Intracellular Dynamics of the Ubiquitin-Proteasome-System

F1000Research

Volumn 4, Issue , 2015, Pages

  Chowdhury, Maisha ^a   Enenkel, Cordula ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; GREEN FLUORESCENT PROTEIN; KARYOPHERIN ALPHA; KARYOPHERIN BETA; NUCLEOPORIN; PROTEASOME; RAN PROTEIN; UBIQUITIN; UBIQUITIN ACTIVATION ENZYME E1; UBIQUITIN CONJUGATING ENZYME E2; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

BLEACHING; CELL CYCLE PROGRESSION; CELL NUCLEUS MEMBRANE; CELL PH; CELL PROLIFERATION; CYTOPLASM; DIMERIZATION; ENDOPLASMIC RETICULUM MEMBRANE; EUKARYOTIC CELL; GENE EXPRESSION; HUMAN; JUXTA NUCLEAR QUALITY CONTROL COMPARTMENT; MAMMAL CELL; MOLECULAR DYNAMICS; NONHUMAN; NUCLEAR EXPORT SIGNAL; NUCLEAR IMPORT; NUCLEAR LOCALIZATION SIGNAL; NUCLEAR PORE COMPLEX; OOCYTE; PROTEIN AGGREGATION; PROTEIN ASSEMBLY; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN HOMEOSTASIS; PROTEIN STRUCTURE; QUALITY CONTROL; REVIEW; XENOPUS LAEVIS;

EID: 84940985395     PISSN: 20461402     EISSN: 1759796X     Source Type: Journal    
DOI: 10.12688/f1000research.6835.1     Document Type: Review

References (81)

1. Aitchison JD Rout MP: The yeast nuclear pore complex and transport through it. Genetics. 2012;190(3):855-883. 22419078 10.1534/genetics.111.127803 3296253
2. Amsterdam A Pitzer F Baumeister W: Changes in intracellular localization of proteasomes in immortalized ovarian granulosa cells during mitosis associated with a role in cell cycle control. Proc Natl Acad Sci U S A. 1993;90(1):99-103. 8380501 10.1073/pnas.90.1.99 45607
3. Bajorek M Finley D Glickman MH: Proteasome disassembly and downregulation is correlated with viability during stationary phase. Curr Biol. 2003;13(13):1140-1144. 12842014 10.1016/S0960-9822(03)00417-2
4. Barrault MB Richet N Godard C: Dual functions of the Hsm3 protein in chaperoning and scaffolding regulatory particle subunits during the proteasome assembly. Proc Natl Acad Sci U S A. 2012;109(17):E1001-1010. 22460800 10.1073/pnas.1116538109 3340050
5. Beckwith R Estrin E Worden EJ: Reconstitution of the 26S proteasome reveals functional asymmetries in its AAA+ unfoldase. Nat Struct Mol Biol. 2013;20(10):1164-1172. 24013205 10.1038/nsmb.2659 3869383
6. Chen L Madura K: Degradation of specific nuclear proteins occurs in the cytoplasm in Saccharomyces cerevisiae. Genetics. 2014a;197(1):193-197. 24621829 10.1534/genetics.114.163824 4012479
7. Chen L Madura K: Yeast importin-α (Srp1) performs distinct roles in the import of nuclear proteins and in targeting proteasomes to the nucleus. J Biol Chem. 2014b;289(46):32339-32352. 25274630 10.1074/jbc.M114.582023 4231706
8. Chen L Romero L Chuang SM: Sts1 plays a key role in targeting proteasomes to the nucleus. J Biol Chem. 2011;286(4):3104-3118. 21075847 10.1074/jbc.M110.135863 3024803
9. Ciechanover A Brundin P: The ubiquitin proteasome system in neurodegenerative diseases: sometimes the chicken, sometimes the egg. Neuron. 2003;40(2):427-446. 14556719 10.1016/S0896-6273(03)00606-8
10. Coux O Tanaka K Goldberg AL: Structure and functions of the 20S and 26S proteasomes. Annu Rev Biochem. 1996;65:801-847. 8811196 10.1146/annurev.bi.65.070196.004101
