Chaperones and multitasking proteins in the nucleolus

Proteins of the Nucleolus: Regulation, Translocation, & Biomedical Functions

Volumn 9789400758186, Issue , 2013, Pages 149-172

  Kodiha, Mohamed ^a   Stochaj, Ursula ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

Chaperones; Heat shock proteins; Nucleolar multitasking proteins; Protein targeting; Stress

Indexed keywords

EID: 84932145293     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-94-007-5818-6_7     Document Type: Chapter

References (131)

1. Abdelmohsen K, Tominaga K, Lee EK, Srikantan S, Kang M-J, Kim MM, Selimyan R, Martindale JL, Yang X, Carrier F, Zhan M, Becker KG, Gorospe M (2011) Enhanced translation by Nucleolin via G-rich elements in coding and non-coding regions of target mRNAs. Nucleic Acids Res 39:8513-8530
2. Ahmad Y, Boisvert FM, Gregor P, Cobley A, Lamond AI (2008) NOPdb: nucleolar proteome database-2008 update. Nucleic Acids Res 37:D181-D184
3. Albanese V, Reissmann S, Frydman J (2010) A ribosome-anchored chaperone network that facilitates eukaryotic ribosome biogenesis. J Cell Biol 189:69-81
4. Amin MA, Matsunaga S, Uchiyama S, Fukui K (2008) Depletion of nucleophosmin leads to distortion of nucleolar and nuclear structures in HeLa cells. Biochem J 415:345-351
5. Andersen JS, Lam YW, Leung AKL, Ong S-E, Lyon CE, Lamond AI, Mann M (2005) Nucleolar proteome dynamics. Nature 433:77-83
6. Avitabile D, Bailey B, Cottage CT, Sundararaman B, Joyo A, McGregor M, Gude N, Truffa S, Zarrabi A, Konstandin M, Khan M, Mohsin S, Volkers M, Toko H, Mason M, Cheng Z, Din S, Alvarez R, Fischer K, Sussman MA (2011) Nucleolar stress is an early response to myocardial damage involving nucleolar proteins nucleostemin and nucleophosmin. Proc Natl Acad Sci USA 108:6145-6150
7. Banski P, Kodiha M, Stochaj U (2010a) Chaperones and multitasking proteins in the nucleolus: networking together for survival? Trends Biochem Sci 35:361-367
8. Banski P, Mahboubi H, Kodiha M, Shrivastava S, Kanagaratham C, Stochaj U (2010b) Nucleolar targeting of the chaperone Hsc70 is regulated by stress, cell signaling, and a composite targeting signal which is controlled by autoinhibition. J Biol Chem 285:21858-21867
9. Banski P, Kodiha M, Stochaj U (2011) Exploring the nucleolar proteome: novel concepts for chaperone trafficking and function. Curr Proteomics 8:59-82
10. Belenguer P, Caizergues-Ferrer M, Labbe JC, Doree M, Amalric F (1990) Mitosis-specific phosphorylation of nucleolin by p34cdc2 protein kinase. Mol Cell Biol 10:3607-3618
11. Bier C, Knauer SK, Docter D, Schneider G, Kramer OH, Stauber RH (2011) The importin-alpha/nucleophosmin switch controls taspase1 protease function. Traffic 12:703-714
12. Biggiogera M, Fakan S, Kaufmann SH, Black A, Shaper JH, Busch H (1989) Simultaneous immunoelectron microscopic visualization of protein B23 and C23 distribution in the HeLa cell nucleolus. J Histochem Cytochem 37:1371-1374
13. Boisvert F-M, van Koningsbruggen S, Navascues J, Lamond AI (2007) The multifunctional nucleolus. Nat Rev Mol Cell Biol 8:574-585
14. Boulon S, Westman BJ, Hutten S, Boisvert F-M, Lamond AI (2010) The nucleolus under stress. Mol Cell 40:216-227
15. Calle A, Ugrinova I, Epstein AL, Bouvet P, Diaz J-J, Greco A (2008) Nucleolin is required for an efficient herpes simplex virus type 1 infection. J Virol 82:4762-4773
