Login Register Cart 0
Review Article

The Ubiquitin-Proteasome Pathway and Resistance Mechanisms Developed Against the Proteasomal Inhibitors in Cancer Cells

Author(s): Azmi Yerlikaya* and Ertan Kanbur

Volume 21, Issue 13, 2020

Page: [1313 - 1325] Pages: 13

DOI: 10.2174/1389450121666200525004714

Price: $65

Abstract

Background: The ubiquitin-proteasome pathway is crucial for all cellular processes and is, therefore, a critical target for the investigation and development of novel strategies for cancer treatment. In addition, approximately 30% of newly synthesized proteins never attain their final conformations due to translational errors or defects in post-translational modifications; therefore, they are also rapidly eliminated by the ubiquitin-proteasome pathway.

Objective: Here, an effort was made to outline the recent findings deciphering the new molecular mechanisms involved in the regulation of ubiquitin-proteasome pathway as well as the resistance mechanisms developed against proteasome inhibitors in cell culture experiments and in the clinical trials.

Results: Since cancer cells have higher proliferation rates and are more prone to translational errors, they require the ubiquitin-proteasome pathway for selective advantage and sustained proliferation. Therefore, drugs targeting the ubiquitin-proteasome pathway are promising agents for the treatment of both hematological and solid cancers.

Conclusion: A number of proteasome inhibitors are approved and used for the treatment of advanced and relapsed multiple myeloma. Unfortunately, drug resistance mechanisms may develop very fast within days of the start of the proteasome inhibitor-treatment either due to the inherent or acquired resistance mechanisms under selective drug pressure. However, a comprehensive understanding of the mechanisms leading to the proteasome inhibitor-resistance will eventually help the design and development of novel strategies involving new drugs and/or drug combinations for the treatment of a number of cancers.

Keywords: Bortezomib, cancer, proteasome, resistance, ubiquitin, myeloma.