11. Crosas B Hanna J Kirkpatrick DS: Ubiquitin chains are remodeled at the proteasome by opposing ubiquitin ligase and deubiquitinating activities. Cell. 2006;127(7):1401-1413. 17190603 10.1016/j.cell.2006.09.051
12. Doherty KM Pride LD Lukose J: Loss of a 20S proteasome activator in Saccharomyces cerevisiae downregulates genes important for genomic integrity, increases DNA damage, and selectively sensitizes cells to agents with diverse mechanisms of action. G3 (Bethesda). 2012;2(8):943-959. 22908043 10.1534/g3.112.003376 3411250
13. Enenkel C: Proteasome dynamics. Biochim Biophys Acta. 2014;1843(1):39-46. 23545412 10.1016/j.bbamcr.2013.03.023
14. Enenkel C Lehmann A Kloetzel PM: Subcellular distribution of proteasomes implicates a major location of protein degradation in the nuclear envelope-ER network in yeast. EMBO J. 1998;17(21):6144-6154. 9799224 10.1093/emboj/17.21.6144 1170941
15. Enenkel C Lehmann A Kloetzel PM: GFP-labelling of 26S proteasomes in living yeast: insight into proteasomal functions at the nuclear envelope/rough ER. Mol Biol Rep. 1999;26(1-2):131-135. 10363659 10.1023/A:1006973803960
16. Eytan E Ganoth D Armon T: ATP-dependent incorporation of 20S protease into the 26S complex that degrades proteins conjugated to ubiquitin. Proc Natl Acad Sci U S A. 1989;86(20):7751-7755. 2554287 10.1073/pnas.86.20.7751 298148
17. Fehlker M Wendler P Lehmann A: Blm3 is part of nascent proteasomes and is involved in a late stage of nuclear proteasome assembly. EMBO Rep. 2003;4(10):959-963. 12973301 10.1038/sj.embor.embor938 1326396
18. Finley D: Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annu Rev Biochem. 2009;78:477-513. 19489727 10.1146/annurev.biochem.78.081507.101607 3431160
19. Finley D Tanaka K Mann C: Unified nomenclature for subunits of the Saccharomyces cerevisiae proteasome regulatory particle. Trends Biochem Sci. 1998;23(7):244-245. 9697412 10.1016/S0968-0004(98)01222-5
20. Finley D Ulrich HD Sommer T: The ubiquitin-proteasome system of Saccharomyces cerevisiae. Genetics. 2012;192(2):319-360. 23028185 10.1534/genetics.112.140467 3454868
21. Fishbain S Inobe T Israeli E: Sequence composition of disordered regions fine-tunes protein half-life. Nat Struct Mol Biol. 2015;22(3):214-221. 25643324 10.1038/nsmb.2958 4351145
22. Funakoshi M Tomko RJ Jr Kobayashi H: Multiple assembly chaperones govern biogenesis of the proteasome regulatory particle base. Cell. 2009;137(5):887-899. 19446322 10.1016/j.cell.2009.04.061 2718848
23. Glickman MH Rubin DM Fried VA: The regulatory particle of the Saccharomyces cerevisiae proteasome. Mol Cell Biol. 1998;18(6):3149-3162. 9584156 108897
24. Goldberg AL: Protein degradation and protection against misfolded or damaged proteins. Nature. 2003;426(6968):895-899. 14685250 10.1038/nature02263
25. Gorlich D Kutay U: Transport between the cell nucleus and the cytoplasm. Annu Rev Cell Dev Biol. 1999;15:607-660. 10611974 10.1146/annurev.cellbio.15.1.607
26. Groll M Bajorek M Köhler A: A gated channel into the proteasome core particle. Nat Struct Biol. 2000;7(11):1062-1067. 11062564 10.1038/80992
27. Groll M Ditzel L Löwe J: Structure of 20S proteasome from yeast at 2.4 A resolution. Nature. 1997;386(6624):463-471. 9087403 10.1038/386463a0
28. Groothuis TA Reits EA: Monitoring the distribution and dynamics of proteasomes in living cells. Methods Enzymol. 2005;399:549-563. 16338381 10.1016/S0076-6879(05)99037-X
