933
Views
24
CrossRef citations to date
0
Altmetric
Reviews

The proteasome: mechanisms of biology and markers of activity and response to treatment in multiple myeloma

, , , , , , , & show all
Pages 1707-1714 | Received 11 Mar 2013, Accepted 20 Jul 2013, Published online: 24 Jan 2014

References

  • Wilkinson KD, Urban MK, Haas AL. Ubiquitin is the ATP-dependent proteolysis factor I of rabbit reticulocytes. J Biol Chem 1980;255: 7529–7532.
  • Etlinger JD, Goldberg AL. A soluble ATP-dependent proteolytic system responsible for the degradation of abnormal proteins in reticulocytes. Proc Natl Acad Sci USA 1977;74:54–58.
  • Hershko A, Ciechanover A, Rose IA. Resolution of the ATP-dependent proteolytic system from reticulocytes:a component that interacts with ATP. Proc Natl Acad Sci USA 1979;76:3107–3110.
  • Ciechanover A, Elias S, Heller H, et al. Characterization of the heat-stable polypeptide of the ATP-dependent proteolytic system from reticulocytes. J Biol Chem 1980;255:7525–7528.
  • Hutter G, Rieken M, Pastore A, et al. The proteasome inhibitor bortezomib targets cell cycle and apoptosis and acts synergistically in a sequence-dependent way with chemotherapeutic agents in mantle cell lymphoma. Ann Hematol 2012;91:847–856.
  • Loir M, Caraty A, Lanneau M, et al. Purification and characterization of ubiquitin from mammalian testis. FEBS Lett 1984;169:199–204.
  • Hanna J, Meides A, Zhang DP, et al. A ubiquitin stress response induces altered proteasome composition. Cell 2007;129: 747–759.
  • Hanna J, Leggett DS, Finley D. Ubiquitin depletion as a key mediator of toxicity by translational inhibitors. Mol Cell Biol 2003; 23:9251–9261.
  • D’Arcy P, Brnjic S, Olofsson MH, et al. Inhibition of proteasome deubiquitinating activity as a new cancer therapy. Nat Med 2011;17: 1636–1640.
  • 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;22:345–358.
  • Handley PM, Mueckler M, Siegel NR, et al. Molecular cloning, sequence, and tissue distribution of the human ubiquitin- activating enzyme E1. Proc Natl Acad Sci USA 1991;88:258–262.
  • Jin J, Li X, Gygi SP, et al. Dual E1 activation systems for ubiquitin differentially regulate E2 enzyme charging. Nature 2007;447: 1135–1138.
  • Schulman BA, Harper JW. Ubiquitin-like protein activation by E1 enzymes: the apex for downstream signalling pathways. Nat Rev Mol Cell Biol 2009;10:319–331.
  • Li W, Bengtson MH, Ulbrich A, et al. Genome-wide and functional annotation of human E3 ubiquitin ligases identifies MULAN, a mitochondrial E3 that regulates the organelle's dynamics and signaling. PloS One 2008;3:e1487.
  • Mattern MR, Wu J, Nicholson B. Ubiquitin-based anticancer therapy: carpet bombing with proteasome inhibitors vs surgical strikes with E1, E2, E3, or DUB inhibitors. Biochim Biophys Acta 2012;1823:2014–2021.
  • Xu GW, Ali M, Wood TE, et al. The ubiquitin-activating enzyme E1 as a therapeutic target for the treatment of leukemia and multiple myeloma. Blood 2010;115:2251–2259.
  • Saeki Y, Tanaka K. Assembly and function of the proteasome. Methods Mol Biol 2012;832:315–337.
  • Glickman MH, Rubin DM, Coux O, et al. A subcomplex of the proteasome regulatory particle required for ubiquitin-conjugate degradation and related to the COP9-signalosome and eIF3. Cell 1998;94:615–623.
  • Verma R, Aravind L, Oania R, et al. Role of Rpn11 metalloprotease in deubiquitination and degradation by the 26S proteasome. Science 2002;298:611–615.
  • Yao T, Cohen RE. A cryptic protease couples deubiquitination and degradation by the proteasome. Nature 2002;419:403–407.
  • Lecker SH, Goldberg AL, Mitch WE. Protein degradation by the ubiquitin-proteasome pathway in normal and disease states. J Am Soc Nephrol 2006;17:1807–1819.
