Linking the activity of bortezomib in multiple myeloma and autoimmune diseases

Critical Reviews in Oncology/Hematology

Volumn 92, Issue 2, 2014, Pages 61-70

  Škrott, Zdeněk ^a   Cvek, Boris ^a  

^a PALACKÝ UNIVERSITY   (Czech Republic)

Author keywords

Autoimmune diseases; Bortezomib; Multiple myeloma; Proteostasis; Resistance; Ubiquitin proteasome system

Indexed keywords

BORTEZOMIB; X BOX BINDING PROTEIN 1; ANTINEOPLASTIC AGENT; BORONIC ACID DERIVATIVE; PYRAZINE DERIVATIVE;

AUTOIMMUNE DISEASE; CANCER RESISTANCE; CHEMOSENSITIVITY; CLINICAL EVALUATION; DRUG MECHANISM; HUMAN; IMMUNOPATHOLOGY; IN VITRO STUDY; MULTIPLE MYELOMA; NONHUMAN; PROTEIN HOMEOSTASIS; REVIEW; ANIMAL; AUTOIMMUNE DISEASES; METABOLISM;

ANIMALS; ANTINEOPLASTIC AGENTS; AUTOIMMUNE DISEASES; BORONIC ACIDS; HUMANS; MULTIPLE MYELOMA; PYRAZINES;

EID: 84908346392     PISSN: 10408428     EISSN: 18790461     Source Type: Journal    
DOI: 10.1016/j.critrevonc.2014.05.003     Document Type: Review

References (127)