16. Chamousset D, De Wever V, Moorhead GB, Chen Y, Boisvert F-M, Lamond AI, Trinkle-Mulcahy L (2010) RRP1B targets PP1 to mammalian cell nucleoli and is associated with Pre-60S ribosomal subunits. Mol Biol Cell 21:4212-4226
17. Chen D, Huang S (2001) Nucleolar components involved in ribosome biogenesis cycle between the nucleolus and nucleoplasm in interphase cells. J Cell Biol 153:169-176
18. Chiu CM, Tsay YG, Chang CJ, Lee SC (2002) Nopp140 is a mediator of the protein kinase A signaling pathway that activates the acute phase response alpha1-acid glycoprotein gene. J Biol Chem 277:39102-39111
19. Chu A, Matusiewicz N, Stochaj U (2001) Heat-induced nuclear accumulation of hsc70s is regulated by phosphorylation and inhibited in con fl uent cells. FASEB J 15:1478-1480
20. Chun YS, Park JW, Kim MS, Shima H, Nagao M, Lee SH, Park SW, Chung MH (1999) Role of the 78-kDa glucose-regulated protein as an activity modulator of protein phosphatase1 gamma2. Biochem Biophys Res Commun 259:300-304
21. Cmarko D, Smigova J, Minichova L, Popov A (2008) Nucleolus: The ribosome factory. Histol Histopathol 23:1291-1298
22. Cong R, Das S, Bouvet P (2011) The multiple properties and functions of nucleolin. In: Olson MOJ (ed) The nucleolus, vol 15. Springer, New York
23. Coute Y, Burgess JA, Diaz JJ, Chichester C, Lisacek F, Greco A, Sanchez JC (2006) Deciphering the human nucleolar proteome. Mass Spectrom Rev 25:215-234
24. Csermely P, Soti C, Blatch GL (2007) Chaperones as parts of cellular networks. Adv Exp Med Biol 594:55-63
25. Dancso B, Spiro Z, Arslan MA, Nguyen MT, Papp D, Csermely P, Soti C (2010) The heat shock connection of metabolic stress and dietary restriction. Curr Pharm Biotech 11:139-145
26. Daniely Y, Borowiec JA (2000) Formation of a complex between nucleolin and replication protein A after cell stress prevents initiation of DNA replication. J Cell Biol 149:799-810
27. Daniely Y, Dimitrova DD, Borowiec JA (2002) Stress-dependent nucleolin mobilization mediated by p53-nucleolin complex formation. Mol Cell Biol 22:6014-6022
28. De Koning L, Corpet A, Haber JE, Almouzni G (2007) Histone chaperones: An escort network regulating histone traffic. Nat Struct Mol Biol 14:997-1007
29. Del Alamo M, Hogan DJ, Pechmann S, Albanese V, Brown PO, Frydman J (2011) De fining the specificity of cotranslationally acting chaperones by systematic analysis of mRNAs associated with ribosome-nascent chain complexes. PLoS Biol 9:e1001100
30. Emmott E, Hiscox JA (2009) Nucleolar targeting: The hub of the matter. EMBO Rep 10:231-238
31. Emmott E, Dove BK, Howell G, Chappell LA, Reed ML, Boyne JR, You JH, Brooks G, Whitehouse A, Hiscox JA (2008) Viral nucleolar localisation signals determine dynamic trafficking within the nucleolus. Virology 380:191-202
32. Emmott E, Smith C, Emmett SR, Dove BK, Hiscox JA (2010) Elucidation of the avian nucleolar proteome by quantitative proteomics using SILAC and changes in cells infected with the coronavirus infectious bronchitis virus. Proteomics 10:3558-3562
33. Endo A, Kitamura N, Komada M (2009) Nucleophosmin/B23 regulates ubiquitin dynamics in nucleoli by recruiting deubiquitylating enzyme USP36. J Biol Chem 284:27918-27923
34. Flaherty KM, DeLuca-Flaherty C, McKay DB (1990) Three-dimensional structure of the ATPase fragment of a 70K heat-shock cognate protein. Nature 346:623-628