  • Murata S, Minami Y, Minami M, et al. CHIP is a chaperone-dependent E3 ligase that ubiquitylates unfolded protein. EMBO Rep 2001;2:1133–1138.
  • Shastri N, Schwab S, Serwold T. Producing nature's gene- chips: the generation of peptides for display by MHC class I molecules. Annu Rev Immunol 2002;20:463–493.
  • Kusmierczyk AR, Hochstrasser M. Some assembly required: dedicated chaperones in eukaryotic proteasome biogenesis. Biol Chem 2008;389:1143–1151.
  • Le Tallec B, Barrault MB, Courbeyrette R, et al. 20S proteasome assembly is orchestrated by two distinct pairs of chaperones in yeast and in mammals. Mol Cell 2007;27:660–674.
  • Hirano Y, Hendil KB, Yashiroda H, et al. A heterodimeric complex that promotes the assembly of mammalian 20S proteasomes. Nature 2005;437:1381–1385.
  • Ramos PC, Hockendorff J, Johnson ES, et al. Ump1p is required for proper maturation of the 20S proteasome and becomes its substrate upon completion of the assembly. Cell 1998;92:489–499.
  • Funakoshi M, Tomko RJ Jr, Kobayashi H, et al. Multiple assembly chaperones govern biogenesis of the proteasome regulatory particle base. Cell 2009;137:887–899.
  • Fukunaga K, Kudo T, Toh-e A, et al. Dissection of the assembly pathway of the proteasome lid in Saccharomyces cerevisiae. Biochem Biophys Res Commun 2010;396:1048–1053.
  • Groettrup M, Kraft R, Kostka S, et al. A third interferon- gamma-induced subunit exchange in the 20S proteasome. Eur J Immunol 1996;26:863–869.
  • Murata S, Sasaki K, Kishimoto T, et al. Regulation of CD8 + T cell development by thymus-specific proteasomes. Science 2007;316: 1349–1353.
  • Groettrup M, Kirk CJ, Basler M. Proteasomes in immune cells: more than peptide producers?Nat Rev Immunol 2010;10:73–78.
  • Orlowski RZ, Baldwin AS Jr. NF-kappaB as a therapeutic target in cancer. Trends Mol Med 2002;8:385–389.
  • Hideshima T, Mitsiades C, Akiyama M, et al. Molecular mechanisms mediating antimyeloma activity of proteasome inhibitor PS-341. Blood 2003;101:1530–1534.
  • Delic J, Masdehors P, Omura S, et al. The proteasome inhibitor lactacystin induces apoptosis and sensitizes chemo- and radioresistant human chronic lymphocytic leukaemia lymphocytes to TNF-alpha-initiated apoptosis. Br J Cancer 1998;77:1103–1107.
  • Cenci S, Mezghrani A, Cascio P, et al. Progressively impaired proteasomal capacity during terminal plasma cell differentiation. EMBO J 2006;25:1104–1113.
  • Masciarelli S, Fra AM, Pengo N, et al. CHOP-independent apoptosis and pathway-selective induction of the UPR in developing plasma cells. Mol Immunol 2010;47:1356–1365.
  • Kopito RR. Aggresomes, inclusion bodies and protein aggregation. Trends Cell Biol 2000;10:524–530.
  • Garcia-Mata R, Bebok Z, Sorscher EJ, et al. Characterization and dynamics of aggresome formation by a cytosolic GFP-chimera. J Cell Biol 1999;146:1239–1254.
  • Arrasate M, Mitra S, Schweitzer ES, et al. Inclusion body formation reduces levels of mutant huntingtin and the risk of neuronal death. Nature 2004;431:805–810.
  • Bowman AB, Yoo SY, Dantuma NP, et al. Neuronal dysfunction in a polyglutamine disease model occurs in the absence of ubiquitin-proteasome system impairment and inversely correlates with the degree of nuclear inclusion formation. Hum Mol Genet 2005;14: 679–691.
  • Wong ES, Tan JM, Soong WE, et al. Autophagy-mediated clearance of aggresomes is not a universal phenomenon. Hum Mol Genet 2008;17:2570–2582.
  • De Duve C, Pressman BC, Gianetto R, et al. Tissue fractionation studies. 6. Intracellular distribution patterns of enzymes in rat-liver tissue. Biochem J 1955;60:604–617.
