Blm10 facilitates nuclear import of proteasome core particles

EMBO Journal

Volumn 32, Issue 20, 2013, Pages 2697-2707

  Weberruss, Marion H ^a,b   Savulescu, Anca F ^c   Jando, Julia ^d   Bissinger, Thomas ^b   Harel, Amnon ^e   Glickman, Michael H ^c   Enenkel, Cordula ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF STUTTGART   (Germany)

^c TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^d UNIVERSITY OF ZURICH   (Switzerland)

^e BAR ILAN UNIVERSITY   (Israel)

Author keywords

Blm10; nuclear import; proteasome activator; protein aggregation; quiescence

Indexed keywords

KARYOPHERIN BETA; NUCLEAR PROTEIN; NUCLEOPORIN; PEPTIDES AND PROTEINS; PROTEASOME; PROTEIN; PROTEIN BLM 10; UNCLASSIFIED DRUG;

ARTICLE; CELL COMPONENT; CELL DIVISION; CELL GROWTH; CELL NUCLEUS; CELL PROLIFERATION; CORE PARTICLE; NONHUMAN; NUCLEAR IMPORT; NUCLEAR PORE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; YEAST;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CELL NUCLEUS; CELL PROLIFERATION; CYTOPLASMIC GRANULES; GREEN FLUORESCENT PROTEINS; MODELS, BIOLOGICAL; NUCLEAR PORE COMPLEX PROTEINS; ORGANISMS, GENETICALLY MODIFIED; PROTEASOME ENDOPEPTIDASE COMPLEX; RECEPTORS, CYTOPLASMIC AND NUCLEAR; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; XENOPUS;

EID: 84885858648     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2013.192     Document Type: Article

References (60)