35. Fujiwara Y, Fujiwara K, Goda N, Iwaya N, Tenno T, Shirakawa M, Hiroaki H (2011) Structure and function of the N-terminal nucleolin binding domain of nuclear valosin-containing protein-like 2 (NVL2) harboring a nucleolar localization signal. J Biol Chem 286:21732-21741
36. Gadad SS, Rajan RE, Senapati P, Chatterjee S, Shandilya J, Dash PK, Ranga U, Kundu TK (2011) HIV-1 infection induces acetylation of NPM1 that facilitates Tat localization and enhances viral transactivation. J Mol Biol 410:997-1007
37. Gao H, Jin S, Song Y, Fu M, Wang M, Liu Z, Wu M, Zhan Q (2005) B23 regulates GADD45a nuclear translocation and contributes to GADD45a-induced cell cycle G2-M arrest. J Biol Chem 280:10988-10996
38. Gerber DA, Souquere-Besse S, Puvion F, Dubois MF, Bensaude O, Cochet C (2000) Heat-induced relocalization of protein kinase CK2 Implication of CK2 in the context of cellular stress. J Biol Chem 275:23919-23926
39. Hartl FU, Bracher A, Hayer-Hartl M (2011) Molecular chaperones in protein folding and proteostasis. Nature 475:324-332
40. He F, DiMario P (2011) Structure and function of Nopp140 and treacle. In: Olson MOJ (ed) The nucleolus, vol 15. Springer, New York
41. Heldens L, Dirks RP, Hensen SMM, Onnekink C, van Genesen ST, Rustenburg F, Lubsen NH (2010) Co-chaperones are limiting in a depleted chaperone network. Cell Mol Life Sci 67:4035-4048
42. Hernandez-Verdun D (2011) Assembly and disassembly of the nucleolus during the cell cycle. Nucleus 2:189-194
43. Hiscox JA (2002) The nucleolus-a gateway to viral infection? Arch Virol 147:1077-1089
44. Hiscox JA (2007) RNA viruses: hijacking the dynamic nucleolus. Nat Rev Microbiol 5:119-127
45. Hiscox JA, Whitehouse A, Matthews DA (2010) Nucleolar proteomics and viral infection. Proteomics 10:4077-4086
46. Hornbeck PV, Kornhauser JM, Tkachev S, Zhang B, Skrzypek E, Murray B, Latham V, Sullivan M (2012) PhosphSitePlus: A comprehensive resource for investigating the structure and function of experimentally determined post-translational modifications in man and mouse. Nuc Acids Res 40:D261-D270
47. Hovanessian AG, Soundaramourty C, El Khoury D, Nondier I, Svab J, Krust B (2010) Surface expressed nucleolin is constantly induced in tumor cells to mediate calcium-dependent ligand internalization. PLoS One 5:e15787
48. Hutten S, Prescott A, James J, Riesenberg S, Boulon S, Lam YW, Lamond AI (2011) An intranucleolar body associated with rDNA. Chromosoma 120:481-499
49. Isaac C, Yang Y, Meier UT (1998) Nopp140 functions as a molecular link between the nucleolus and the coiled bodies. J Cell Biol 142:319-329
50. Jaiswal H, Conz C, Otto H, Wol fl e T, Fitzke E, Mayer MP, Rospert S (2011) The chaperone network connected to human ribosome-associated complex. Mol Cell Biol 31:1160-1173
51. Jiang B, Zhang B, Liang P, Song J, Deng H, Tu Z, Deng G, Xiao X (2010) Nucleolin/C23 mediates the antiapoptotic effect of heat shock protein 70 during oxidative stress. FEBS J 277:642-652
52. Kang BH, Plescia J, Dohi T, Rosa J, Doxsey SJ, Altieri DC (2007) Regulation of tumor cell mitochondrial homeostasis by an organelle-specific Hsp90 chaperone network. Cell 131:257-270
53. Kerr LE, Birse-Archbold JL, Short DM, McGregor AL, Heron I, Macdonald DC, Thompson J, Carlson GJ, Kelly JS, McCulloch J, Sharkey J (2007) Nucleophosmin is a novel Bax chaperone that regulates apoptotic cell death. Oncogene 26:2554-2562