« Previous Next »
Graphical Abstract

[1]
Pohl C, Dikic I. Cellular quality control by the ubiquitin-proteasome system and autophagy. Science 2019; 366(6467): 818-22.
[http://dx.doi.org/10.1126/science.aax3769] [PMID: 31727826]
[2]
Wang F, Canadeo LA, Huibregtse JM. Ubiquitination of newly synthesized proteins at the ribosome. Biochimie 2015; 114: 127-33.
[http://dx.doi.org/10.1016/j.biochi.2015.02.006] [PMID: 25701549]
[3]
Drummond DA, Wilke CO. The evolutionary consequences of erroneous protein synthesis. Nat Rev Genet 2009; 10(10): 715-24.
[http://dx.doi.org/10.1038/nrg2662] [PMID: 19763154]
[4]
Schubert U, Antón LC, Gibbs J, Norbury CC, Yewdell JW, Bennink JR. Rapid degradation of a large fraction of newly synthesized proteins by proteasomes. Nature 2000; 404(6779): 770-4.
[http://dx.doi.org/10.1038/35008096] [PMID: 10783891]
[5]
Bastide A, David A. The ribosome, (slow) beating heart of cancer (stem) cell. Oncogenesis 2018; 7(4): 34.
[http://dx.doi.org/10.1038/s41389-018-0044-8] [PMID: 29674660]
[6]
Martineau Y, Müller D, Pyronnet S. Targeting protein synthesis in cancer cells. Oncoscience 2014; 1(7): 484-5.
[http://dx.doi.org/10.18632/oncoscience.63] [PMID: 25594050]
[7]
Vaklavas C, Blume SW, Grizzle WE. Translational dysregulation in cancer: molecular insights and potential clinical applications in biomarker development. Front Oncol 2017; 7: 158.
[http://dx.doi.org/10.3389/fonc.2017.00158] [PMID: 28798901]
[8]
Santos M, Fidalgo A, Varanda AS, Oliveira C, Santos MAS. tRNA deregulation and its consequences in cancer. Trends Mol Med 2019; 25(10): 853-65.
[http://dx.doi.org/10.1016/j.molmed.2019.05.011] [PMID: 31248782]
[9]
Luce MC, Tschanz KD, Gotto DA, Bunn CL. The accuracy of protein synthesis in reticulocyte and HeLa cell lysates. Biochim Biophys Acta 1985; 825(3): 280-8.
[http://dx.doi.org/10.1016/0167-4781(85)90015-6] [PMID: 4016118]
[10]
Pollard JW, Harley CB, Chamberlain JW, Goldstein S, Stanners CP. Is transformation associated with an increased error frequency in mammalian cells? J Biol Chem 1982; 257(11): 5977-9.
[PMID: 6281250]
[11]
Arlt A, Bauer I, Schafmayer C, et al. Increased proteasome subunit protein expression and proteasome activity in colon cancer relate to an enhanced activation of nuclear factor E2-related factor 2 (Nrf2). Oncogene 2009; 28(45): 3983-96.
[http://dx.doi.org/10.1038/onc.2009.264] [PMID: 19734940]
[12]
Chen L, Madura K. Increased proteasome activity, ubiquitin-conjugating enzymes, and eEF1A translation factor detected in breast cancer tissue. Cancer Res 2005; 65(13): 5599-606.
[http://dx.doi.org/10.1158/0008-5472.CAN-05-0201] [PMID: 15994932]
[13]
Stoebner PE, Lavabre-Bertrand T, Henry L, et al. High plasma proteasome levels are detected in patients with metastatic malignant melanoma. Br J Dermatol 2005; 152(5): 948-53.
[http://dx.doi.org/10.1111/j.1365-2133.2005.06487.x] [PMID: 15888151]
[14]
Chen L, Brewer MD, Guo L, Wang R, Jiang P, Yang X. Enhanced degradation of misfolded proteins promotes tumorigenesis. Cell Rep 2017; 18(13): 3143-54.
[http://dx.doi.org/10.1016/j.celrep.2017.03.010] [PMID: 28355566]
[15]
de Martino M, Hoetzenecker K, Ankersmit HJ, et al. Serum 20S proteasome is elevated in patients with renal cell carcinoma and associated with poor prognosis. Br J Cancer 2012; 106(5): 904-8.
[http://dx.doi.org/10.1038/bjc.2012.20] [PMID: 22294183]
[16]
Dutaud D, Aubry L, Henry L, et al. Development and evaluation of a sandwich ELISA for quantification of the 20S proteasome in human plasma. J Immunol Methods 2002; 260(1-2): 183-93.