1. Moreau P., Richardson P.G., Cavo M., Orlowski R.Z., San Miguel J.F., Palumbo A., Harousseau J.L. Proteasome inhibitors in multiple myeloma: 10 years later. Blood 2012, 120(5):947-959.
2. Palombella V.J., Conner E.M., Fuseler J.W., et al. Role of the proteasome and NF-kappaB in streptococcal cell wall-induced polyarthritis. Proc Nat Acad Sci USA 1998, 95(26):15671-15676. 22.
3. Aghajanian C., Soignet S., Dizon D.S., et al. A phase I trial of the novel proteasome inhibitor PS341 in advanced solid tumor malignancies. Clin Cancer Res 2002, 8(8):2505-2511.
4. Orlowski R.Z., Stinchcombe T.E., Mitchell B.S., et al. Phase I trial of the proteasome inhibitor PS-341 in patients with refractory hematologic malignancies. J Clin Oncol 2002, 20(22):4420-4427.
5. Richardson P.G., Barlogie B., Berenson J., Singhal S., Jagannath S., Irwin D., Rajkumar S.V., Srkalovic G., Alsina M., Alexanian R., Siegel D., Orlowski R.Z., Kuter D., Limentani S.A., Lee S., Hideshima T., Esseltine D.L., Kauffman M., Adams J., Schenkein D.P., Anderson K.C. A phase 2 study of bortezomib in relapsed, refractory myeloma. N Engl J Med 2003, 348(26):2609-2617.
6. Jagannath S., Barlogie B., Berenson J., et al. A phase 2 study of two doses of bortezomib in relapsed or refractory myeloma. Br J Haematol 2004, 127(2):165-172.
7. Richardson P.G., Sonneveld P., Schuster M.W., et al. Bortezomib or high-dose dexamethasone for relapsed multiple myeloma. N Engl J Med 2005, 352(24):2487-2498.
8. Kouroukis C.T., Baldassarre F.G., Haynes A.E., Imrie K., Reece D.E., Cheung M.C. Bortezomib in multiple myeloma: a practice guideline. Clin Oncol (R Coll Radiol) 2014, 26(2):110-119.
9. Herndon T.M., Deisseroth A., Kaminskas E., et al. U.S. Food and Drug Administration approval: carfilzomib for the treatment of multiple myeloma. Clin Cancer Res 2013, 19(17):4559-4563.
10. Kortuem K.M., Stewart A.K. Carfilzomib. Blood 2013, 121(6):893-897.
11. Richardson P.G., SpencerA.Cannell P., et al. Phase 1 clinical evaluation of twice-weekly marizomib (NPI-0052), a novel proteasome inhibitor, in patients with relapsed/refractory multiple myeloma (MM). Blood 2011, 118(21):140-141.
12. Berdeja J.G., Richardson P.G., Lonial S., et al. Phase 1/2 study of oral MLN9708, a novel, investigational proteasome inhibitor, in combination with lenalidomide and dexamethasone in patients with previously untreated multiple myeloma (MM). Blood 2011, 118(21):223.
13. Richardson P.G., Baz R., Wang L., et al. Investigational agent MLN9708, an oral proteasome inhibitor, in patients (pts) with relapsed and/or refractory multiple myeloma (MM): results from the expansion cohorts of a phase 1 dose-escalation study. Blood 2011, 118(21):140.
14. Kane R.C., Dagher R., Farrell A., et al. Bortezomib for the treatment of mantle cell lymphoma. Clin Cancer Res 2007, 13(18):5291-5294.
15. Chen C.I., Kouroukis C.T., White D., et al. Bortezomib is active in patients with untreated or relapsed Waldenstrom's macroglobulinemia: a phase II study of the National Cancer Institute of Canada Clinical Trials Group. J Clin Oncol 2007, 25(12):1570-1575.
16. Treon S.P., Hunter Z.R., Matous J., et al. Multicenter clinical trial of bortezomib in relapsed/refractory Waldenstrom's macroglobulinemia: results of WMCTG Trial 03-248. Clin Cancer Res 2007, 13(11):3320-3325.
17. Dimopoulos M.A., García-Sanz R., Gavriatopoulou M., et al. Primary therapy of Waldenstrom macroglobulinemia (WM) with weekly bortezomib, low-dose dexamethasone, and rituximab (BDR): long-term results of a phase 2 study of the European Myeloma Network (EMN). Blood 2013, 122(19):3276-3282.
18. Troch M., Jonak C., Müllauer L., et al. A phase II study of bortezomib in patients with MALT lymphoma. Haematologica 2009, 94(5):738-742.
19. Conconi A., Martinelli G., Lopez-Guillermo A., et al. Clinical activity of bortezomib in relapsed/refractory MALT lymphomas: results of a phase II study of the International Extranodal Lymphoma Study Group (IELSG). Ann Oncol 2011, 22(3):689-695.