  • Klionsky DJ. Autophagy: from phenomenology to molecular understanding in less than a decade. Nat Rev Mol Cell Biol 2007;8: 931–937.
  • Ashford TP, Porter KR. Cytoplasmic components in hepatic cell lysosomes. J Cell Biol 1962;12:198–202.
  • Hideshima T, Bradner JE, Wong J, et al. Small-molecule inhibition of proteasome and aggresome function induces synergistic antitumor activity in multiple myeloma. Proc Natl Acad Sci USA 2005;102: 8567–8572.
  • Santo L, Hideshima T, Kung AL, et al. Preclinical activity, pharmacodynamic, and pharmacokinetic properties of a selective HDAC6 inhibitor, ACY-1215, in combination with bortezomib in multiple myeloma.Blood 2012;119:2579–2589.
  • Hoang B, Benavides A, Shi Y, et al. Effect of autophagy on multiple myeloma cell viability. Mole Cancer Ther 2009;8:1974–1984.
  • Lamy L, Ngo VN, Emre NC, et al. Control of autophagic cell death by caspase-10 in multiple myeloma. Cancer cell 2013;23: 435–449.
  • Carroll RG, Martin SJ. Autophagy in multiple myeloma: what makes you stronger can also kill you. Cancer cell 2013;23:425–426.
  • 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;14:748–755.
  • Zinszner H, Kuroda M, Wang X, et al. CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev 1998;12:982–995.
  • Brewer JW, Diehl JA. PERK mediates cell-cycle exit during the mammalian unfolded protein response. Proc Natl Acad Sci USA 2000;97:12625–12630.
  • Hideshima T, Chauhan D, Richardson P, et al. NF-kappa B as a therapeutic target in multiple myeloma. J Biol Chem 2002;277: 16639–166347.
  • Obeng EA, Carlson LM, Gutman DM, et al. Proteasome inhibitors induce a terminal unfolded protein response in multiple myeloma cells. Blood 2006;107:4907–4916.
  • Wiest DL, Burkhardt JK, Hester S, et al. Membrane biogenesis during B cell differentiation:most endoplasmic reticulum proteins are expressed coordinately. J Cell Biol 1990;110:1501–1511.
  • Melnick J, Dul JL, Argon Y. Sequential interaction of the chaperones BiP and GRP94 with immunoglobulin chains in the endoplasmic reticulum. Nature 1994;370:373–375.
  • van Anken E, Romijn EP, Maggioni C, et al. Sequential waves of functionally related proteins are expressed when B cells prepare for antibody secretion. Immunity 2003;18:243–253.
  • Meister S, Schubert U, Neubert K, et al. Extensive immunoglobulin production sensitizes myeloma cells for proteasome inhibition. Cancer Res 2007;67:1783–1792.
  • 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;113:3040–3049.
  • Kisselev AF, van der Linden WA, Overkleeft HS. Proteasome inhibitors:an expanding army attacking a unique target. Chem Biol 2012;19:99–115.
  • Kisselev AF, Callard A, Goldberg AL. Importance of the different proteolytic sites of the proteasome and the efficacy of inhibitors varies with the protein substrate. J Biol Chem 2006;281: 8582–8590.
  • Richardson PG, Barlogie B, Berenson J, et al. A phase 2 study of bortezomib in relapsed, refractory myeloma. N Engl J Med 2003; 348:2609–2617.
  • Richardson PG, Barlogie B, Berenson J, et al. Extended follow- up of a phase II trial in relapsed, refractory multiple myeloma::final time-to-event results from the SUMMIT trial. Cancer 2006;106: 1316–1319.
  • Richardson PG, Sonneveld P, Schuster MW, et al. Bortezomib or high-dose dexamethasone for relapsed multiple myeloma. N Engl J Med 2005;352:2487–2498.
  • San Miguel JF, Schlag R, Khuageva NK, et al. Bortezomib plus melphalan and prednisone for initial treatment of multiple myeloma. N Engl J Med 2008;359:906–917.
  • Richardson PG, Weller E, Lonial S, et al. Lenalidomide, bortezomib, and dexamethasone combination therapy in patients with newly diagnosed multiple myeloma. Blood 2010;116:679–686.