[http://dx.doi.org/10.1016/S0022-1759(01)00555-5] [PMID: 11792388]
[17]
Lavabre-Bertrand T, Henry L, Carillo S, et al. Plasma proteasome level is a potential marker in patients with solid tumors and hemopoietic malignancies. Cancer 2001; 92(10): 2493-500.
[http://dx.doi.org/10.1002/1097-0142(20011115)92:10<2493::AID-CNCR1599>3.0.CO;2-F] [PMID: 11745181]
[18]
Wei X, Zeng W, Xie K, Diao P, Tang P. Potential use of chymotrypsin-like proteasomal activity as a biomarker for prostate cancer. Oncol Lett 2018; 15(4): 5149-54.
[http://dx.doi.org/10.3892/ol.2018.7936] [PMID: 29552150]
[19]
Rock KL, Gramm C, Rothstein L, et al. Inhibitors of the proteasome block the degradation of most cell proteins and the generation of peptides presented on MHC class I molecules. Cell 1994; 78(5): 761-71.
[http://dx.doi.org/10.1016/S0092-8674(94)90462-6] [PMID: 8087844]
[20]
Yerlikaya A, Yöntem M. The significance of ubiquitin proteasome pathway in cancer development. Recent Patents Anticancer Drug Discov 2013; 8(3): 298-309.
[http://dx.doi.org/10.2174/1574891X113089990033] [PMID: 23061719]
[21]
Schmidt M, Finley D. Regulation of proteasome activity in health and disease. Biochim Biophys Acta 2014; 1843(1): 13-25.
[http://dx.doi.org/10.1016/j.bbamcr.2013.08.012] [PMID: 23994620]
[22]
Ross JM, Olson L, Coppotelli G. Mitochondrial and ubiquitin proteasome system dysfunction in ageing and disease: two sides of the same coin? Int J Mol Sci 2015; 16(8): 19458-76.
[http://dx.doi.org/10.3390/ijms160819458] [PMID: 26287188]
[23]
Schulman BA, Harper JW. Ubiquitin-like protein activation by E1 enzymes: the apex for downstream signalling pathways. Nat Rev Mol Cell Biol 2009; 10(5): 319-31.
[http://dx.doi.org/10.1038/nrm2673] [PMID: 19352404]
[24]
Best S, Hashiguchi T, Kittai A, et al. Targeting ubiquitin-activating enzyme induces ER stress-mediated apoptosis in B-cell lymphoma cells. Blood Adv 2019; 3(1): 51-62.
[http://dx.doi.org/10.1182/bloodadvances.2018026880] [PMID: 30617217]
[25]
García-Gutiérrez L, Delgado MD, León J. MYC oncogene contributions to release of cell cycle brakes. Genes (Basel) 2019; 10(3) E244.
[http://dx.doi.org/10.3390/genes10030244] [PMID: 30909496]
[26]
Stewart MD, Ritterhoff T, Klevit RE, Brzovic PS. E2 enzymes: more than just middle men. Cell Res 2016; 26(4): 423-40.
[http://dx.doi.org/10.1038/cr.2016.35] [PMID: 27002219]
[27]
Guo J, Wang M, Wang JP, Wu CX. Ubiquitin-conjugating enzyme E2T knockdown suppresses hepatocellular tumorigenesis via inducing cell cycle arrest and apoptosis. World J Gastroenterol 2019; 25(43): 6386-403.
[http://dx.doi.org/10.3748/wjg.v25.i43.6386] [PMID: 31798276]
[28]
Berndsen CE, Wolberger C. New insights into ubiquitin E3 ligase mechanism. Nat Struct Mol Biol 2014; 21(4): 301-7.
[http://dx.doi.org/10.1038/nsmb.2780] [PMID: 24699078]
[29]
George AJ, Hoffiz YC, Charles AJ, Zhu Y, Mabb AM. A comprehensive atlas of E3 ubiquitin ligase mutations in neurological disorders. Front Genet 2018; 9: 29.
[http://dx.doi.org/10.3389/fgene.2018.00029] [PMID: 29491882]
[30]
Jiang Y, Su S, Zhang Y, Qian J, Liu P. Control of mTOR signaling by ubiquitin. Oncogene 2019; 38(21): 3989-4001.
[http://dx.doi.org/10.1038/s41388-019-0713-x] [PMID: 30705402]
[31]
Wang D, Ma L, Wang B, Liu J, Wei W. E3 ubiquitin ligases in cancer and implications for therapies. Cancer Metastasis Rev 2017; 36(4): 683-702.
[http://dx.doi.org/10.1007/s10555-017-9703-z] [PMID: 29043469]
[32]
Cho Y, Kang HG, Kim SJ, et al. Post-translational modification of OCT4 in breast cancer tumorigenesis. Cell Death Differ 2018; 25(10): 1781-95.