20. Zinzani P.L., Musuraca G., Tani M., et al. Phase II trial of proteasome inhibitor bortezomib in patients with relapsed or refractory cutaneous T-cell lymphoma. J Clin Oncol 2007, 25(27):4293-4297.
21. Cvek B. Proteasome inhibitors. Prog Mol Biol Transl Sci 2012, 109:161-226.
22. Finley D. Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annu Rev Biochem 2009, 78:477-513.
23. Cvek B., Dvorak Z. The ubiquitin-proteasome system (UPS) and the mechanism of action of bortezomib. Curr Pharm Des 2011, 17(15):1483-1499.
24. Dick L.R., Fleming P.E. Building on bortezomib: second-generation proteasome inhibitors as anti-cancer therapy. Drug Discovery Today 2010, 15(5-6):243-249.
25. Goldberg A.L. Protein degradation and protection against misfolded or damaged proteins. Nature 2003, 426:895-899.
26. 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 Res 2001, 61(7):3071-3076.
27. Chen Q., Xie W., Kuhn D.J., et al. Targeting the p27 E3 ligase SCF(Skp2) results in p27- and Skp2-mediated cell-cycle arrest and activation of autophagy. Blood 2008, 111(9):4690-4699.
28. Hideshima T., Mitsiades C., Akiyama M., et al. Molecular mechanisms mediating antimyeloma activity of proteasome inhibitor PS-341. Blood 2003, 101(4):1530-1534.
29. Mitsiades N., Mitsiades C.S., Poulaki V., et al. Molecular sequelae of proteasome inhibition in human multiple myeloma cells. Proc Nat Acad Sci USA 2002, 99(22):14374-14379.
30. Pei X.Y., Dai Y., Grant S. The proteasome inhibitor bortezomib promotes mitochondrial injury and apoptosis induced by the small molecule Bcl-2 inhibitor HA14-1 in multiple myeloma cells. Leukemia 2003, 17(10):2036-2045.
31. Qin J.Z., Ziffra J., Stennett L., et al. Proteasome inhibitors trigger NOXA-mediated apoptosis in melanoma and myeloma cells. Cancer Res 2005, 65(14):6282-6293.
32. Karin M. Nuclear factor-κB in cancer development and progression. Nature 2006, 441(7092):431-436.
33. Hayden M.S., Ghosh S. Shared principles in NF-κB signaling. Cell 2008, 132(3):344-362.
34. Hideshima T., Chauhan D., Schlossman R., Richardson P., Anderson K.C. The role of tumor necrosis factor-α in the pathophysiology of human multiple myeloma: therapeutic applications. Oncogene 2001, 20(33):4519-4527.
35. Allen C., Saigal K., Nottingham L., Arun P., Chen Z., Van Waes C. Bortezomib-induced apoptosis with limited clinical response is accompanied by inhibition of canonical but not alternative nuclear factor κB subunits in head and neck cancer. Clin Cancer Res 2008, 14(13):4175-4185.
36. Jazirehi A.R., Economou J.S. Proteasome inhibition blocks NF-κB and ERK1/2 pathways, restores antigen expression, and sensitizes resistant human melanoma to TCR-engineered CTLs. Mol Cancer Ther 2012, 11(6):1332-1341.
37. Pham L.V., Tamayo A.T., Yoshimura L.C., Lo P., Ford R.J. Inhibition of constitutive NF-kappa B activation in mantle cell lymphoma B cells leads to induction of cell cycle arrest and apoptosis. J Immunol 2003, 171(1):88-95.
38. Bersani F., Taulli R., Accornero P., et al. Bortezomib-mediated proteasome inhibition as a potential strategy for the treatment of rhabdomyosarcoma. Eur J Cancer 2008, 44(6):876-884.
39. Keats J.J., Fonseca R., Chesi M., et al. Promiscuous mutations activate the noncanonical NF-kappaB pathway in multiple myeloma. Cancer Cell 2007, 12(2):131-144.
40. Annunziata C.M., Davis R.E., Demchenko Y., et al. Frequent engagement of the classical and alternative NF-kappaB pathways by diverse genetic abnormalities in multiple myeloma. Cancer Cell 2007, 12(2):115-130.
41. Demchenko Y.N., Glebov O.K., Zingone A., Keats J.J., Bergsagel P.L., Kuehl W.M. Classical and/or alternative NF-kappaB pathway activation in multiple myeloma. Blood 2010, 115(17):3541-3552.
42. Orlowski R.Z., Kuhn D.J. Proteasome inhibitors in cancer therapy: lessons from the first decade. Clin Cancer Res 2008, 14(6):1649-1657.
43. Smith M.H., Ploegh H.L., Weissman J.S. Road to ruin: targeting proteins for degradation in the endoplasmic reticulum. Science 2011, 334(6059):1086-1090.