29. Hanna J Hathaway NA Tone Y: Deubiquitinating enzyme Ubp6 functions noncatalytically to delay proteasomal degradation. Cell. 2006;127(1):99-111. 17018280 10.1016/j.cell.2006.07.038
30. Hanna J Waterman D Boselli M: Spg5 protein regulates the proteasome in quiescence. J Biol Chem. 2012;287(41):34400-34409. 22904326 10.1074/jbc.M112.390294 3464545
31. Harper JW Schulman BA: Structural complexity in ubiquitin recognition. Cell. 2006;124(6):1133-1136. 16564007 10.1016/j.cell.2006.03.009
32. Hershko A Ciechanover A: The ubiquitin system. Annu Rev Biochem. 1998;67:425-479. 9759494 10.1146/annurev.biochem.67.1.425
33. Huber EM Groll M: The 19S cap puzzle: a new jigsaw piece. Structure. 2012;20(3):387-388. 22404996 10.1016/j.str.2012.02.006
34. Hügle B Kleinschmidt JA Franke WW: The 22 S cylinder particles of Xenopus laevis. II. Immunological characterization and localization of their proteins in tissues and cultured cells. Eur J Cell Biol. 1983;32(1):157-163. 6667692
35. Huh WK Falvo JV Gerke LC: Global analysis of protein localization in budding yeast. Nature. 2003;425(6959):686-691. 14562095 10.1038/nature02026
36. Isono E Nishihara K Saeki Y: The assembly pathway of the 19S regulatory particle of the yeast 26S proteasome. Mol Biol Cell. 2007;18(2):569-580. 17135287 10.1091/mbc.E06-07-0635 1783769
37. Kaganovich D Kopito R Frydman J: Misfolded proteins partition between two distinct quality control compartments. Nature. 2008;454(7208):1088-1095. 18756251 10.1038/nature07195 2746971
38. Kajava AV: What curves alpha-solenoids? Evidence for an alpha-helical toroid structure of Rpn1 and Rpn2 proteins of the 26 S proteasome. J Biol Chem. 2002;277(51):49791-49798. 12270919 10.1074/jbc.M204982200
39. Kirschner M: Intracellular proteolysis. Trends Cell Biol. 1999;9(12):M42-45. 10611680 10.1016/S0962-8924(99)01666-9
40. Kleinschmidt JA Hügle B Grund C: The 22 S cylinder particles of Xenopus laevis. I. Biochemical and electron microscopic characterization. Eur J Cell Biol. 1983;32(1):143-156. 6667691
41. Knecht E Rivett J: Intracellular Localization of Proteasomes. In Proteasomes: The World of Regulatory Proteolysis.W Hilt, and DH Wolf, eds. (Georgetown, Texas, USA: Landes Bioscience, Eurekah.com).2000;176-185. Reference Source
42. Kock M Nunes MM Hemann M: Proteasome assembly from 15S precursors involves major conformational changes and recycling of the Pba1-Pba2 chaperone. Nat Commun. 2015;6:6123. 25609009 10.1038/ncomms7123
43. Kusmierczyk AR Kunjappu MJ Funakoshi M: A multimeric assembly factor controls the formation of alternative 20S proteasomes. Nat Struct Mol Biol. 2008;15(3):237-244. 18278055 10.1038/nsmb.1389
44. Lam YA Xu W DeMartino GN: Editing of ubiquitin conjugates by an isopeptidase in the 26S proteasome. Nature. 1997;385(6618):737-740. 9034192 10.1038/385737a0
45. Laporte D Salin B Daignan-Fornier B: Reversible cytoplasmic localization of the proteasome in quiescent yeast cells. J Cell Biol. 2008;181(5):737-745. 18504300 10.1083/jcb.200711154 2396804
46. Le Tallec B Barrault MB Guérois R: Hsm3/S5b participates in the assembly pathway of the 19S regulatory particle of the proteasome. Mol Cell. 2009;33(3):389-399. 19217412 10.1016/j.molcel.2009.01.010