[http://dx.doi.org/10.1038/s41418-018-0079-6] [PMID: 29511337]
[33]
Li F, Xie P, Fan Y, et al. C terminus of Hsc70-interacting protein promotes smooth muscle cell proliferation and survival through ubiquitin-mediated degradation of FoxO1. J Biol Chem 2009; 284(30): 20090-8.
[http://dx.doi.org/10.1074/jbc.M109.017046] [PMID: 19483080]
[34]
Ahmed SF, Deb S, Paul I, et al. The chaperone-assisted E3 ligase C terminus of Hsc70-interacting protein (CHIP) targets PTEN for proteasomal degradation. J Biol Chem 2012; 287(19): 15996-6006.
[http://dx.doi.org/10.1074/jbc.M111.321083] [PMID: 22427670]
[35]
Lü S, Wang J. The resistance mechanisms of proteasome inhibitor bortezomib. Biomark Res 2013; 1(1): 13.
[http://dx.doi.org/10.1186/2050-7771-1-13] [PMID: 24252210]
[36]
Morozov AV, Karpov VL. Proteasomes and several aspects of their heterogeneity relevant to cancer. Front Oncol 2019; 9(761): 761.
[http://dx.doi.org/10.3389/fonc.2019.00761] [PMID: 31456945]
[37]
Morozov AV, Karpov VL. Biological consequences of structural and functional proteasome diversity. Heliyon 2018; 4(10) e00894.
[http://dx.doi.org/10.1016/j.heliyon.2018.e00894] [PMID: 30417153]
[38]
Toste Rego A, da Fonseca PCA. Characterization of fully recombinant human 20S and 20S-PA200 proteasome complexes. Mol Cell 2019; 76(1): 138-47.e135.
[39]
Ciechanover A, Schwartz AL. The ubiquitin-proteasome pathway: the complexity and myriad functions of proteins death. Proc Natl Acad Sci USA 1998; 95(6): 2727-30.
[http://dx.doi.org/10.1073/pnas.95.6.2727] [PMID: 9501156]
[40]
Bogyo M, McMaster JS, Gaczynska M, Tortorella D, Goldberg AL, Ploegh H. Covalent modification of the active site threonine of proteasomal beta subunits and the Escherichia coli homolog HslV by a new class of inhibitors. Proc Natl Acad Sci USA 1997; 94(13): 6629-34.
[http://dx.doi.org/10.1073/pnas.94.13.6629] [PMID: 9192616]
[41]
Fenteany G, Standaert RF, Lane WS, Choi S, Corey EJ, Schreiber SL. Inhibition of proteasome activities and subunit-specific amino-terminal threonine modification by lactacystin. Science 1995; 268(5211): 726-31.
[http://dx.doi.org/10.1126/science.7732382] [PMID: 7732382]
[42]
Skerget S, Rosenow M, Polpitiya A, Petritis K, Dorus S, Karr TL. The Rhesus macaque (Macaca mulatta) sperm proteome. Mol Cell Proteomics 2013; 12(11): 3052-67.
[http://dx.doi.org/10.1074/mcp.M112.026476] [PMID: 23816990]
[43]
Tanaka K. The proteasome: overview of structure and functions. Proc Jpn Acad, Ser B, Phys Biol Sci 2009; 85(1): 12-36.
[http://dx.doi.org/10.2183/pjab.85.12] [PMID: 19145068]
[44]
Coffino P. Antizyme, a mediator of ubiquitin-independent proteasomal degradation. Biochimie 2001; 83(3-4): 319-23.
[http://dx.doi.org/10.1016/S0300-9084(01)01252-4] [PMID: 11295492]
[45]
Dyson HJ, Wright PE. Intrinsically unstructured proteins and their functions. Nat Rev Mol Cell Biol 2005; 6(3): 197-208.
[http://dx.doi.org/10.1038/nrm1589] [PMID: 15738986]
[46]
van der Lee R, Lang B, Kruse K, et al. Intrinsically disordered segments affect protein half-life in the cell and during evolution. Cell Rep 2014; 8(6): 1832-44.
[http://dx.doi.org/10.1016/j.celrep.2014.07.055] [PMID: 25220455]
[47]
Moscovitz O, Ben-Nissan G, Fainer I, Pollack D, Mizrachi L, Sharon M. The Parkinson’s-associated protein DJ-1 regulates the 20S proteasome. Nat Commun 2015; 6: 6609.
[http://dx.doi.org/10.1038/ncomms7609] [PMID: 25833141]
[48]
Asher G, Tsvetkov P, Kahana C, Shaul Y. A mechanism of ubiquitin-independent proteasomal degradation of the tumor suppressors p53 and p73. Genes Dev 2005; 19(3): 316-21.