54. Khandelwal N, Simpson J, Taylor G, Rafique S, Whitehouse A, Hiscox J, Stark LA (2011) Nucleolar NF-kappa B/RelA mediates apoptosis by causing cytoplasmic relocalization of nucleophosmin. Cell Death Differ 18:1889-1903
55. Kim HJ, Song EJ, Lee KJ (2002) Proteomic analysis of protein phosphorylations in heat shock response and thermotolerance. J Biol Chem 277:23193-23207
56. Kim K, Dimitrova DD, Carta KM, Saxena A, Daras M, Borowiec JA (2005) Novel checkpoint response to genotoxic stress mediated by nucleolin-replication protein a complex formation. Mol Cell Biol 25:2463-2474
57. Kodiha M, Chu A, Lazrak O, Stochaj U (2005) Stress inhibits nucleocytoplasmic shuttling of heat shock protein hsc70. Am J Physiol Cell Physiol 289:C1034-C1041
58. Kodiha M, Banski P, Stochaj U (2011) Computer-based fl uorescence quantification: A novel approach to study nucleolar biology. BMC Cell Biol 12:25
59. Krastev DB, Slabicki M, Paszkowski-Rogacz M, Hubner NC, Junqueira M, Shevchenko A, Mann M, Neugebauer KM, Buchholz F (2011) A systematic RNAi synthetic interaction screen reveals a link between p53 and snoRNP assembly. Nat Cell Biol 13:809-818
60. Latonen L (2011) Nucleolar aggresomes as counterparts of cytoplasmic aggresomes in proteotoxic stress. Bioessays 33:386-395
61. Latonen L, Moore HM, Bai B, Jaamaa S, Laiho M (2011) Proteasome inhibitors induce nucleolar aggregation of proteasome target proteins and polyadenylated RNA by altering ubiquitin availability. Oncogene 30:790-805
62. Lee WK, Lee SY, Kim WI, Rho YH, Bae YS, Lee C, Kim IY, Yu YG (2008) Characterization of the InsP6-dependent interaction between CK2 and Nopp140. Biochem Biophys Res Commun 376:439-444
63. Lee YH, Mungunsukh O, Tutino RL, Marquez AP, Day RM (2010) Angiotensin-II-induced apoptosis requires regulation of nucleolin and Bcl-xL by SHP-2 in primary lung endothelial cells. J Cell Sci 123:1634-1643
64. Li D, Meier UT, Dobrowolska G, Krebs EG (1997) Specific interaction between casein kinase 2 and the nucleolar protein Nopp140. J Biol Chem 272:3773-3779
65. Lin CY, Tan BC-M, Liu H, Shih C-J, Chien K-Y, Lin C-L, Yung BY-M (2010) Dephosphorylation of nucleophosmin by PP1 b facilitates pRB binding and consequent E2F1-dependent DNA repair. Mol Biol Cell 21:4409-4417
66. Lindenboim L, Blacher E, Borner C, Stein R (2010) Regulation of stress-induced nuclear protein redistribution: A new function of Bax and Bak uncoupled from Bcl-x(L). Cell Death Differ 17:346-359
67. Lindstrom MS (2011) NPM1/B23: A multifunctional chaperone in ribosome biogenesis and chromatin remodeling. Biochem Res Int. doi: 10.1155/2011/195209
68. Liu X, Liu Z, Jang S-W, Ma Z, Shinmura K, Kang S, Dong S, Chen J, Fukasawa K, Ye K (2007) Sumoylation of nucleophosmin/B23 regulates its subcellular localization, mediating cell proliferation and survival. Proc Natl Acad Sci USA 104:9679-9684
69. Louvet E, Junéra HR, Berthuy I, Dl H-V (2006) Compartmentation of the nucleolar processing proteins in the granular component is a CK2-driven process. Mol Biol Cell 17:2537-2546
70. Lymberopoulos MH, Bourget A, Ben Abdeljelil N, Pearson A (2011) Involvement of the UL24 protein in herpes simplex virus 1-induced dispersal of B23 and in nuclear egress. Virology 412:341-348
71. Maggi LB, Weber JD (2005) Nucleolar adaptation in human cancer. Cancer Invest 23:599-608
72. Maggi LB, Kuchenruether M, Dadey DY, Schwope RM, Grisendi S, Townsend RR, PandolfiPP, Weber JD (2008) Nucleophosmin serves as a rate-limiting nuclear export chaperone for the Mammalian ribosome. Mol Cell Biol 28:7050-7065