1. Aebi M, Clark MW, Vijayraghavan U, Abelson J (1990) A yeast mutant, PRP20, altered in mRNA metabolism and maintenance of the nuclear structure, is defective in a gene homologous to the human gene RCC1 which is involved in the control of chromosome condensation. Mol Gen Genet 224: 72-80
2. Bajorek M, Finley D, Glickman MH (2003) Proteasome disassembly and downregulation is correlated with viability during stationary phase. Curr Biol 13: 1140-1144
3. Blickwedehl J, McEvoy S, Wong I, Kousis P, Clements J, Elliott R, Cresswell P, Liang P, Bangia N (2007) Proteasomes and proteasome activator 200 kDa (PA200) accumulate on chromatin in response to ionizing radiation. Radiat Res 167: 663-674
4. Chen L, Romero L, Chuang SM, Tournier V, Joshi KK, Lee JA, Kovvali G, Madura K (2011) Sts1 plays a key role in targeting proteasomes to the nucleus. J Biol Chem 286: 3104-3118
5. Cook A, Bono F, Jinek M, Conti E (2007) Structural biology of nucleocytoplasmic transport. Ann Review Biochem 76: 647-671
6. Costanzo M, Baryshnikova A, Bellay J, Kim Y, Spear ED, Sevier CS, Ding H, Koh JL, Toufighi K, Mostafavi S, Prinz St J, Onge RP, VanderSluis B, Makhnevych T, Vizeacoumar FJ, Alizadeh S, Bahr S, Brost RL, Chen Y, Cokol M et al. (2010) The genetic landscape of a cell. Science 327: 425-431
7. Dange T, Smith D, Noy T, Rommel PC, Jurzitza L, Cordero RJ, Legendre A, Finley D, Goldberg AL, Schmidt M (2011) Blm10 protein promotes proteasomal substrate turnover by an active gating mechanism. J Biol Chem 286: 42830-42839
8. Doherty KM, Pride LD, Lukose J, Snydsman BE, Charles R, Pramanik A, Muller EG, Botstein D, Moore CW (2012) 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) 2: 943-959
9. Enenkel C (2013) Proteasome dynamics. Biochim Biophys Acta S0167-4889: 00124-00129
10. Enenkel C, Blobel G, Rexach M (1995) Identification of a yeast karyopherin heterodimer that targets import substrate to mammalian nuclear pore complexes. J Biol Chem 270: 16499-16502
11. Enenkel C, Lehmann A, Kloetzel PM (1998) Subcellular distribution of proteasomes implicates a major location of protein degradation in the nuclear envelope-ER network in yeast. EMBO J 17: 6144-6154
12. Enenkel C, Schulke N, Blobel G (1996) Expression in yeast of binding regions of karyopherins alpha and beta inhibits nuclear import and cell growth. Proc Natl Acad Sci USA 93: 12986-12991
13. Febres DE, Pramanik A, Caton M, Doherty K, McKoy J, Garcia E, Alejo W, Moore CW (2001) The novel BLM3 gene encodes a protein that protects against lethal effects of oxidative damage. Cell Mol Biol 47: 1149-1162
14. Fehlker M, Wendler P, Lehmann A, Enenkel C (2003) Blm3 is part of nascent proteasomes and is involved in a late stage of nuclear proteasome assembly. EMBO Rep 4: 959-963
15. Fried H, Kutay U (2003) Nucleocytoplasmic transport: Taking an inventory. Cell Mol Life Sci 60: 1659-1688
16. Glickman MH, Raveh D (2005) Proteasome plasticity. FEBS Lett 579: 3214-3223
17. Groll M, Bajorek M, Kohler A, Moroder L, Rubin DM, Huber R, Glickman MH, Finley D (2000) A gated channel into the proteasome core particle. Nat Struct Mol Biol 7: 1062-1067
18. Groll M, Ditzel L, Lowe J, Stock D, Bochtler M, Bartunik HD, Huber R (1997) Structure of 20S proteasome from yeast at 2.4 A resolution. Nature 386: 463-471
19. Hahn S, Schlenstedt G (2011) Importin beta-type nuclear transport receptors have distinct binding affinities for Ran-GTP. Biochem Biophysic Res Commun 406: 383-388
20. Huber EM, Basler M, Schwab R, Heinemeyer W, Kirk CJ, Groettrup M, Groll M (2012) Immuno- and constitutive proteasome crystal structures reveal differences in substrate and inhibitor specificity. Cell 148: 727-738
21. Huber EM, Groll M (2012) The 19S cap puzzle: A new jigsaw piece. Structure 20: 387-388
22. Isono E, Nishihara K, Saeki Y, Yashiroda H, Kamata N, Ge L, Ueda T, Kikuchi Y, Tanaka K, Nakano A, Toh-e A (2007) The assembly pathway of the 19S regulatory particle of the yeast 26S proteasome. Mol Biol Cell 18: 569-580
23. Iwanczyk J, Sadre-Bazzaz K, Ferrell K, Kondrashkina E, Formosa T, Hill CP, Ortega J (2006) Structure of the Blm10-20 S proteasome complex by cryo-electron microscopy. Insights into the mechanism of activation of mature yeast proteasomes. J Mol Biol 363: 648-659
24. Kaganovich D, Kopito R, Frydman J (2008) Misfolded proteins partition between two distinct quality control compartments. Nature 454: 1088-1095
25. Kajava AV, Gorbea C, Ortega J, Rechsteiner M, Steven AC (2004) New HEAT-like repeat motifs in proteins regulating proteasome structure and function. J Struct Biol 146: 425-430
26. Khor B, Bredemeyer AL, Huang CY, Turnbull IR, Evans R, Maggi Jr. LB, White JM, Walker LM, Carnes K, Hess RA, Sleckman BP (2006) Proteasome activator PA200 is required for normal spermatogenesis. Mol Cell Biol 26: 2999-3007
27. Kleijnen MF, Roelofs J, Park S, Hathaway NA, Glickman M, King RW, Finley D (2007) Stability of the proteasome can be regulated allosterically through engagement of its proteolytic active sites. Nat Struct Mol Biol 14: 1180-1188
28. Kloetzel PM (2004) Generation of major histocompatibility complex class I antigens: functional interplay between proteasomes and TPPII. Nat Immunol 5: 661-669