[http://dx.doi.org/10.1101/gad.319905] [PMID: 15687255]
[49]
Moscovitz O, Tsvetkov P, Hazan N, et al. A mutually inhibitory feedback loop between the 20S proteasome and its regulator, NQO1. Mol Cell 2012; 47(1): 76-86.
[http://dx.doi.org/10.1016/j.molcel.2012.05.049] [PMID: 22793692]
[50]
Olshina MA, Arkind G, Kumar Deshmukh F, et al. Regulation of the 20S proteasome by a novel family of inhibitory proteins. Antioxid Redox Signal 2020; 32(9): 636-55.
[http://dx.doi.org/10.1089/ars.2019.7816] [PMID: 31903784]
[51]
Dinkova-Kostova AT, Talalay P. NAD(P)H:quinone acceptor oxidoreductase 1 (NQO1), a multifunctional antioxidant enzyme and exceptionally versatile cytoprotector. Arch Biochem Biophys 2010; 501(1): 116-23.
[http://dx.doi.org/10.1016/j.abb.2010.03.019] [PMID: 20361926]
[52]
Sollner S, Schober M, Wagner A, et al. Quinone reductase acts as a redox switch of the 20S yeast proteasome. EMBO Rep 2009; 10(1): 65-70.
[http://dx.doi.org/10.1038/embor.2008.218] [PMID: 19029946]
[53]
Richardson PG, Anderson KC. Bortezomib: a novel therapy approved for multiple myeloma. Clin Adv Hematol Oncol 2003; 1(10): 596-600.
[PMID: 16258456]
[54]
Park JE, Miller Z, Jun Y, Lee W, Kim KB. Next-generation proteasome inhibitors for cancer therapy. Transl Res 2018; 198: 1-16.
[http://dx.doi.org/10.1016/j.trsl.2018.03.002] [PMID: 29654740]
[55]
Berkers CR, Verdoes M, Lichtman E, et al. Activity probe for in vivo profiling of the specificity of proteasome inhibitor bortezomib. Nat Methods 2005; 2(5): 357-62.
[http://dx.doi.org/10.1038/nmeth759] [PMID: 15846363]
[56]
Chen D, Frezza M, Schmitt S, Kanwar J, Dou QP. Bortezomib as the first proteasome inhibitor anticancer drug: current status and future perspectives. Curr Cancer Drug Targets 2011; 11(3): 239-53.
[http://dx.doi.org/10.2174/156800911794519752] [PMID: 21247388]
[57]
Aras B, Yerlikaya A. Bortezomib and etoposide combinations exert synergistic effects on the human prostate cancer cell line PC-3. Oncol Lett 2016; 11(5): 3179-84.
[http://dx.doi.org/10.3892/ol.2016.4340] [PMID: 27123085]
[58]
Appel A. Drugs: More shots on target. Nature 2011; 480(7377): S40-2.
[http://dx.doi.org/10.1038/480S40a] [PMID: 22169800]
[59]
Buac D, Shen M, Schmitt S, et al. From bortezomib to other inhibitors of the proteasome and beyond. Curr Pharm Des 2013; 19(22): 4025-38.
[http://dx.doi.org/10.2174/1381612811319220012] [PMID: 23181572]
[60]
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): 333-9.
[http://dx.doi.org/10.3892/mmr_000000262] [PMID: 21472244]
[61]
Hurchla MA, Garcia-Gomez A, Hornick MC, et al. The epoxyketone-based proteasome inhibitors carfilzomib and orally bioavailable oprozomib have anti-resorptive and bone-anabolic activity in addition to anti-myeloma effects. Leukemia 2013; 27(2): 430-40.
[http://dx.doi.org/10.1038/leu.2012.183] [PMID: 22763387]
[62]
Arastu-Kapur S, Anderl JL, Kraus M, et al. Nonproteasomal targets of the proteasome inhibitors bortezomib and carfilzomib: a link to clinical adverse events. Clin Cancer Res 2011; 17(9): 2734-43.
[http://dx.doi.org/10.1158/1078-0432.CCR-10-1950] [PMID: 21364033]
[63]
Richardson PG, Baz R, Wang M, et al. Phase 1 study of twice-weekly ixazomib, an oral proteasome inhibitor, in relapsed/refractory multiple myeloma patients. Blood 2014; 124(7): 1038-46.
[http://dx.doi.org/10.1182/blood-2014-01-548826] [PMID: 24920586]
[64]
Zhang J, Wu P, Hu Y. Clinical and marketed proteasome inhibitors for cancer treatment. Curr Med Chem 2013; 20(20): 2537-51.
[http://dx.doi.org/10.2174/09298673113209990122] [PMID: 23531219]