73. McKeown PC, Shaw PJ, McKeown PC, Shaw PJ (2009) Chromatin: linking structure and function in the nucleolus. Chromosoma 118:11-23
74. Meier UT (2005) The many facets of H/ACA ribonucleoproteins. Chromosoma 114:1-14
75. Miyata Y (2009) Protein kinase CK2 in health and disease: CK2: The kinase controlling the Hsp90 chaperone machinery. Cell Mol Life Sci 66:1840-1849
76. Miyata Y, Yahara I (1992) The 90-kDa heat shock protein, HSP90, binds and protects casein kinase II from self-aggregation and enhances its kinase activity. J Biol Chem 267:7042-7047
77. Mollapour M, Neckers L (2011) Post-translational modifications of Hsp90 and their contributions to chaperone regulation. Biochim Biophys Acta Mol Cell Res 1823:648-655
78. Mongelard F, Bouvet P (2007) Nucleolin: A multiFACeTed protein. Trends Cell Biol 17:80-86
79. Morcillo G, Gorab E, Tanguay RM, Diez JL (1997) Specific intranucleolar distribution of Hsp70 during heat shock in polytene cells. Exp Cell Res 236:361-370
80. Morimoto RI (2008) Proteotoxic stress and inducible chaperone networks in neurodegenerative disease and aging. Genes Dev 22:1427-1438
81. Morimoto RI, Driessen AJM, Hegde RS, Langer T (2011) The life of proteins: The good, the mostly good and the ugly. Nat Struct Mol Biol 18:1-4
82. Negi SS, Olson MOJ (2006) Effects of interphase and mitotic phosphorylation on the mobility and location of nucleolar protein B23. J Cell Sci 119:3676-3685
83. Okuwaki M (2008) The structure and functions of NPM1/Nucleophsmin/B23, a multifunctional nucleolar acidic protein. J Biochem 143:441-448
84. Pai CY, Chen HK, Sheu HL, Yeh NH (1995) Cell-cycle-dependent alterations of a highly phosphorylated nucleolar protein p130 are associated with nucleologenesis. J Cell Sci 108:1911-1920
85. Panova TB, Panov KI, Russell J, Zomerdijk JCBM (2006) Casein kinase 2 associates with initiation-competent RNA polymerase I and has multiple roles in ribosomal DNA transcription. Mol Cell Biol 26:5957-5968
86. Pederson T, Tsai RY, Pederson T (2009) In search of nonribosomal nucleolar protein function and regulation. J Cell Biol 184:771-776
87. Pelham HR (1984) Hsp70 accelerates the recovery of nucleolar morphology after heat shock. EMBO J 3:3095-3100
88. Pelham H, Lewis M, Lindquist S (1984) Expression of a Drosophila heat shock protein in mammalian cells: Transient association with nucleoli after heat shock. Philos Trans R Soc Lond B Biol Sci 307:301-307
89. Pellar GJ, DiMario PJ (2003) Deletion and site-specific mutagenesis of nucleolin's carboxy GAR domain. Chromosoma 111:461-469
90. Pendle AF, Clark GP, Boon R, Lewandowska D, Lam YW, Andersen J, Mann M, Lamond AI, Brown JW, Shaw PJ (2005) Proteomic analysis of the Arabidopsis nucleolus suggests novel nucleolar functions. Mol Biol Cell 16:260-269
91. Prinos P, Lacoste M, Wong J, Bonneau A, Georges E (2010) Mutation of cysteine 21 inhibits nucleophosmin/B23 oligomerization and chaperone activity. Int J Biochem Mol Biol 2:24-30
92. Raska I, Shaw PJ, Cmarko D (2006) New insights into nucleolar architecture and activity. Int Rev Cytol 255:177-235
93. Roth DM, Balch WE (2011) Modeling general proteostasis: Proteome balance in health and disease. Curr Opin Cell Biol 23:126-134
94. Sagawa F, Ibrahim H, Morrison AL, Wilusz CJ, Wilusz J (2011) Nucleophosmin deposition during mRNA 3 end processing in fluences poly(A) tail length. EMBO J 30:3994-4005