  • van Rhee F, Szymonifka J, Anaissie E, et al. Total Therapy 3 for multiple myeloma: prognostic implications of cumulative dosing and premature discontinuation of VTD maintenance components, bortezomib, thalidomide, and dexamethasone, relevant to all phases of therapy. Blood 2010;116:1220–1227.
  • Cavo M, Tacchetti P, Patriarca F, et al. Bortezomib with thalidomide plus dexamethasone compared with thalidomide plus dexamethasone as induction therapy before, and consolidation therapy after, double autologous stem-cell transplantation in newly diagnosed multiple myeloma:a randomised phase 3 study. Lancet 2010;376:2075–2085.
  • 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;17:2734–2743.
  • FDA approves Kyprolis for some patients with multiple myeloma. 2012. Available from: www.fda.gov/NewsEvents/Newsroom/PressAnnouncements/ucm312920.htm
  • Wolf JL, Vij R, Lonial S, et al. Neurotoxic and peripheral neuropathic effects in preclinical and clinical studies of carfilzomib (CFZ), a novel proteasome inhibitor (PI). J Clin Oncol 2010;28(15 Suppl.): Abstract 8135.
  • Wang Y, Ai L, Cui G, et al. Once- versus twice-weekly bortezomib induction therapy with dexamethasone in newly diagnosed multiple myeloma. J Huazhong Univ Sci Technolog Med Sci 2012;32:495–500.
  • Moreau P, Pylypenko H, Grosicki S, et al. Subcutaneous versus intravenous administration of bortezomib in patients with relapsed multiple myeloma: a randomised, phase 3, non-inferiority study. Lancet Oncol 2011;12:431–440.
  • Richardson PG, Hideshima T, Anderson KC. Bortezomib (PS-341): a novel, first-in-class proteasome inhibitor for the treatment of multiple myeloma and other cancers. Cancer Control 2003;10:361–369.
  • Pan Y, Gao Y, Chen L, et al. Targeting autophagy augments in vitro and in vivo antimyeloma activity of DNA-damaging chemotherapy. Clin Cancer Res 2011;17:3248–3258.
  • Zeng R, Chen Y, Zhao S, et al. Autophagy counteracts apoptosis in human multiple myeloma cells exposed to oridonin in vitro via regulating intracellular ROS and SIRT1. Acta Pharmacol Sin 2012;33:91–100.
  • Sharma RC, Inoue S, Roitelman J, et al. Peptide transport by the multidrug resistance pump. J Biol Chem 1992;267:5731–5734.
  • de Jong MC, Slootstra JW, Scheffer GL, et al. Peptide transport by the multidrug resistance protein MRP1. Cancer Res 2001;61: 2552–2557.
  • Chauhan D, Li G, Shringarpure R, et al. Blockade of Hsp27 overcomes bortezomib/proteasome inhibitor PS-341 resistance in lymphoma cells. Cancer Res 2003;63:6174–6177.
  • 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: 2489–2499.
  • Vij R, Siegel D, Kaufman JL, et al. Results of an ongoing open-label, phase II study of carfilzomib in patients with relapsed and/or refractory multiple myeloma (R/R MM). J Clin Oncol 2010;28:15(Suppl.): Abstract 8000.
  • Badros A, Burger AM, Philip S, et al. Phase I study of vorinostat in combination with bortezomib for relapsed and refractory multiple myeloma. Clinical Cancer Res 2009;15:5250–5257.
  • Wada M, Kosaka M, Saito S, et al. Serum concentration and localization in tumor cells of proteasomes in patients with hematologic malignancy and their pathophysiologic significance. J Lab Clin Med 1993;121:215–223.
  • Hoffmann O, Heubner M, Anlasik T, et al. Circulating 20S proteasome in patients with non-metastasized breast cancer. Anticancer Res 2011;31:2197–2201.
  • Egerer K, Kuckelkorn U, Rudolph PE, et al. Circulating proteasomes are markers of cell damage and immunologic activity in autoimmune diseases. J Rheumatol 2002;29:2045–2052.
  • 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;152:948–953.
  • Roth GA, Moser B, Krenn C, et al. Heightened levels of circulating 20S proteasome in critically ill patients. Eur J Clin Invest 2005;35: 399–403.
  • Jakob C, Egerer K, Liebisch P, et al. Circulating proteasome levels are an independent prognostic factor for survival in multiple myeloma. Blood 2007;109:2100–2105.
  • 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;106:904–908.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.