[65]
Li H, Chen Z, Hu T, et al. Novel proteasome inhibitor ixazomib sensitizes neuroblastoma cells to doxorubicin treatment. Sci Rep 2016; 6: 34397.
[http://dx.doi.org/10.1038/srep34397] [PMID: 27687684]
[66]
Hungria VTM, Crusoé EQ, Bittencourt RI, et al. New proteasome inhibitors in the treatment of multiple myeloma. Hematol Transfus Cell Ther 2019; 41(1): 76-83.
[http://dx.doi.org/10.1016/j.htct.2018.07.003] [PMID: 30793108]
[67]
Muz B, Ghazarian RN, Ou M, Luderer MJ, Kusdono HD, Azab AK. Spotlight on ixazomib: potential in the treatment of multiple myeloma. Drug Des Devel Ther 2016; 10: 217-26.
[PMID: 26811670]
[68]
Shi Y, Bieerkehazhi S, Ma H. Next-generation proteasome inhibitor oprozomib enhances sensitivity to doxorubicin in triple-negative breast cancer cells. Int J Clin Exp Pathol 2018; 11(5): 2347-55.
[PMID: 31938346]
[69]
Manasanch EE, Orlowski RZ. Proteasome inhibitors in cancer therapy. Nat Rev Clin Oncol 2017; 14(7): 417-33.
[http://dx.doi.org/10.1038/nrclinonc.2016.206] [PMID: 28117417]
[70]
Yerlikaya A, Erin N. Differential sensitivity of breast cancer and melanoma cells to proteasome inhibitor Velcade. Int J Mol Med 2008; 22(6): 817-23.
[PMID: 19020781]
[71]
Besse A, Besse L, Kraus M, et al. Proteasome inhibition in multiple myeloma: head-to-head comparison of currently available proteasome inhibitors. Cell Chem Biol 2019; 26(3): 340-51.e343.
[http://dx.doi.org/10.1016/j.chembiol.2018.11.007]
[72]
Di K, Lloyd GK, Abraham V, et al. Marizomib activity as a single agent in malignant gliomas: ability to cross the blood-brain barrier. Neuro-oncol 2016; 18(6): 840-8.
[http://dx.doi.org/10.1093/neuonc/nov299] [PMID: 26681765]
[73]
Rausch JL, Ali AA, Lee DM, et al. Differential antitumor activity of compounds targeting the ubiquitin-proteasome machinery in gastrointestinal stromal tumor (GIST) cells. Sci Rep 2020; 10(1): 5178.
[http://dx.doi.org/10.1038/s41598-020-62088-7] [PMID: 32198455]
[74]
Meena AS, Sharma A, Kumari R, Mohammad N, Singh SV, Bhat MK. Inherent and acquired resistance to paclitaxel in hepatocellular carcinoma: molecular events involved. PLoS One 2013; 8(4) e61524.
[http://dx.doi.org/10.1371/journal.pone.0061524] [PMID: 23613870]
[75]
Zahreddine H, Borden KL. Mechanisms and insights into drug resistance in cancer. Front Pharmacol 2013; 4: 28.
[http://dx.doi.org/10.3389/fphar.2013.00028] [PMID: 23504227]
[76]
Mansoori B, Mohammadi A, Davudian S, Shirjang S, Baradaran B. The Different mechanisms of cancer drug resistance: a brief review. Adv Pharm Bull 2017; 7(3): 339-48.
[http://dx.doi.org/10.15171/apb.2017.041] [PMID: 29071215]
[77]
Oerlemans R, Franke NE, Assaraf YG, et al. Molecular basis of bortezomib resistance: proteasome subunit beta5 (PSMB5) gene mutation and overexpression of PSMB5 protein. Blood 2008; 112(6): 2489-99.
[http://dx.doi.org/10.1182/blood-2007-08-104950] [PMID: 18565852]
[78]
Suzuki E, Demo S, Deu E, et al. Molecular mechanisms of bortezomib resistant adenocarcinoma cells. PLoS One 2011; 6(12) e27996.
[http://dx.doi.org/10.1371/journal.pone.0027996] [PMID: 22216088]
[79]
Wu YX, Yang JH, Saitsu H. Bortezomib-resistance is associated with increased levels of proteasome subunits and apoptosis-avoidance. Oncotarget 2016; 7(47): 77622-34.
[http://dx.doi.org/10.18632/oncotarget.12731] [PMID: 27769058]
[80]
Politou M, Karadimitris A, Terpos E, Kotsianidis I, Apperley JF, 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): 240-1.
[http://dx.doi.org/10.1016/j.leukres.2005.06.014] [PMID: 16081156]
[81]