29. Kremer M, Henn A, Kolb C, Basler M, Moebius J, Guillaume B, Leist M, Van den Eynde BJ, Groettrup M (2010) Reduced immunoproteasome formation and accumulation of immunoproteasomal precursors in the brains of lymphocytic choriomeningitis virusinfected mice. J Immunol 185: 5549-5560
30. Kutay U, Izaurralde E, Bischoff FR, Mattaj IW, Gorlich D (1997) Dominant-negative mutants of importin-beta block multiple pathways of import and export through the nuclear pore complex. EMBO J 16: 1153-1163
31. Laporte D, Lebaudy A, Sahin A, Pinson B, Ceschin J, Daignan- Fornier B, Sagot I (2011) Metabolic status rather than cell cycle signals control quiescence entry and exit. J Cell Biol 192: 949-957
32. Laporte D, Salin B, Daignan-Fornier B, Sagot I (2008) Reversible cytoplasmic localization of the proteasome in quiescent yeast cells. J Cell Biol 181: 737-745
33. Lee SJ, Matsuura Y, Liu SM, Stewart M (2005) Structural basis for nuclear import complex dissociation by RanGTP. Nature 435: 693-696
34. Lehmann A, Janek K, Braun B, Kloetzel PM, Enenkel C (2002) 20 S proteasomes are imported as precursor complexes into the nucleus of yeast. J Mol Biol 317: 401-413
35. Lehmann A, Jechow K, Enenkel C (2008) Blm10 binds to preactivated proteasome core particles with open gate conformation. EMBO Rep 9: 1237-1243
36. Li X, Kusmierczyk AR, Wong P, Emili A, Hochstrasser M (2007) beta-Subunit appendages promote 20S proteasome assembly by overcoming an Ump1-dependent checkpoint. EMBO J 26: 2339-2349
37. Lopez AD, Tar K, Krugel U, Dange T, Ros IG, Schmidt M (2011) Proteasomal degradation of Sfp1 contributes to the repression of ribosome biogenesis during starvation and is mediated by the proteasome activator Blm10. Mol Biol Cell 22: 528-540
38. Macara IG (2001) Transport into and out of the nucleus. Microbiol Mol Biol Rev 65: 570-594
39. Marelli M, Aitchison JD, Wozniak RW(1998) Specific binding of the karyopherin Kap121p to a subunit of the nuclear pore complex containing Nup53p, Nup59p, and Nup170p. J Cell Biol 143: 1813-1830
40. Marques AJ, Glanemann C, Ramos PC, Dohmen RJ (2007) The C-terminal extension of the beta7 subunit and activator complexes stabilize nascent 20 S proteasomes and promote their maturation. J Biol Chem 282: 34869-34876
41. Mayr J, Wang HR, Nederlof P, Baumeister W (1999) The import pathway of human and Thermoplasma 20S proteasomes into HeLa cell nuclei is different from that of classical NLS-bearing proteins. Biol Chem 380: 1183-1192
42. Oeffinger M, Dlakic M, Tollervey D (2004) A pre-ribosome-associated HEAT-repeat protein is required for export of both ribosomal subunits. Genes Dev 18: 196-209
43. Peth A, Uchiki T, Goldberg AL (2010) ATP-dependent steps in the binding of ubiquitin conjugates to the 26S proteasome that commit to degradation. Mol Cell 40: 671-681
44. Ramos PC, Dohmen RJ (2008) PACemakers of proteasome core particle assembly. Structure 16: 1296-1304
45. Sadre-Bazzaz K, Whitby FG, Robinson H, Formosa T, Hill CP (2010) Structure of a Blm10 complex reveals common mechanisms for proteasome binding and gate opening. Mol Cell 37: 728-735
46. Savulescu AF, Glickman MH (2011) Proteasome Activator 200: The HEAT is on. Mol Cell Proteomics 10: 006890
47. Savulescu AF, Shorer H, Kleifeld O, Cohen I, Gruber R, Glickman MH, Harel A (2011) Nuclear import of an intact preassembled proteasome particle. Mol Biol Cell 22: 880-891
48. Schlenstedt G, Saavedra C, Loeb JD, Cole CN, Silver PA (1995) The GTP-bound form of the yeast Ran/TC4 homologue blocks nuclear protein import and appearance of poly(A) RNA in the cytoplasm. Proc Natl Acad Sci USA 92: 225-229
49. Schmidt M, Haas W, Crosas B, Santamaria PG, Gygi SP, Walz T, Finley D (2005) The HEAT repeat protein Blm10 regulates the yeast proteasome by capping the core particle. Nat Struct Mol Biol 12: 294-303
50. Stadtmueller BM, Hill CP (2011) Proteasome activators. Mol Cell 41: 8-19
51. Tanaka K (2009) The proteasome: Overview of structure and functions. Proc Jpn Acad Ser B Phys Biol Sci 85: 12-36
52. Tanaka K, Yoshimura T, Tamura T, Fujiwara T, Kumatori A, Ichihara A (1990) Possible mechanism of nuclear translocation of proteasomes. FEBS Lett 271: 41-46
53. Ustrell V, Hoffman L, Pratt G, Rechsteiner M (2002) PA200, a nuclear proteasome activator involved in DNA repair. EMBO J 21: 3516-3525
54. Vetter IR, Arndt A, Kutay U, Gorlich D, Wittinghofer A (1999) Structural view of the Ran-Importin beta interaction at 2.3 A resolution. Cell 97: 635-646
55. Wang HR, Kania M, Baumeister W, Nederlof PM (1997) Import of human and Thermoplasma 20S proteasomes into nuclei of HeLa cells requires functional NLS sequences. Eur J Cell Biol 73: 105-113
56. 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 karyopherin alphabeta and proteasome functions. J Biol Chem 279: 37751-37762
57. Wente SR, Rout MP (2010) The nuclear pore complex and nuclear transport. Cold Spring Harb Perspect Biol 2: A000562
58. Wong DH, Corbett AH, Kent HM, Stewart M, Silver PA (1997) Interaction between the small GTPase Ran/Gsp1p and Ntf2p is required for nuclear transport. Mol Cell Biol 17: 3755-3767
59. Yano R, Oakes M, Yamaghishi M, Dodd JA, Nomura M (1992) Cloning and characterization of SRP1, a suppressor of temperature- sensitive RNA polymerase I mutations, in Saccharomyces cerevisiae. Mol Cell Biol 12: 5640-5651
60. Blm10 imports proteasome core particles MH Weberruss et al Canada