44. Tabas I., Ron D. Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress. Nat Cell Biol 2011, 13(3):184-190.
45. Nawrocki S.T., Carew J.S., Dunner K., et al. Bortezomib inhibits PKR-like endoplasmic reticulum (ER) kinase and induces apoptosis via ER stress in human pancreatic cancer cells. Cancer Res 2005, 65(24):11510-11519.
46. Fribley A., Zeng Q., Wang C.Y. Proteasome inhibitor PS-341 induces apoptosis through induction of endoplasmic reticulum stress-reactive oxygen species in head and neck squamous cell carcinoma cells. Mol Cell Biol 2004, 24(22):9695-9704.
47. Fels D.R., Ye J., Segan A.T., et al. Preferential cytotoxicity of bortezomib toward hypoxic tumor cells via overactivation of endoplasmic reticulum stress pathways. Cancer Res 2008, 68(22):9323-9330.
48. Lee A.H., Iwakoshi N.N., Anderson K.C., Glimcher L.H. Proteasome inhibitors disrupt the unfolded protein response in myeloma cells. Proc Nat Acad Sci USA 2003, 100:9946-9951.
49. Obeng E.A., Carlson L.M., Gutman D.M., Harrington W.J., Lee K.P., Boise L.H. Proteasome inhibitors induce a terminal unfolded protein response in multiple myeloma cells. Blood 2006, 107(12):4907-4916.
50. Palombella V.J., Rando O.J., Goldberg A.L., Maniatis T. The ubiquitin-proteasome pathway is required for processing the NF-kappa B1 precursor protein and the activation of NF-κB. Cell 1994, 78(5):773-785.
51. Nemeth Z.H., Wong H.R., Odoms K., et al. Proteasome inhibitors induce inhibitory kappa B (I kappa B) kinase activation, I kappa B alpha degradation, and nuclear factor kappa B activation in HT-29 cells. Mol Pharmacol 2004, 65(2):342-349.
52. Hideshima T., Chauhan D., Richardson P., et al. NF-(B as a therapeutic target in multiple myeloma. J Biol Chem 2002, 277(19):16639-16647.
53. Hideshima T., Ikeda H., Chauhan D., et al. Bortezomib induces canonical nuclear factor-kappaB activation in multiple myeloma cells. Blood 2009, 114(5):1046-1052.
54. Holbeck S.L., Collins J.M., Doroshow J.H. Analysis of Food and Drug Administration-approved anticancer agents in the NCI60 panel of human tumor cell lines. Mol Cancer Ther 2010, 9(5):1451-1460.
55. Milano A., Iaffaioli R.V., Caponigro F. The proteasome: a worthwhile target for the treatment of solid tumours?. Eur J Cancer 2007, 43(7):1125-1133.
56. Caravita T., de Fabritiis P., Palumbo A., Amadori S., Boccadoro M. Bortezomib: efficacy comparisons in solid tumors and hematologic malignancies. Nat Clin Pract Oncol 2006, 3(7):374-387.
57. Borrell B. How accurate are cancer cell lines?. Nature 2010, 463(7283):858.
58. Sandberg R., Ernberg I. The molecular portrait of in vitro growth by meta-analysis of gene-expression profiles. Genome Biol 2005, 6(8):R65.
59. Pan C., Kumar C., Bohl S., Klingmueller U., Mann M. Comparative proteomic phenotyping of cell lines and primary cells to assess preservation of cell type-specific functions. Mol Cell Proteomics 2009, 8(3):443-450.
60. Powers E.T., Morimoto R.I., Dillin A., Kelly J.W., Balch W.E. Biological and chemical approaches to diseases of proteostasis deficiency. Annu Rev Biochem 2009, 78:959-991.
61. Williamson M.J., Silva M.D., Terkelsen J., et al. The relationship among tumor architecture, pharmacokinetics, pharmacodynamics, and efficacy of bortezomib in mouse xenograft models. Mol Cancer Ther 2009, 8(12):3234-3243.
62. Driscoll J.J., Minter A., Driscoll D.A., Burris J.K. The ubiquitin+proteasome protein degradation pathway as a therapeutic strategy in the treatment of solid tumor malignancies. Anticancer Agents Med Chem 2011, 11(2):242-246.
63. Cvek B. Ixazomib citrate, proteasome inhibitor oncolytic. Drug Future 2012, 37(8):561-565.
64. Kupperman E., Lee E.C., Cao Y., et al. Evaluation of the proteasome inhibitor MLN9708 in preclinical models of human cancer. Cancer Res 2010, 70(5):1970-1980.