Barrio S, Stühmer T, Da-Viá M, et al. Spectrum and functional validation of PSMB5 mutations in multiple myeloma. Leukemia 2019; 33(2): 447-56.
[http://dx.doi.org/10.1038/s41375-018-0216-8] [PMID: 30026573]
[82]
Jagannathan S, Vad N, Vallabhapurapu S, Vallabhapurapu S, Anderson KC, Driscoll JJ. MiR-29b replacement inhibits proteasomes and disrupts aggresome+autophagosome formation to enhance the antimyeloma benefit of bortezomib. Leukemia 2015; 29(3): 727-38.
[http://dx.doi.org/10.1038/leu.2014.279] [PMID: 25234165]
[83]
Albornoz N, Bustamante H, Soza A, Burgos P. Cellular responses to proteasome inhibition: molecular mechanisms and beyond. Int J Mol Sci 2019; 20(14) E3379.
[http://dx.doi.org/10.3390/ijms20143379] [PMID: 31295808]
[84]
Hao R, Nanduri P, Rao Y, et al. Proteasomes activate aggresome disassembly and clearance by producing unanchored ubiquitin chains. Mol Cell 2013; 51(6): 819-28.
[http://dx.doi.org/10.1016/j.molcel.2013.08.016] [PMID: 24035499]
[85]
Kaliszczak M, van Hechanova E, Li Y, et al. The HDAC6 inhibitor C1A modulates autophagy substrates in diverse cancer cells and induces cell death. Br J Cancer 2018; 119(10): 1278-87.
[http://dx.doi.org/10.1038/s41416-018-0232-5] [PMID: 30318510]
[86]
Moriya S, Komatsu S, Yamasaki K, et al. Targeting the integrated networks of aggresome formation, proteasome, and autophagy potentiates ER stress mediated cell death in multiple myeloma cells. Int J Oncol 2015; 46(2): 474-86.
[http://dx.doi.org/10.3892/ijo.2014.2773] [PMID: 25422130]
[87]
Hideshima T, Mazitschek R, Qi J, et al. HDAC6 inhibitor WT161 downregulates growth factor receptors in breast cancer. Oncotarget 2017; 8(46): 80109-23.
[http://dx.doi.org/10.18632/oncotarget.19019] [PMID: 29113288]
[88]
Stessman HA, Baughn LB, Sarver A, et al. Profiling bortezomib resistance identifies secondary therapies in a mouse myeloma model. Mol Cancer Ther 2013; 12(6): 1140-50.
[http://dx.doi.org/10.1158/1535-7163.MCT-12-1151] [PMID: 23536725]
[89]
Samali A, Cotter TG. Heat shock proteins increase resistance to apoptosis. Exp Cell Res 1996; 223(1): 163-70.
[http://dx.doi.org/10.1006/excr.1996.0070] [PMID: 8635489]
[90]
Wallington-Beddoe CT, Sobieraj-Teague M, Kuss BJ, Pitson SM. Resistance to proteasome inhibitors and other targeted therapies in myeloma. Br J Haematol 2018; 182(1): 11-28.
[http://dx.doi.org/10.1111/bjh.15210] [PMID: 29676460]
[91]
Yerlikaya A, DoKudur H. Investigation of the eIF2alpha phosphorylation mechanism in response to proteasome inhibition in melanoma and breast cancer cells. Mol Biol (Mosk) 2010; 44(5): 859-66.
[PMID: 21090173]
[92]
Chauhan D, Li G, Shringarpure R, et al. Blockade of Hsp27 overcomes Bortezomib/proteasome inhibitor PS-341 resistance in lymphoma cells. Cancer Res 2003; 63(19): 6174-7.
[PMID: 14559800]
[93]
Hamouda MA, Belhacene N, Puissant A, et al. The small heat shock protein B8 (HSPB8) confers resistance to bortezomib by promoting autophagic removal of misfolded proteins in multiple myeloma cells. Oncotarget 2014; 5(15): 6252-66.
[http://dx.doi.org/10.18632/oncotarget.2193] [PMID: 25051369]
[94]
Besse A, Stolze SC, Rasche L, et al. Carfilzomib resistance due to ABCB1/MDR1 overexpression is overcome by nelfinavir and lopinavir in multiple myeloma. Leukemia 2018; 32(2): 391-401.
[http://dx.doi.org/10.1038/leu.2017.212] [PMID: 28676669]
[95]
O’Connor R, Ooi MG, Meiller J, et al. The interaction of bortezomib with multidrug transporters: implications for therapeutic applications in advanced multiple myeloma and other neoplasias. Cancer Chemother Pharmacol 2013; 71(5): 1357-68.