47. Lehmann A Janek K Braun B: 20 S proteasomes are imported as precursor complexes into the nucleus of yeast. J Mol Biol. 2002;317(3):401-413. 11922673 10.1006/jmbi.2002.5443
48. Lehmann A Jechow K Enenkel C: Blm10 binds to pre-activated proteasome core particles with open gate conformation. EMBO Rep. 2008;9(12):1237-1243. 18927584 10.1038/embor.2008.190 2603454
49. Li X Kusmierczyk AR Wong P: beta-Subunit appendages promote 20S proteasome assembly by overcoming an Ump1-dependent checkpoint. EMBO J. 2007;26(9):2339-2349. 17431397 10.1038/sj.emboj.7601681 1864979
50. McDonald HB Byers B: A proteasome cap subunit required for spindle pole body duplication in yeast. J Cell Biol. 1997;137(3):539-553. 9151663 10.1083/jcb.137.3.539 2139890
51. Moore MS Blobel G: The GTP-binding protein Ran/TC4 is required for protein import into the nucleus. Nature. 1993;365(6447):661-663. 8413630 10.1038/365661a0
52. Pack CG Yukii H Toh-e A: Quantitative live-cell imaging reveals spatio-temporal dynamics and cytoplasmic assembly of the 26S proteasome. Nat Commun. 2014;5:3396. 24598877 10.1038/ncomms4396
53. Panté N Kann M: Nuclear pore complex is able to transport macromolecules with diameters of about 39 nm. Mol Biol Cell. 2002;13(2):425-434. 11854401 10.1091/mbc.01-06-0308 65638
54. Park S Roelofs J Kim W: Hexameric assembly of the proteasomal ATPases is templated through their C termini. Nature. 2009;459(7248):866-870. 19412160 10.1038/nature08065 2722381
55. Park SH Kukushkin Y Gupta R: PolyQ proteins interfere with nuclear degradation of cytosolic proteins by sequestering the Sis1p chaperone. Cell. 2013;154(1):134-145. 23791384 10.1016/j.cell.2013.06.003
56. Peters LZ Hazan R Breker M: Formation and dissociation of proteasome storage granules are regulated by cytosolic pH. J Cell Biol. 2013;201(5):663-671. 23690178 10.1083/jcb.201211146 3664706
57. Prasad R Kawaguchi S Ng DT: A nucleus-based quality control mechanism for cytosolic proteins. Mol Biol Cell. 2010;21(13):2117-2127. 20462951 10.1091/mbc.E10-02-0111 2893977
58. Ramos PC Dohmen RJ: PACemakers of proteasome core particle assembly. Structure. 2008;16(9):1296-1304. 18786393 10.1016/j.str.2008.07.001
59. Ramos PC Hockendorff J Johnson ES: Ump1p is required for proper maturation of the 20S proteasome and becomes its substrate upon completion of the assembly. Cell. 1998;92(4):489-499. 9491890 10.1016/S0092-8674(00)80942-3
60. Rechsteiner M Hill CP: Mobilizing the proteolytic machine: cell biological roles of proteasome activators and inhibitors. Trends Cell Biol. 2005;15(1):27-33. 15653075 10.1016/j.tcb.2004.11.003
61. Reits EA Benham AM Plougastel B: Dynamics of proteasome distribution in living cells. EMBO J. 1997;16(20):6087-6094. 9321388 10.1093/emboj/16.20.6087 1326292
62. Rendueles PS Wolf DH: Proteinase function in yeast: biochemical and genetic approaches to a central mechanism of post-translational control in the eukaryote cell. FEMS Microbiol Rev. 1988;4(1):17-45. 3078768 10.1111/j.1574-6968.1988.tb02706.x-i1
63. Rexach M Blobel G: Protein import into nuclei: association and dissociation reactions involving transport substrate, transport factors, and nucleoporins. Cell. 1995;83(5):683-692. 8521485 10.1016/0092-8674(95)90181-7