65. Chauhan D., Tian Z., Zhou B., et al. In vitro and in vivo selective antitumor activity of a novel orally bioavailable proteasome inhibitor MLN9708 against multiple myeloma cells. Clin Cancer Res 2011, 17(16):5311-5321.
66. Tian Z., Zhao J.J., Tai Y.T., et al. Investigational agent MLN9708/2238 targets tumor-suppressor miR33b in MM cells. Blood 2012, 120(19):3958-3967.
67. Richardson P.G., Berdeja J.G., Niesvizky R., et al. Oral weekly MLN9708, an investigational proteasome inhibitor, in combination with lenalidomide and dexamethasone in patients (pts) with previ- ously untreated multiple myeloma (MM): a phase I/II study. J Clin Oncol 2012, 30(suppl). (abstr 8033).
68. Lonial S., Baz R.C., Wang M., et al. Phase I study of twice-weekly dosing of the investigational oral proteasome inhibitor MLN9708 in patients (pts) with relapsed and/or refractory multiple myeloma (MM). J Clin Oncol 2012, 30(suppl). (abstr 8017).
69. Smith D.C., Sullivan D., Infante J.R., et al. MLN9708, an investigational proteasome inhibitor, in patients (pts) with solid tumors: Updated phase I results. J Clin Oncol 2012, 30(suppl). (abstr e13603).
70. Papadopoulos K.P., Burris H.A., Gordon M., et al. A phase I/II study of carfilzomib 2-10-min infusion in patients with advanced solid tumors. Cancer Chemother Pharmacol 2013, 72(4):861-868.
71. Gomez A.M., Willcox N., Molenaar P.C., et al. Targeting plasma cells with proteasome inhibitors: possible roles in treating myasthenia gravis. Ann NY Acad Sci 2012, 1274:48-59.
72. Lifter J., Kincade P.W., Choi Y.S. Subpopulations of chicken B lymphocytes. J Immunol 1976, 117(6):2220-2225.
73. Lipsky P.E. Systemic lupus erythematosus: an autoimmune disease of B cell hyperactivity. Nat Immunol 2001, 2(9):764-766.
74. Díaz-Manera J., Martinez-Hernandez E., Querol L., et al. Long-lasting treatment effect of rituximab in MuSK myasthenia. Neurology 2012, 78(3):189-193.
75. Gehrs B.C., Friedberg R.C. Autoimmune hemolytic anemia. Am J Hematol 2002, 69(4):258-271.
76. Hoyer B.F., Manz R.A., Radbruch A., Hiepe F. Long-lived plasma cells and their contribution to autoimmunity. Ann NY Acad Sci 2005, 1050:124-133.
77. Cascio P., Oliva L., Cerruti F., et al. Dampening Ab responses using proteasome inhibitors following in vivo B cell activation. Eur J Immunol 2008, 38(3):658-667.
78. Neubert K., Meister S., Moser K., et al. The proteasome inhibitor bortezomib depletes plasma cells and protects mice with lupus-like disease from nephritis. Nat Med 2008, 14(7):748-755.
79. Ichikawa H.T., Conley T., Muchamuel T., et al. Beneficial effect of novel proteasome inhibitors in murine lupus via dual inhibition of type I interferon and autoantibody-secreting cells. Arthritis Rheum 2012, 64(2):493-503.
80. Seavey M.M., Lu L.D., Stump K.L., Wallace N.H., Ruggeri B.A. Novel, orally active, proteasome inhibitor, delanzomib (CEP-18770), ameliorates disease symptoms and glomerulonephritis in two preclinical mouse models of SLE. Int Immunopharmacol 2012, 12(1):257-270.
81. Gomez A.M., Vrolix K., Martinez-Martinez P., et al. Proteasome inhibition with bortezomib depletes plasma cells and autoantibodies in experimental autoimmune myasthenia gravis. J Immunol 2011, 186(4):2503-2513.
82. Meslier Y., Andre S., Dimitrov J.D., et al. Bortezomib delays the onset of factor VIII inhibitors in experimental hemophilia A, but fails to eliminate established anti-factor VIII IgG-producing cells. J Thromb Haemost 2011, 9(4):719-728.
83. Sadaka B., Alloway R.R., Shields A.R., Schmidt N.M., Woodle E.S. Proteasome inhibition for antibody-mediated allograft rejection. Semin Hematol 2012, 49(3):263-269.
84. Schroyens W., O'Connell C., Sykes D.B. Complete and partial responses of the TEMPI syndrome to bortezomib. N Engl J Med 2012, 367(8):778-780.
85. Sykes D.B., Schroyens W., O'Connell C. The TEMPI syndrome-a novel multisystem disease. N Engl J Med 2011, 365(5):475-477.
86. Shortt J., Oh D.H., Opat S.S. ADAMTS13 antibody depletion by bortezomib in thrombotic thrombocytopenic purpura. N Engl J Med 2013, 368(1):90-92.
