Increased expression and altered subunit composition of proteasomes induced by continuous proteasome inhibition establish apoptosis resistance and hyperproliferation of Burkitt lymphoma cells

Journal of Cellular Biochemistry

Volumn 103, Issue 1, 2008, Pages 270-283

  Fuchs, Dominik ^a   Berges, Carsten ^a   Opelz, Gerhard ^a   Daniel, Volker ^a   Naujokat, Cord ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Adaptive modification; Apoptosis resistance; Bortezomib; Proteasome; Subunit composition

Indexed keywords

19S PROTEASOME; 20S PROTEASOME; BORTEZOMIB; CHYMOTRYPSIN; HEAT SHOCK PROTEIN 27; PEPTIDASE; PROTEASOME; PROTEASOME MATURATION PROTEIN; PROTEIN P53; PROTEIN SUBUNIT; STAUROSPORINE; UNCLASSIFIED DRUG;

ADAPTATION; APOPTOSIS; ARTICLE; BURKITT LYMPHOMA; CELL CYCLE PROGRESSION; CELL PROLIFERATION; CELL SURVIVAL; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; GAMMA IRRADIATION; HUMAN; HUMAN CELL; LYMPHOMA CELL; MOLECULAR WEIGHT; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DEGRADATION; PROTEIN EXPRESSION;

APOPTOSIS; BORONIC ACIDS; BURKITT LYMPHOMA; CELL LINE, TUMOR; CELL PROLIFERATION; ENZYME ACTIVATION; GLYCOPROTEINS; HEAT-SHOCK PROTEINS; HUMANS; NEOPLASM PROTEINS; P-GLYCOPROTEIN; POLYUBIQUITIN; PROTEASE INHIBITORS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN SUBUNITS; PYRAZINES; TUMOR SUPPRESSOR PROTEIN P53; UBIQUITINATION;

EUKARYOTA;

EID: 38149082008     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.21405     Document Type: Article

References (53)