64. Roelofs J Park S Haas W: Chaperone-mediated pathway of proteasome regulatory particle assembly. Nature. 2009;459(7248):861-865. 19412159 10.1038/nature08063 2727592
65. Russell SJ Steger KA Johnston SA: Subcellular localization, stoichiometry, and protein levels of 26 S proteasome subunits in yeast. J Biol Chem. 1999;274(31):21943-21952. 10419517 10.1074/jbc.274.31.21943
66. Sahtoe DD Sixma TK: Layers of DUB regulation. Trends Biochem Sci. 2015;40(8):456-467. 26073511 10.1016/j.tibs.2015.05.002
67. Salomons FA Acs K Dantuma NP: Illuminating the ubiquitin/proteasome system. Exp Cell Res. 2010;316(8):1289-1295. 20149791 10.1016/j.yexcr.2010.02.003
68. Saunier R Esposito M Dassa EP: Integrity of the Saccharomyces cerevisiae Rpn11 protein is critical for formation of proteasome storage granules (PSG) and survival in stationary phase. PLoS One. 2013;8(8):e70357. 23936414 10.1371/journal.pone.0070357 3735599
69. Sugaya K Ishihara Y Inoue S: Nuclear localization of ubiquitin-activating enzyme Uba1 is characterized in its mammalian temperature-sensitive mutant. Genes Cells. 2015. 26059705 10.1111/gtc.12257
70. Sugaya K Ishihara Y Inoue S: Characterization of ubiquitin-activating enzyme Uba1 in the nucleus by its mammalian temperature-sensitive mutant. PLoS One. 2014;9(5):e96666. 24805847 10.1371/journal.pone.0096666 4013028
71. Tanaka K Yoshimura T Tamura T: Possible mechanism of nuclear translocation of proteasomes. FEBS Lett. 1990;271(1-2):41-46. 2226812 10.1016/0014-5793(90)80367-R
72. Tsien RY: The green fluorescent protein. Annu Rev Biochem. 1998;67:509-544. 9759496 10.1146/annurev.biochem.67.1.509
73. Vabulas RM Hartl FU: Protein synthesis upon acute nutrient restriction relies on proteasome function. Science. 2005;310(5756):1960-1963. 16373576 10.1126/science.1121925
74. van Deventer S Menendez-Benito V van Leeuwen F: N-terminal acetylation and replicative age affect proteasome localization and cell fitness during aging. J Cell Sci. 2015;128(1):109-117. 25413350 10.1242/jcs.157354 4282048
75. Verma R Aravind L Oania R: Role of Rpn11 metalloprotease in deubiquitination and degradation by the 26S proteasome. Science. 2002;298(5593):611-615. 12183636 10.1126/science.1075898
76. von Mikecz A: The nuclear ubiquitin-proteasome system. J Cell Sci. 2006;119(Pt 10):1977-1984. 16687735 10.1242/jcs.03008
77. Weberruss MH Savulescu AF Jando J: Blm10 facilitates nuclear import of proteasome core particles. EMBO J. 2013;32(20):2697-2707. 23982732 10.1038/emboj.2013.192 3801435
78. Wendler P Lehmann A Janek K: The bipartite nuclear localization sequence of Rpn2 is required for nuclear import of proteasomal base complexes via karyopherin alphabeta and proteasome functions. J Biol Chem. 2004;279(36):37751-37762. 15210724 10.1074/jbc.M403551200
79. Wente SR Rout MP: The nuclear pore complex and nuclear transport. Cold Spring Harb Perspect Biol. 2010;2(10):a000562. 20630994 10.1101/cshperspect.a000562 2944363
80. Wojcik C DeMartino GN: Intracellular localization of proteasomes. Int J Biochem Cell Biol. 2003;35(5):579-589. 12672451 10.1016/S1357-2725(02)00380-1
81. Wozniak RW Rout MP Aitchison JD: Karyopherins and kissing cousins. Trends Cell Biol. 1998;8(5):184-188. 9695836 10.1016/S0962-8924(98)01248-3