87. Deng S., Zhou H., Xiong R., et al. Over-expression of genes and proteins of ubiquitin specific peptidases (USPs) and proteasome subunits (PSs) in breast cancer tissue observed by the methods of RFDD-PCR and proteomics. Breast Cancer Res Treat 2007, 104(1):21-30.
88. Geiger T., Wehner A., Schaab C., Cox J., Mann M. Comparative proteomic analysis of eleven common cell lines reveals ubiquitous but varying expression of most proteins. Mol Cell Proteomics 2012, 11(3). (M111.014050). http://www.ncbi.nlm.nih.gov/pubmed/%3Fterm=Geiger+T%2C+Wehner+A.
89. Ross D.T., Scherf U., Eisen M.B., et al. Systematic variation in gene expression patterns in human cancer cell lines. Nat Genet 2000, 24(3):227-235.
90. Moghaddas Gholami A., Hahne H., Wu Z., et al. Global proteome analysis of the NCI-60 cell line panel. Cell Rep 2013, 4(3):609-620.
91. Codony-Servat J., Tapia M.A., Bosch M., et al. Differential cellular and molecular effects of bortezomib, a proteasome inhibitor, in human breast cancer cells. Mol Cancer Ther 2006, 5(3):665-675.
92. Bianchi G., Oliva L., Cascio P., et al. The proteasome load versus capacity balance determines apoptotic sensitivity of multiple myeloma cells to proteasome inhibition. Blood 2009, 113(13):3040-3049.
93. Meister S., Schubert U., Neubert K., et al. Extensive immunoglobulin production sensitizes myeloma cells for proteasome inhibition. Cancer Res 2007, 67(4):1783-1792.
94. Schubert U., Anton L.C., Gibbs J., Norbury C.C., Yewdell J.W., Bennink J.R. Rapid degradation of a large fraction of newly synthesized proteins by proteasomes. Nature 2000, 404(6779):770-774.
95. Qian S.B., Princiotta M.F., Bennink J.R., Yewdell J.W. Characterization of rapidly degraded polypeptides in mammalian cells reveals a novel layer of nascent protein quality control. J Biol Chem 2006, 281(1):392-400.
96. Cenci S., Oliva L., Cerruti F., et al. Pivotal advance: protein synthesis modulates responsiveness of differentiating and malignant plasma cells to proteasome inhibitors. J Leukoc Biol 2012, 92(5):921-931.
97. Cenci S., Mezghrani A., Cascio P., et al. Progressively impaired proteasomal capacity during terminal plasma cell differentiation. EMBO J 2006, 25(5):1104-1113.
98. Santo L., Hideshima T., Kung A.L., et al. Preclinical activity, pharmacodynamic, and pharmacokinetic properties of a selective HDAC6 inhibitor, ACY-1215, in combination with bortezomib in multiple myeloma. Blood 2012, 119(11):2579-2589.
99. Richardson P.G., Schlossman R.L., Alsina M., et al. PANORAMA 2: panobinostat in combination with bortezomib and dexamethasone in patients with relapsed and bortezomib-refractory myeloma. Blood 2013, 122(14):2331-2337.
100. Auner H.W., Moody A.M., Ward T.H., et al. Combined inhibition of p97 and the proteasome causes lethal disruption of the secretory apparatus in multiple myeloma cells. PLoS One 2013, 8(9):e74415.
101. Mitsiades C.S., Mitsiades N.S., McMullan C.J., et al. Antimyeloma activity of heat shock protein-90 inhibition. Blood 2006, 107(3):1092-1100.
102. Yerlikaya A., Okur E., Eker S., Erin N. Combined effects of the proteasome inhibitor bortezomib and Hsp70 inhibitors on the B16F10 melanoma cell line. Mol Med Rep 2010, 3(2):333-339.
103. Sonnemann J., Marx C., Becker S., et al. p53-dependent and p53-independent anticancer effects of different histone deacetylase inhibitors. Br J Cancer 2014, 110(3):656-667.
104. Orlowski R.Z. Novel agents for multiple myeloma to overcome resistance in phase III clinical trials. Semin Oncol 2013, 40(5):634-651.
105. Lacy M.Q., McCurdy A.R. Pomalidomide. Blood 2013, 122(14):2305-2309.
106. McConkey D.J., Zhu K. Mechanisms of proteasome inhibitor action and resistance in cancer. Drug Resist Updat 2008, 11(4-5):164-179.
107. Kale A.J., Moore B.S. Molecular mechanisms of acquired proteasome inhibitor resistance. J Med Chem 2012, 55(23):10317-10327.
108. Ri M., Iida S., Nakashima T., et al. Bortezomib-resistant myeloma cell lines: a role for mutated PSMB5 in preventing the accumulation of unfolded proteins and fatal ER stress. Leukemia 2010, 24(8):1506-1512.
