Proteasomes crossing the nuclear border

Nucleus

Volumn 2, Issue 4, 2011, Pages 258-263

  Savulescu, Anca F ^a   Rotem, Asaf ^a,b   Harel, Amnon ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

26S proteasome; Nuclear bodies; Nuclear import; Nuclear pore complex; Ran GTPase

Indexed keywords

HOLOENZYME; NUCLEOPLASMIN; PROTEASOME;

ARTICLE; CELL COMPARTMENTALIZATION; CELL FREE SYSTEM; CELL NUCLEUS; HUMAN; MEDICAL LITERATURE; MITOSIS; PROTEIN ASSEMBLY; PROTEIN DEGRADATION; PROTEIN LOCALIZATION;

EID: 83455206904     PISSN: 19491034     EISSN: 19491042     Source Type: Journal    
DOI: 10.4161/nucl.2.4.16267     Document Type: Article

References (57)

1. Glickman MH, Ciechanover A. The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol Rev 2002; 82:373-428.
2. Finley D. Recognition and processing of ubiquitinprotein conjugates by the proteasome. Annu Rev Biochem 2009; 78:477-513.
3. Glickman MH. Getting in and out of the proteasome. Semin Cell Dev Biol 2000; 11:149-158.
4. Pickart CM, Cohen RE. Proteasomes and their kin: proteases in the machine age. Nat Rev Mol Cell Biol 2004; 5:177-187.
5. Laporte D, Salin B, Daignan-Fornier B, Sagot I. Reversible cytoplasmic localization of the proteasome in quiescent yeast cells. J Cell Biol 2008; 181:737-745.
6. Russell SJ, Steger KA, Johnston SA. Subcellular localization, stoichiometry and protein levels of 26 S proteasome subunits in yeast. J Biol Chem 1999; 274:21943-1952.
7. Wojcik C, DeMartino GN. Intracellular localization of proteasomes. Int J Biochem Cell Biol 2003; 35:579-589.
8. Isono E, Nishihara K, Saeki Y, Yashiroda H, Kamata N, Ge L, et al. The assembly pathway of the 19S regulatory particle of the yeast 26S proteasome. Mol Biol Cell 2007; 18:569-580.
9. Lehmann A, Janek K, Braun B, Kloetzel PM, Enenkel C. 20 S proteasomes are imported as precursor complexes into the nucleus of yeast. J Mol Biol 2002; 317:401-413.
10. Wendler P, Lehmann A, Janek K, Baumgart S, Enenkel C. 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; 279:37751-37762.
11. Adori C, Low P, Moszkovkin G, Bagdy G, Laszlo L, Kovacs GG. Subcellular distribution of components of the ubiquitin-proteasome system in non-diseased human and rat brain. J Histochem Cytochem 2006; 54:263-267.
12. Gordon C. The intracellular localization of the proteasome. Curr Top Microbiol Immunol 2002; 268:175-184.
13. Mattsson K, Pokrovskaja K, Kiss C, Klein G, Szekely L. Proteins associated with the promyelocytic leukemia gene product (PML)-containing nuclear body move to the nucleolus upon inhibition of proteasomedependent protein degradation. Proc Natl Acad Sci USA 2001; 98:1012-1017.
14. Palmer A, Rivett AJ, Thomson S, Hendil KB, Butcher GW, Fuertes G, et al. Subpopulations of proteasomes in rat liver nuclei, microsomes and cytosol. Biochem J 1996; 316:401-407.
15. Reits EA, Benham AM, Plougastel B, Neefjes J, Trowsdale J. Dynamics of proteasome distribution in living cells. EMBO J 1997; 16:6087-6094.
16. von Mikecz A, Chen M, Rockel T, Scharf A. The nuclear ubiquitin-proteasome system: visualization of proteasomes, protein aggregates and proteolysis in the cell nucleus. Methods Mol Biol 2008; 463:191-202.