95. Sahi C, Craig EA (2007) Network of general and specialty J protein chaperones of the yeast cytosol. Proc Natl Acad Sci USA 104:7163-7168
96. Salminen A, Kaarniranta K (2009) SIRT1 regulates the ribosomal DNA locus: epigenetic candles twinkle longevity in the Christmas tree. Biochem Biophys Res Commun 378:6-9
97. Scherl A, Coute Y, Deon C, Calle A, Kindbeiter K, Sanchez JC, Greco A, Hochstrasser D, Diaz JJ (2002) Functional proteomic analysis of human nucleolus. Mol Biol Cell 13:4100-4109
98. Schmidt-Zachmann MS, Nigg EA (1993) Protein localization to the nucleolus: A search for targeting domains in nucleolin. J Cell Sci 105:799-806
99. Schwab MS, Dreyer C (1997) Protein phosphorylation sites regulate the function of the bipartite NLS of nucleolin. Eur J Cell Biol 73:287-297
100. Scott MS, Boisvert F-M, McDowall MD, Lamond AI, Barton GJ (2010) Characterization and prediction of protein nucleolar localization sequences. Nucleic Acids Res 38:7388-7399
101. Scott MS, Boisvert F-M, Lamond AI, Barton GJ (2011a) PNAC: A protein nucleolar association classifier. BMC Genomics 12:74
102. Scott MS, Troshin PV, Barton GJ (2011b) NoD: A nucleolar localization sequence detector for eukaryotic and viral proteins. BMC Bioinformatics 12:317
103. Semba S, Mizuuchi E, Yokozaki H (2010) Requirement of phosphatase of regenerating liver-3 for the nucleolar localization of nucleolin during the progression of colorectal carcinoma. Cancer Sci 101:2254-2261
104. Shandilya J, Swaminathan V, Gadad SS, Choudhari R, Kodaganur GS, Kundu TK (2009) Acetylated NPM1 localizes in the nucleoplasm and regulates transcriptional activation of genes implicated in oral cancer manifestation. Mol Cell Biol 29:5115-5127
105. Sirri V, Urcuqui-Inchima S, Roussel P, Hernandez-Verdun D (2008) Nucleolus: The fascinating nuclear body. Histochem Cell Biol 129:13-31
106. Soundararajan S, Chen W, Spicer EK, Courtenay-Luck N, Fernandes DJ (2008) The nucleolin targeting aptamer AS1411 destabilizes Bcl-2 messenger RNA in human breast cancer cells. Cancer Res 68:2358-2365
107. Stark LA, Taliansky M (2009) Old and new faces of the nucleolus. EMBO Rep 10:35-40
108. Stark C, Breitkreutz BJ, Chatr-Aryamontri A, Boucher L, Oughtred R, Livstone MS, Nixon J, Van Auken K, Wang X, Shi X, Reguly T, Rust JM, Winter A, Dolinski K, Tyers M (2011) The BioGRID interaction database: 2011 update. Nucleic Acids Res 39:D698-D704
109. Swaminathan V, Kishore AH, Febitha KK, Kundu TK (2005) Human histone chaperone nucleophosmin enhances acetylation-dependent chromatin transcription. Mol Cell Biol 25:7534-7545
110. Szebeni A, Olson MOJ (1999) Nucleolar protein B23 has molecular chaperone activities. Protein Sci 8:905-912
111. Szebeni A, Mehrotra B, Baumann A, Adam SA, Wingfield PT, Olson MOJ (1997) Nucleolar protein B23 stimulates nuclear import of the HIV-1 Rev protein and NLS-conjugated albumin. Biochemistry 36:3941-3949
112. Szebeni A, Hingorani K, Negi S, Olson MOJ (2003) Role of protein kinase CK2 phosphorylation in the molecular chaperone activity of nucleolar protein B23. J Biol Chem 278:9107-9115
113. Takagi M, Absalon MJ, McLure KG, Kastan MB (2005) Regulation of p53 translation and induction after DNA damage by ribosomal protein L26 and nucleolin. Cell 123:49-63
114. Thiry M, Cheutin T, Lamaye F, Thelen N, Meier UT, O'Donohue MF, Ploton D (2009) Localization of Nopp140 within mammalian cells during interphase and mitosis. Histochem Cell Biol 132:129-140