109. Franke N.E., Niewerth D., Assaraf Y.G., et al. Impaired bortezomib binding to mutant β5 subunit of the proteasome is the underlying basis for bortezomib resistance in leukemia cells. Leukemia 2012, 26(4):757-768.
110. 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(6):2489-2499.
111. Suzuki E., Demo S., Deu E., et al. Molecular mechanisms of bortezomib resistant adenocarcinoma cells. PLoS One 2011, 6(12):e27996.
112. Balsas P., Galan-Malo P., Marzo I., Naval J. Bortezomib resistance in a myeloma cell line is associated to PSMβ5 overexpression and polyploidy. Leuk Res 2012, 36(2):212-218.
113. Lu S., Yang J., Song X., et al. Point mutation of the proteasome beta5 subunit gene is an important mechanism of bortezomib resistance in bortezomib-selected variants of Jurkat T cell lymphoblastic lymphoma/leukemia line. J Pharmacol Exp Ther 2008, 326(2):423-431.
114. Lichter D.I., Danaee H., Pickard M.D., et al. Sequence analysis of β-subunit genes of the 20S proteasome in patients with relapsed multiple myeloma treated with bortezomib or dexamethasone. Blood 2012, 120(23):4513-4516.
115. Politou M., Karadimitris A., Terpos E., Kotsianidis I., Apperley J.F., Rahemtulla A. No evidence of mutations of the PSMB5 (beta-5 subunit of proteasome) in a case of myeloma with clinical resistance to bortezomib. Leuk Res 2006, 30(2):240-241.
116. Catley L., Weisberg E., Kiziltepe T., et al. Aggresome induction by proteasome inhibitor bortezomib and alpha-tubulin hyperacetylation by tubulin deacetylase (TDAC) inhibitor LBH589 are synergistic in myeloma cells. Blood 2006, 108(10):3441-3449.
117. Mitsiades C.S., Mitsiades N.S., McMullan C.J., et al. Transcriptional signature of histone deacetylase inhibition in multiple myeloma: biological and clinical implications. Proc Nat Acad Sci USA 2004, 101(2):540-545.
118. Weber D.M., Graef T., Hussein M., et al. Phase I trial of vorinostat combined with bortezomib for the treatment of relapsing and/or refractory multiple myeloma. Clin Lymphoma Myeloma Leuk 2012, 12(5):319-324.
119. San-Miguel J.F., Richardson P.G., Gunther A., et al. Phase Ib study of panobinostat and bortezomib in relapsed or relapsed and refractory multiple myeloma. J Clin Oncol 2013, 31(29):3696-3703.
120. Stessman H.A., Mansoor A., Zhan F., Linden M.A., Van Ness B., Baughn L.B. Bortezomib resistance can be reversed by induced expression of plasma cell maturation markers in a mouse in vitro model of multiple myeloma. PLoS One 2013, 8(10):e77608.
121. Gu J.L., Li J., Zhou Z.H., et al. Differentiation induction enhances bortezomib efficacy and overcomes drug resistance in multiple myeloma. Biochem Biophys Res Commun 2012, 420(3):644-650.
122. Leung-Hagesteijn C., Erdmann N., Cheung G., et al. Xbp1s-negative tumor B cells and pre-plasmablasts mediate therapeutic proteasome inhibitor resistance in multiple myeloma. Cancer Cell 2013, 24(3):289-304.
123. Ling S.C., Lau E.K., Al-Shabeeb A., et al. Response of myeloma to the proteasome inhibitor bortezomib is correlated with the unfolded protein response regulator XBP-1. Haematologica 2012, 97(1):64-72.
124. Chapman M.A., Lawrence M.S., Keats J.J., et al. Initial genome sequencing and analysis of multiple myeloma. Nature 2011, 471(7339):467-472.
125. Tian Z., D'Arcy P., Wang X., et al. A novel small molecule inhibitor of deubiquitylating enzyme USP14 and UCHL5 induces apoptosis in multiple myeloma and overcomes bortezomib resistance. Blood 2014, 123(5):706-716.
126. Anchoori R.K., Karanam B., Peng S., et al. A bis-benzylidine piperidone targeting proteasome ubiquitin receptor RPN13/ADRM1 as a therapy for cancer. Cancer Cell 2013, 24(6):791-805.
127. Chauhan D., Tian Z., Nicholson B., et al. A small molecule inhibitor of ubiquitin-specific protease-7 induces apoptosis in multiple myeloma cells and overcomes bortezomib resistance. Cancer Cell 2012, 22(3):345-358.