1. Baumeister W, Walz J, Zühl F, Seemüller E. 1998. The proteasome: Paradigm of a self-compartmentalizing protease. Cell 92:367-380.
2. Bruey JM, Ducasse C, Bonniaud P, Ravagnan L, Susin SA, Diaz-Latoud C, Gurbuxani S, Arrigo AP, Kroemer G, Solary E, Garrido C. 2000. Hsp27 negatively regulates cell death by interacting with cytochrome c. Nat Cell Biol 2:645-652.
3. Chauhan D, Li G, Shringarpure R, Podar K, Ohtake Y, Hideshima T, Anderson KC. 2003. Blockade of Hsp27 overcomes Bortezomib/proteasome inhibitor PS-341 resistance in lymphoma cells. Cancer Res 63:6174-6177.
4. Chen F, Chang D, Goh M, Klibanov SA, Ljungman M. 2000. Role of p53 in cell cycle regulation and apoptosis following exposure to proteasome inhibitors. Cell Growth Differ 11:239-246.
5. Ciechanover A. 2006. The ubiquitin proteolytic system. Neurology 66:S7-S19.
6. Concannon CG, Koehler BF, Reimertz C, Murphy BM, Bonner C, Thurow N, Ward MW, Villunger A, Strasser A, Kogel D, Prehn JH. 2007. Apoptosis induced by proteasome inhibition in cancer cells: Predominant role of the p53/PUMA pathway. Oncogene 26:1681-1692.
7. Dahlmann B, Ruppert T, Kuehn L, Merforth S, Kloetzel PM. 2000. Different proteasome subtypes in a single tissue exhibit different enzymatic properties. J Mol Biol 303:643-653.
8. Dhein J, Walczak H, Bäumler C, Debatin KM, Krammer PH. 1995. Autocrine T-cell suicide mediated by APO-1/(Fas/CD95). Nature 373:438-441.
9. Dick TP, Nussbaum AK, Deeg M, Heinemeyer W, Groll M, Schirle M, Keilholz W, Stevanovic S, Wolf DH, Huber R, Rammensee HG, Schild H. 1998. Contribution of proteasomal beta-subunits to the cleavage of peptide substrates analyzed with yeast mutants. J Biol Chem 273:25637 25646.
10. Garrido C, Bruey JM, Fromentin A, Hammann A, Arrigo AP, Solary E. 1999. Hsp27 inhibits cytochrome c-dependent activation of procaspase-9. FASEB J 13: 2061-2070.
11. Gavioli R, Frisan T, Vertuani S, Bornkamp GW, Masucci MG. 2001. c-myc overexpression activates alternative pathways for intracellular proteolysis in lymphoma cells. Nat Cell Biol 3:283-288.
12. Geier E, Pfeifer G, Wilm M, Lucchiari-Hartz M, Baumeister W, Eichmann K, Niedermann G. 1999. A giant protease with potential to substitute for some functions of the proteasome. Science 283:978-981.
13. Glas R, Bogyo M, McMaster JS, Gaczynska M, Ploegh HL. 1998. A proteolytic system that compensates for loss of proteasome function. Nature 392:618-622.
14. Glickman MH, Ciechanover A. 2002. The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol Rev 82:373-428.
15. Glickman MH, Rubin DM, Coux O, Wefes I, Pfeifer G, Cjeka Z, Baumeister W, Fried VA, Finley D. 1998. A subcomplex of the proteasome regulatory particle required for ubiquitin-conjugate degradation and related to the COP9-signalosome and elF3. Cell 94:615-623.
16. Groll M, Huber R. 2004. Inhibitors of the eukarotic 20S proteasome core particle: A structural approach. Biochim Biophys Acta 1695:33-44.
17. Hong X, Lei L, Glas R. 2003. Tumors acquire inhibitor of apoptosis protein (IAP)-mediated apoptosis resistance through altered specificity of cytosolic proteolysis. J Exp Med 197:1731-1743.
18. Ichihara A, Tanaka K. 1995. Roles of proteasomes in cell growth. Mol Biol Rep 21:49-52.
19. Ito H, Kamei K, Iwamoto I, Inaguma Y, Garcia-Mata R, Sztul E, Kata K 2002. Inhibition of proteasomes induce accumulation, phosphorylation, and recruitment of Hsp27 and alphaB-crystallin to aggresomes. J Biochem 131:593-603.
20. Kisselev AF, Akopian TN, Castillo V, Goldberg AL. 1999. Proteasome active sites allosterically regulate each other, suggesting a bite-chew mechanism for protein breakdown. Mol Cell 4:395-402.
21. Kisselev AF, Callard A, Goldberg AL. 2006. Importance of the different proteolytic sites of the proteasome and efficacy of inhibitors varies with the protein substrate. J Biol Chem 281:8582-8590.
22. Kloetzel PM. 2001. Antigen processing by the proteasome. Nat Rev Mol Cell Biol 2:179-187.
23. Kraus M, Rückrich T, Reich M, Gogel J, Beck A, Kammer W, Berkers CR, Burg D, Overkleeft H, Ovaa H, Driessen C. 2007. Activity patterns of proteasome subunits reflect bortezomib sensitivity of hematologic malignancies and are viable in primary human leukemia cells. Leukemia 21:84-92.
24. Krüger E, Kloetzel PM, Enenkel C. 2001. 20S proteasome biogenesis. Biochimie 83:289-293.
25. Krüger E, Kuckelkorn U, Sijts A, Kloetzel PM. 2003. The components of the proteasome system and their role in MHC class I antigen processing. Rev Physiol Biochem Pharmacol 148:81-104.
26. Lam YA, Lawson TG, Velayutham M, Zweier JL, Pickart CM. 2002. A proteasomal ATPase subunit recognizes the polyubiquitin degradation signal. Nature 416:763-767.
27. Lee CS, Tee LY, Warmke T, Vinjamoori A, Cai A, Fagan AM, Snider BJ. 2004. A proteasomal stress response: Pretreatment with proteasome inhibitors increases proteasome activity and reduces neuronal vulnerability to oxidative injury. J Neurochem 91:996-1006.
28. Lopes UG, Erhardt P, Yao R, Cooper GM. 1997. p53-dependent induction of apoptosis by proteasome inhibitors. J Biol Chem 272:12893-12896.