[http://dx.doi.org/10.1007/s00280-013-2136-7] [PMID: 23589314]
[96]
Panischeva LA, Kakpakova ES, Rybalkina EY, Stavrovskaya AA. Influence of proteasome inhibitor bortezomib on the expression of multidrug resistance genes and Akt kinase activity. Biochemistry (Mosc) 2011; 76(9): 1009-16.
[http://dx.doi.org/10.1134/S0006297911090045] [PMID: 22082269]
[97]
Brünnert D, Kraus M, Stühmer T, et al. Novel cell line models to study mechanisms and overcoming strategies of proteasome inhibitor resistance in multiple myeloma. Biochim Biophys Acta Mol Basis Dis 2019; 1865(6): 1666-76.
[http://dx.doi.org/10.1016/j.bbadis.2019.04.003] [PMID: 30954557]
[98]
Lü 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. Exp Hematol 2009; 37(7): 831-7.
[http://dx.doi.org/10.1016/j.exphem.2009.04.001] [PMID: 19426847]
[99]
Franke NE, Niewerth D, Assaraf YG, 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): 757-68.
[http://dx.doi.org/10.1038/leu.2011.256] [PMID: 21941364]
[100]
Yerlikaya A, Okur E. An investigation of the mechanisms underlying the proteasome inhibitor bortezomib resistance in PC3 prostate cancer cell line. Cytotechnology 2020; 72(1): 121-30.
[http://dx.doi.org/10.1007/s10616-019-00362-x] [PMID: 31863311]
[101]
Weyburne ES, Wilkins OM, Sha Z, et al. Inhibition of the Proteasome β2 Site Sensitizes Triple-Negative Breast Cancer Cells to β5 Inhibitors and Suppresses Nrf1 Activation. Cell Chem Biol 2017; 24(2): 218-30.
[http://dx.doi.org/10.1016/j.chembiol.2016.12.016] [PMID: 28132893]
[102]
Li B, Fu J, Chen P, et al. The nuclear factor (erythroid-derived 2)-like 2 and proteasome maturation protein axis mediate bortezomib resistance in multiple myeloma. J Biol Chem 2015; 290(50): 29854-68.
[http://dx.doi.org/10.1074/jbc.M115.664953] [PMID: 26483548]
[103]
Xu H, Han H, Song S, et al. Exosome-transmitted PSMA3 and PSMA3-AS1 promote proteasome inhibitor resistance in multiple myeloma. Clin Cancer Res 2019; 25(6): 1923-35.
[http://dx.doi.org/10.1158/1078-0432.CCR-18-2363] [PMID: 30610101]
[104]
Radhakrishnan SK, Lee CS, Young P, Beskow A, Chan JY, Deshaies RJ. Transcription factor Nrf1 mediates the proteasome recovery pathway after proteasome inhibition in mammalian cells. Mol Cell 2010; 38(1): 17-28.
[http://dx.doi.org/10.1016/j.molcel.2010.02.029] [PMID: 20385086]
[105]
Sha Z, Goldberg AL. Proteasome-mediated processing of Nrf1 is essential for coordinate induction of all proteasome subunits and p97. Curr Biol 2014; 24(14): 1573-83.
[http://dx.doi.org/10.1016/j.cub.2014.06.004] [PMID: 24998528]
[106]
Zhang Y, Liu Y, Liu H, Tang WH. Exosomes: biogenesis, biologic function and clinical potential. Cell Biosci 2019; 9: 19.
[http://dx.doi.org/10.1186/s13578-019-0282-2] [PMID: 30815248]
[107]
Farrell ML, Reagan MR. Soluble and cell-cell-mediated drivers of proteasome inhibitor resistance in multiple myeloma. Front Endocrinol (Lausanne) 2018; 9: 218.
[http://dx.doi.org/10.3389/fendo.2018.00218] [PMID: 29765356]
[108]
Kuhn DJ, Berkova Z, Jones RJ, et al. Targeting the insulin-like growth factor-1 receptor to overcome bortezomib resistance in preclinical models of multiple myeloma. Blood 2012; 120(16): 3260-70.
[http://dx.doi.org/10.1182/blood-2011-10-386789] [PMID: 22932796]
[109]
Muguruma Y, Yahata T, Warita T, et al. Jagged1-induced Notch activation contributes to the acquisition of bortezomib resistance in myeloma cells. Blood Cancer J 2017; 7(12): 650.
[http://dx.doi.org/10.1038/s41408-017-0001-3] [PMID: 29242532]

Rights & Permissions Print Cite
Article Metrics
65
3
© 2024 Bentham Science Publishers | Privacy Policy