17. Lafarga M, Berciano MT, Pena E, Mayo I, Castano JG, Bohmann D, et al. Clastosome: a subtype of nuclear body enriched in 19S and 20S proteasomes, ubiquitin and protein substrates of proteasome. Mol Biol Cell 2002; 13:2771-2782.
18. Carmo-Fonseca M, Berciano MT, Lafarga M. Orphan nuclear bodies. Cold Spring Harb Perspect Biol 2010; 2:000703.
19. Rockel TD, Stuhlmann D, von Mikecz A. Proteasomes degrade proteins in focal subdomains of the human cell nucleus. J Cell Sci 2005; 118:5231-5242.
20. Heun P. SUM Organization of the nucleus. Curr Opin Cell Biol 2007; 19:350-355.
21. Pines J, Lindon C. Proteolysis: anytime, any place, anywhere? Nat Cell Biol 2005; 7:731-735.
22. Tao LZ, Cheung AY, Nibau C, Wu HM. RAC GTPases in tobacco and Arabidopsis mediate auxininduced formation of proteolytically active nuclear protein bodies that contain AUX/IAA proteins. Plant Cell 2005; 17:2369-2383.
23. Floyd ZE, Trausch-Azar JS, Reinstein E, Ciechanover A, Schwartz AL. The nuclear ubiquitin-proteasome system degrades Myo D. J Biol Chem 2001; 276:22468-22475.
24. Lenk U, Sommer T. Ubiquitin-mediated proteolysis of a short-lived regulatory protein depends on its cellular localization. J Biol Chem 2000; 275:39403-39910.
25. Karni-Schmidt O, Zupnick A, Castillo M, Ahmed A, Matos T, Bouvet P, et al. p53 is localized to a subnucleolar compartment after proteasomal inhibition in an energy-dependent manner. J Cell Sci 2008; 121:4098-4105.
26. Wade M, Wang YV, Wahl GM. The p53 orchestra: Mdm2 and Mdmx set the tone. Trends Cell Biol 2010; 20:299-309.
27. Gonzalez F, Delahodde A, Kodadek T, Johnston SA. Recruitment of a 19S proteasome subcomplex to an activated promoter. Science 2002; 296:548-550.
28. Koues OI, Dudley RK, Mehta NT, Greer SF. The 19S proteasome positively regulates histone methylation at cytokine inducible genes. Biochim Biophys Acta 2009; 1789:691-701.
29. Truax AD, Koues OI, Mentel MK, Greer SF. The 19S ATPase S6a (S6'/TBP1) regulates the transcription initiation of class II transactivator. J Mol Biol 2010; 395:254-269.
30. Mayr J, Wang HR, Nederlof P, Baumeister W. The import pathway of human and Thermoplasma 20S proteasomes into HeLa cell nuclei is different from that of classical NLS-bearing proteins. Biol Chem 1999; 380:1183-1192.
31. Wang HR, Kania M, Baumeister W, Nederlof PM. Import of human and Thermoplasma 20S proteasomes into nuclei of HeLa cells requires functional NLS sequences. Eur J Cell Biol 1997; 73:105-113.
32. Fahrenkrog B, Koser J, Aebi U. The nuclear pore complex: a jack of all trades? Trends Biochem Sci 2004; 29:175-182.
33. Harel A, Forbes DJ. Importin beta: conducting a much larger cellular symphony. Mol Cell 2004;16:319-330.
34. Hetzer MW, Wente SR. Border control at the nucleus: biogenesis and organization of the nuclear membrane and pore complexes. Dev Cell 2009; 17:606-616.
35. Onischenko E, Weis K. Nuclear pore complex-a coat specifically tailored for the nuclear envelope. Curr Opin Cell Biol 2011.
36. Guttinger S, Laurell E, Kutay U. Orchestrating nuclear envelope disassembly and reassembly during mitosis. Nat Rev Mol Cell Biol 2009; 10:178-191.
37. Fernandez-Martinez J, Rout MP. Nuclear pore complex biogenesis. Curr Opin Cell Biol 2009; 21:603-612.
38. Savulescu AF, Shorer H, Kleifeld O, Cohen I, Gruber R, Glickman MH, et al. Nuclear import of an intact preassembled proteasome particle. Mol Biol Cell 2011; 22:880-891.