29. Ludescher C, Thaler J, Drach D, Drach J, Spitaler M, Gattringer C, Huber H, Hofmann J. 1992. Detection of activity of P-glycoprotein in human tumour samples using rhodamine 123. Br J Haematol 82:161-168.
30. Maki CG, Huibregtse JM, Howley PM. 1995. In vivo ubiquitination and proteasome-mediated degradation of p53. Cancer Res 56:2649-2654.
31. McCormack T, Baumeister W, Grenier L, Moomaw C, Plamondon L, Pramanik B, Slaughter C, Soucy F, Stein R, Zühl F, Dick L. 1997. Active site-directed inhibitors of Rhodococcus 20S proteasome. J Biol Chem 272:26103-26109.
32. Meiners S, Heyken D, Weller A, Ludwig A, Stangl K, Kloetzel PM, Krüger E. 2003. Inhibition of proteasome activity induces concerted expression of proteasome genes and de novo formation of mammalian proteasomes. J Biol Chem 278:21517-21525.
33. Naujokat C, Hoffmann S. 2002. Role and function of the 26S proteasome in proliferation and apoptosis. Lab Invest 82:965-980.
34. Naujokat C, Sezer O, Zinke H, Leclere A, Hauptmann S, Possinger K. 2000. Proteasome inhibitors induce caspase-dependent apoptosis and accumulation of p21WAF/Cip1 in human immature leukemic cells. Eur J Haematol 65:221-236.
35. Naujokat C, Daniel V, Bauer TM, Sadeghi M, Opelz G. 2003. Cell cycle- and activation-dependent regulation of cyclosporin A-induced T cell apoptosis. Biochem Biophys Res Commun 310:347-354.
36. Nicoletti I, Migliorati G, Pagliacci MC, Grignani F, Riccardi C. 1991. A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytomatry. J Immunol Methods 139:271-279.
37. Papandreou CN, Daliani DD, Nix D, Yang H, Madden T, WangX, Pien CS, Millikan RE, Tu SM, Pagliaro L, Kim J, Adams J, Elliott P, Esseltine D, Petrusich A, Dieringer P, Perez C, Logothetis CJ. 2004. Phase I trial of the proteasome inhibitor bortezomib in patients with advanced solid tumors with observations in androgen-independent prostate cancer. J Clin Oncol 22:2108-2121.
38. Parcellier A, Schmitt E, Gurbuxani S, Seigneurin-Berny D, Pance A, Chantome A, Plenchette S, Khochbin S, Solary E, Garrido C. 2003. Hsp27 is a ubiquitin-binding protein involved in I-kappaB alpha proteasomal degradation. Mol Cell Biol 23:5790-5802.
39. Pei XY, Dai Y, Grant S. 2003. The proteasome inhibitor bortezomib promotes mitochondrial injury and apoptosis induced by the small molecule Bcl-2 inhibitor HA 14-1in multiple myeloma cells. Leukemia 17:2036-2045.
40. Princiotta MF, Schubert U, Chen W, Bennink JR, Myunk J, Crews CM, Yewdell JW. 2001. Cells adapted to the proteasome inhibitor 4-hydroxy-5-iodo-3- nitrophenylacetyl-Leu-Leu-leucinal-vinyl sulfone require enzymatically active proteasomes for continued survival. Proc Natl Acad Sci USA 98:513-518.
41. Rajkumar SV, Richardson PG, Hideshima T, Anderson KC. 2005. Proteasome inhibition as a novel therapeutic target in human cancer. J Clin Oncol 23:630-639.
42. Richardson PG, Mitsiades C, Hideshima T, Anderson KC. 2006. Bortezomib: Proteasome inhibition as an effective anticancer therapy. Annu Rev Med 57:33-47.
43. Schwarz K, Eggers M, Soza A, Koszinowski UH, Kloetzel PM, Groettrup M. 2000. The proteasome regulator PA28 alpha/beta can enhance antigen presentation without affecting 20S proteasome subunit composition. Eur J Immunol 30:3672-3679.
44. Shibatani T, Carlson EJ, Larabee F, McCormack AL, Früh K, Skach WR. 2006. Global organization and function of mammalian cytosolic proteasome pools: Implications for PA28 and 19S regulatory complexes. Mol Biol Cell 17: 4962-4971.
45. Shimbara N, Orino E, Sone S, Ogura T, Takashina M, Shono M, Tamura T, Yasuda H, Tanaka K, Ichihara A. 1992. Regulation of gene expression of proteasomes (multi-protease complexes) during growth and differentiation of human hematopoietic cells. J Biol Chem 267:18100-181109.
46. Tanahashi N, Murakami Y, Minami Y, Shimbara N, Hendil KB, Tanaka K. 2000. Hybrid proteasomes. Induction by interferon-gamma and contribution to ATP-dependent proteolysis. J Biol Chem 275:14336-14345.
47. Voges D, Zwickl P, Baumeister W. 1999. The 26S proteasome: A molecular machine designed for controlled proteolysis. Annu Rev Biochem 68:1015-1068.
48. Wang EW, Kessler BM, Borodovsky A, Cravatt BF, Bogyo M, Ploegh HL, Glas R. 2000. Integration of the ubiquitin-proteasome pathway with a cytosolic oligopeptidase activity. Proc Natl Acad Sci USA 97:9990-9995.
49. Wendler P, Lehmann A, Janek K, Baumgart S, Enenkel C. 2004. The bipartite nuclear localization sequence of Rpn2 is required for nuclear import of proteasomal base complexes via karypherin alpha/beta and proteasome functions. J Biol Chem 279:37751-37762.
50. Witt E, Zantopf D, Schmidt M, Kraft R, Kloetzel PM, Krüger E. 2000. Characterisation of the newly identified human Ump1 homologue POMP and analysis of LMP7 (beta5i) incorporation into 20S proteasomes. J Mol Biol 301:1-9.
51. Wojcik C, DeMartino GN. 2002. Analysis of Drosophila 26S proteasome using RNA interference. J Biol Chem 277:6188-6197.
52. Yang QH, Du C. 2004. Smac/DIABOLO selectively reduces the levels of c-IAP1 and C-IAP2 but not that of XIAP and livin in HeLa cells. J Biol Chem 279:16963-16970.
53. Yin D, Zhou H, Liu G, Ong JM, Black KL, Koeffler HP. 2005. Proteasome inhibitor PS-341 causes cell growth arrest and apoptosis in human glioblastoma multiforme (GBM). Oncogene 24:344-354.