioma cells and glioma stem cells to TRAIL-induced apoptosis by PKCepsilon-dependent downregulation of AKT and XIAP expressions. Cellular Signalling 2011, 23:1348-1357.
74. Kaunisto A., Kochin V., Asaoka T., et al. PKC-mediated phosphorylation regulates c-FLIP ubiquitylation and stability. Cell Death and Differentiation 2009, 16:1215-1226.
75. Georgakis G.V., Li Y., Humphreys R., et al. Activity of selective fully human agonistic antibodies to the TRAIL death receptors TRAIL-R1 and TRAIL-R2 in primary and cultured lymphoma cells: induction of apoptosis and enhancement of doxorubicin- and bortezomib-induced cell death. British Journal of Haematology 2005, 130:501-510.
76. Kabore A.F., Sun J., Hu X., McCrea K., Johnston J.B., Gibson S.B. The TRAIL apoptotic pathway mediates proteasome inhibitor induced apoptosis in primary chronic lymphocytic leukemia cells. Apoptosis 2006, 11:1175-1193.
77. Liu F.T., Agrawal S.G., Gribben J.G., et al. Bortezomib blocks Bax degradation in malignant B cells during treatment with TRAIL. Blood 2008, 111:2797-2805.
78. Pasquini L., Petronelli A., Petrucci E., et al. Primary ovarian cancer cells are sensitive to the proaptotic effects of proteasome inhibitors. International Journal of Oncology 2010, 36:707-713.
79. Saulle E., Petronelli A., Pasquini L., et al. Proteasome inhibitors sensitize ovarian cancer cells to TRAIL induced apoptosis. Apoptosis 2007, 12:635-655.
80. Unterkircher T., Cristofanon S., Vellanki S.H., et al. Bortezomib primes glioblastoma, including glioblastoma stem cells, for TRAIL by increasing tbid stability and mitochondrial apoptosis. Clinical Cancer Research 2011, 17:4019-4030.
81. Riccioni R., Senese M., Diverio D., et al. M4 and M5 acute myeloid leukaemias display a high sensitivity to Bortezomib-mediated apoptosis. British Journal of Haematology 2007, 139:194-205.
82. Armeanu-Ebinger S., Fuchs J., Wenz J., Seitz G., Ruck P., Warmann S.W. Proteasome inhibition overcomes TRAIL resistance in human hepatoblastoma cells. Frontiers in Bioscience (Elite Edition) 2012, 4:2194-2202.
83. Reya T., Morrison S.J., Clarke M.F., Weissman I.L. Stem cells, cancer, and cancer stem cells. Nature 2001, 414:105-111.
84. Iannolo G., Conticello C., Memeo L., De Maria R. Apoptosis in normal and cancer stem cells. Critical Reviews in Oncology/Hematology 2008, 66:42-51.
85. Kruyt F.A., Schuringa J.J. Apoptosis and cancer stem cells: implications for apoptosis targeted therapy. Biochemical Pharmacology 2010, 80:423-430.
86. Magee J.A., Piskounova E., Morrison S.J. Cancer stem cells: impact, heterogeneity, and uncertainty. Cancer Cell 2012, 21:283-296.
87. Yong A.S., Keyvanfar K., Hensel N., et al. Primitive quiescent CD34+ cells in chronic myeloid leukemia are targeted by in vitro expanded natural killer cells, which are functionally enhanced by bortezomib. Blood 2009, 113:875-882.
88. Yang T.M., Barbone D., Fennell D.A., Broaddus V.C. Bcl-2 family proteins contribute to apoptotic resistance in lung cancer multicellular spheroids. American Journal of Respiratory Cell and Molecular Biology 2009, 41:14-23.
89. Perez L.E., Parquet N., Meads M., Anasetti C., Dalton W. Bortezomib restores stroma-mediated APO2L/TRAIL apoptosis resistance in multiple myeloma. European Journal of Haematology 2010, 84:212-222.
90. Christian P.A., Thorpe J.A., Schwarze S.R. Velcade sensitizes prostate cancer cells to TRAIL induced apoptosis and suppresses tumor growth in vivo. Cancer Biology and Therapy 2009, 8:73-80.
91. Lee S., Yagita H., Sayers T.J., Celis E. Optimized combination therapy using bortezomib, TRAIL and TLR agonists in established breast tumors. Cancer Immunology, Immunotherapy 2010, 59:1073-1081.
92. Chen K.F., Yu H.C., Liu C.Y., et al. Bortezomib sensitizes HCC cells to CS-1008, an antihuman death receptor 5 antibody, through the inhibition of CIP2A. Molecular Cancer Therapeutics 2011, 10:892-901.
93. Cheriyath V., Jacobs B.S., Hussein M.A. Proteasome inhibitors in the clinical setting: benefits and strategies to overcome multiple myeloma resistance to proteasome inhibitors. Drugs in R and D 2007, 8:1-12.
94. de Wilt L.H., Jansen G., Assaraf Y.G., et al. Proteasome-based mechanisms of intrinsic and acquired bortezomib resistance in non-small cell lung cancer. Biochemical Pharmacology 2012, 83:207-217.
95. Franke N.E., Niewerth D., Assaraf Y.G., et al. Impaired bortezomib binding to mutant beta5 subunit of the proteasome is the underlying basis for bortezomib resistance in leukemia cells. Leukemia 2012, 26:757-768.
96. Lu S., Yang J., Chen Z., et al. Different mutants of PSMB5 confer varying bortezomib resistance in T lymphoblastic lymphoma/leukemia cells derived from the Jurkat cell line. Experimental Hematology 2009, 37:831-837.
97. Oerlemans R., Franke N.E., Assaraf Y.G., et al. Molecular basis of bortezomib resistance: proteasome subunit beta5 (PSMB5) gene mutation and overexpression of PSMB5 protein. Blood 2008, 112:2489-2499.
98. Kisselev A.F., van der Linden W.A., Overkleeft H.S. Proteasome inhibitors: an expanding army attacking a unique target. Chemistry and Biology 2012, 19:99-115.
99. Demo S.D., Kirk C.J., Aujay M.A., et al. Antitumor activity of PR-171, a novel irreversible inhibitor of the proteasome. Cancer Research 2007, 67:6383-6391.
100. Chauhan D., Singh A.V., Aujay M., et al. A novel orally active proteasome inhibitor ONX 0912 triggers in vitro and in vivo cytotoxicity in multiple myeloma. Blood 2010, 116:4906-4915.
101. Muchamuel T., Basler M., Aujay M.A., et al. A selective inhibitor of the immunoproteasome subunit LMP7 blocks cytokine production and attenuates progression of experimental arthritis. Nature Medicine 2009, 15:781-787.
102. Li X., Wood T.E., Sprangers R., et al. Effect of noncompetitive proteasome inhibition on bortezomib resistance. Journal of the National Cancer Institute 2010, 102:1069-1082.