39. Chan RC, Forbes DI. In vitro study of nuclear assembly and nuclear import using Xenopus egg extracts. Methods Mol Biol 2006; 322:289-300.
40. Macaulay C, Forbes DJ. Assembly of the nuclear pore: biochemically distinct steps revealed with NEM, GTP gamma S and BAPTA. J Cell Biol 1996; 132:5-20.
41. Rotem A, Gruber R, Shorer H, Shaulov L, Klein E, Harel A. Importin beta regulates the seeding of chromatin with initiation sites for nuclear pore assembly. Mol Biol Cell 2009; 20:4031-4042.
42. Fried H, Kutay U. Nucleocytoplasmic transport: takingan inventory. Cell Mol Life Sci 2003; 60:1659-1688.
43. Gorlich D, Pante N, Kutay U, Aebi U, Bischoff FR. Identification of different roles for RanGDP and RanGTP in nuclear protein import. EMBO J 1996; 15:5584-5594.
44. Effantin G, Rosenzweig R, Glickman MH, Steven AC. Electron microscopic evidence in support of alpha-solenoid models of proteasomal subunits Rpn1 and Rpn2. J Mol Biol 2009; 386:1204-1211.
45. 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; 277:49791-4978.
46. Henderson BR, Fagotto F. The ins and outs of APC and beta-catenin nuclear transport. EMBO Rep 2002; 3:834-839.
47. Jaggi RD, Franco-Obregon A, Muhlhausser P, Thomas F, Kutay U, Ensslin K. Modulation of nuclear pore topology by transport modifiers. Biophys J 2003; 84:665-670.
48. Kutay U, Izaurralde E, Bischoff FR, Mattaj IW, Gorlich D. Dominant-negative mutants of importinbeta block multiple pathways of import and export through the nuclear pore complex. EMBO J 1997; 16:1153-1163.
49. Wu J, Matunis MJ, Kraemer D, Blobel G, Coutavas E. Nup358, a cytoplasmically exposed nucleoporin with peptide repeats, Ran-GTP binding sites, zinc fingers, a cyclophilin A homologous domain, and a leucinerich region. J Biol Chem 1995; 270:14209-14213.
50. Pichler A, Gast A, Seeler JS, Dejean A, Melchior F. The nucleoporin RanBP2 has SUMO1 E3 ligase activity. Cell 2002; 108:109-120.
51. Forbes DJ, Kirschner MW, Newport JW. Spontaneous formation of nucleus-like structures around bacteriophage DNA microinjected into Xenopus eggs. Cell 1983; 34:13-23.
52. Lohka MJ, Masui Y. Formation in vitro of sperm pronuclei and mitotic chromosomes induced by amphibian ooplasmic components. Science 1983; 220:719-721.
53. Cabrera R, Sha Z, Vadakkan TJ, Otero J, Kriegenburg F, Hartmann-Petersen R, et al. Proteasome nuclear import mediated by Arc3 can influence efficient DNA damage repair and mitosis in Schizosaccharomyces pombe. Mol Biol Cell 2010; 21:3125-136.
54. Funakoshi M, Tomko RJ Jr, Kobayashi H, Hochstrasser M. Multiple assembly chaperones govern biogenesis of the proteasome regulatory particle base. Cell 2009; 137:887-899.
55. Hendil KB, Kriegenburg F, Tanaka K, Murata S, Lauridsen AM, Johnsen AH, et al. The 20S proteasome as an assembly platform for the 19S regulatory complex. J Mol Biol 2009; 394:320-328.
56. Kaneko T, Hamazaki J, Iemura S, Sasaki K, Furuyama K, Natsume T, et al. Assembly pathway of the Mammalian proteasome base subcomplex is mediated by multiple specific chaperones. Cell 2009; 137:914-925.
57. Roelofs J, Park S, Haas W, Tian G, McAllister FE, Huo Y, et al. Chaperone-mediated pathway of proteasome regulatory particle assembly. Nature 2009; 459:861-865.