115. Ugrinova I, Monier K, Ivaldi C, Thiry M, Storck S, Mongelard F, Bouvet P (2007) Inactivation of nucleolin leads to nucleolar disruption, cell cycle arrest and defects in centrosome duplication. BMC Mol Biol 8:66
116. Unal E, Kinde B, Amon A (2011) Gametogenesis eliminates age-induced cellular damage and resets life span in yeast. Science 332:1554-1557
117. Voisine C, Pedersen JS, Morimoto RI (2010) Chaperone networks: Tipping the balance in protein folding diseases. Neurobiol Dis 40:12-20
118. Voit R, Schnapp A, Kuhn A, Rosenbauer H, Hirschmann P, Stunnenberg HG, Grummt I (1992) The nucleolar transcription factor mUBF is phosphorylated by casein kinase II in the C-terminal hyperacidic tail which is essential for transactivation. EMBO J 11:2211-2218
119. Wang Y, Guan J, Wang H, Leeper D, Iliakis G (2001) Regulation of DNA replication after heat shock by replication protein a-nucleolin interactions. J Biol Chem 276:20579-20588
120. Wang C, Query CC, Meier UT (2002) Immunopuri fied small nucleolar ribonucleoprotein particles pseudouridylate rRNA independently of their association with phosphorylated Nopp140. Mol Cell Biol 22:8457-8466
121. Wang S-A, Li H-Y, Hsu T-I, Chen S-H, Wu C-J, Chang W-C, Hung J-J (2011) Heat shock protein 90 stabilizes nucleolin to increase mRNA stability in mitosis. J Biol Chem 286:43816-43829
122. Watkins NJ, Lemm I, Ingelfinger D, Schneider C, Hossbach M, Urlaub H, Lührmann R (2004) Assembly and maturation of the U3 snoRNP in the nucleoplasm in a large dynamic multiprotein complex. Mol Cell 16:789-798
123. Westman BJ, Verheggen C, Hutten S, Lam YW, Bertrand E, Lamond AI (2010) A proteomic screen for nucleolar SUMO targets shows SUMOylation modulates the function of Nop5/Nop58. Mol Cell 39:618-631
124. Yang Y, Isaac C, Wang C, Dragon F, Pogacic V, Meier UT (2000) Conserved composition of mammalian box H/ACA and box C/D small nucleolar ribonucleoprotein particles and their interaction with the common factor Nopp140. Mol Biol Cell 11:567-577
125. Yang C, Maiguel DA, Carrier F (2002) Identification of nucleolin and nucleophosmin as genotoxic stress-responsive RNA-binding proteins. Nucleic Acids Res 30:2251-2260
126. Yang L, Reece JM, Cho J, Bortner CD, Shears SB (2008) The nucleolus exhibits an osmotically regulated gatekeeping activity that controls the spatial dynamics and functions of nucleolin. J Biol Chem 283:11823-11831
127. Yao Z, Duan S, Hou D, Wang W, Wang G, Liu Y, Wen L, Wu M (2010) B23 acts as a nucleolar stress sensor and promotes cell survival through its dynamic interaction with hnRNPU and hnRNPA1. Oncogene 29:1821-1834
128. Yogev O, Saadon K, Anzi S, Inoue K, Shaulian E (2008) DNA damage-dependent translocation of B23 and p19 ARF is regulated by the Jun N-terminal kinase pathway. Cancer Res 68:1398-1406
129. Yun C, Wang Y, Mukhopadhyay D, Backlund P, Kolli N, Yergey A, Wilkinson KD, Dasso M (2008) Nucleolar protein B23/nucleophosmin regulates the vertebrate SUMO pathway through SENP3 and SENP5 proteases. J Cell Biol 183:589-595
130. Zhao R, Houry WA (2007) Molecular interaction network of the Hsp90 chaperone system. Adv Exp Med Biol 594:27-36
131. Zhu Y, Lu D, DiMario P (1999) Nucleolin, defective for MPF phosphorylation, localizes normally during mitosis and nucleologenesis. Histochem Cell Biol 111:477-487