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Chaperones and Multitasking Proteins in the Nucleolus

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Proteins of the Nucleolus

Abstract

A large number of molecular chaperones and multitasking proteins are located in the nucleolus. The nucleolar association of many of these proteins is dynamic and regulated by the physiological state of the cell. Recent progress in proteomics, imaging and image quantification advanced our understanding of the nucleolar response to stress and disease. In particular, heat shock proteins and their co-chaperones in conjunction with nucleolar multitasking proteins are components that are critical for the proper organization and function of nucleoli, especially under stress and disease conditions. To accomplish these tasks, chaperones together with multitasking proteins are likely to build a compartment-specific network in the nucleolus, where it supports protein homeostasis. However, despite the importance of chaperones and co-chaperones for cellular proteostasis, little is known about their specific functions in the nucleolus. Here, we focus on the targeting signals and molecular mechanisms that underlie the nucleolar trafficking of chaperones and multitasking proteins, as exemplified by heat shock protein hsc70 and the nucleolar proteins B23, nucleolin and Nopp140. It will be discussed how their subcellular localization is affected by physiological or environmental changes and modulated by cell signaling. We describe several links that connect chaperones with nucleolar multitasking proteins and speculate on the specific contributions of chaperones to nucleolar biology. The chapter concludes by highlighting some of the open questions as they are emerging from the current developments in the field.

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Abbreviations

CK2:

Casein kinase 2

DFC:

Dense fibrillar center

FC:

Fibrillar component

GAR:

Glycine-arginine-rich

GC:

Granular component

GFP:

Aequorea victoria green fluorescent protein

HAT:

Histone acetylase

HDAC:

Histone deacetylase

NoD:

Nucleolar localization sequence detector

NoLS:

Nucleolar localization sequence, nucleolar localization signal

NoMP:

Nucleolar multitasking protein

NOR:

Nucleolus organizer region

PP1:

Protein phosphatase PP1

PP2A:

Protein phosphatase PP2A

SnoRNP:

Small nucleolar ribonucleoprotein

SUMO:

Small ubiquitin-like modifier

References

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Ahmad Y, Boisvert FM, Gregor P, Cobley A, Lamond AI (2008) NOPdb: nucleolar proteome database-2008 update. Nucleic Acids Res 37:D181–D184

    Article  PubMed  CAS  Google Scholar 

  • Albanese V, Reissmann S, Frydman J (2010) A ribosome-anchored chaperone network that facilitates eukaryotic ribosome biogenesis. J Cell Biol 189:69–81

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Andersen JS, Lam YW, Leung AKL, Ong S-E, Lyon CE, Lamond AI, Mann M (2005) Nucleolar proteome dynamics. Nature 433:77–83

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • BaÅ„ski P, Kodiha M, Stochaj U (2010a) Chaperones and multitasking proteins in the nucleolus: networking together for survival? Trends Biochem Sci 35:361–367

    Article  PubMed  CAS  Google Scholar 

  • BaÅ„ski 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

    Article  PubMed  CAS  Google Scholar 

  • BaÅ„ski P, Kodiha M, Stochaj U (2011) Exploring the nucleolar proteome: novel concepts for chaperone trafficking and function. Curr Proteomics 8:59–82

    Article  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Boisvert F-M, van Koningsbruggen S, Navascues J, Lamond AI (2007) The multifunctional nucleolus. Nat Rev Mol Cell Biol 8:574–585

    Article  PubMed  CAS  Google Scholar 

  • Boulon S, Westman BJ, Hutten S, Boisvert F-M, Lamond AI (2010) The nucleolus under stress. Mol Cell 40:216–227

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Chu A, Matusiewicz N, Stochaj U (2001) Heat-induced nuclear accumulation of hsc70s is regulated by phosphorylation and inhibited in confluent cells. FASEB J 15:1478–1480

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Cmarko D, Smigova J, Minichova L, Popov A (2008) Nucleolus: the ribosome factory. Histol Histopathol 23:1291–1298

    PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Csermely P, Soti C, Blatch GL (2007) Chaperones as parts of cellular networks. Adv Exp Med Biol 594:55–63

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Daniely Y, Dimitrova DD, Borowiec JA (2002) Stress-dependent nucleolin mobilization mediated by p53-nucleolin complex formation. Mol Cell Biol 22:6014–6022

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Del Alamo M, Hogan DJ, Pechmann S, Albanese V, Brown PO, Frydman J (2011) Defining the specificity of cotranslationally acting chaperones by systematic analysis of mRNAs associated with ribosome-nascent chain complexes. PLoS Biol 9:e1001100

    Article  PubMed  CAS  Google Scholar 

  • Emmott E, Hiscox JA (2009) Nucleolar targeting: the hub of the matter. EMBO Rep 10:231–238

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Hartl FU, Bracher A, Hayer-Hartl M (2011) Molecular chaperones in protein folding and proteostasis. Nature 475:324–332

    Article  PubMed  CAS  Google Scholar 

  • He F, DiMario P (2011) Structure and function of Nopp140 and treacle. In: Olson MOJ (ed) The nucleolus, vol 15. Springer, New York

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Hernandez-Verdun D (2011) Assembly and disassembly of the nucleolus during the cell cycle. Nucleus 2:189–194

    Article  PubMed  Google Scholar 

  • Hiscox JA (2002) The nucleolus – a gateway to viral infection? Arch Virol 147:1077–1089

    Article  PubMed  CAS  Google Scholar 

  • Hiscox JA (2007) RNA viruses: hijacking the dynamic nucleolus. Nat Rev Microbiol 5:119–127

    Article  PubMed  CAS  Google Scholar 

  • Hiscox JA, Whitehouse A, Matthews DA (2010) Nucleolar proteomics and viral infection. Proteomics 10:4077–4086

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Jaiswal H, Conz C, Otto H, Wolfle T, Fitzke E, Mayer MP, Rospert S (2011) The chaperone network connected to human ribosome-associated complex. Mol Cell Biol 31:1160–1173

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Kim HJ, Song EJ, Lee KJ (2002) Proteomic analysis of protein phosphorylations in heat shock response and thermotolerance. J Biol Chem 277:23193–23207

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Kodiha M, BaÅ„ski P, Stochaj U (2011) Computer-based fluorescence quantification: a novel approach to study nucleolar biology. BMC Cell Biol 12:25

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Latonen L (2011) Nucleolar aggresomes as counterparts of cytoplasmic aggresomes in proteotoxic stress. Bioessays 33:386–395

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Lin CY, Tan BC-M, Liu H, Shih C-J, Chien K-Y, Lin C-L, Yung BY-M (2010) Dephosphorylation of nucleophosmin by PP1β facilitates pRB binding and consequent E2F1-dependent DNA repair. Mol Biol Cell 21:4409–4417

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Lindstrom MS (2011) NPM1/B23: a multifunctional chaperone in ribosome biogenesis and chromatin remodeling. Biochem Res Int. doi:10.1155/2011/195209

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Maggi LB, Weber JD (2005) Nucleolar adaptation in human cancer. Cancer Invest 23:599–608

    Article  PubMed  CAS  Google Scholar 

  • Maggi LB, Kuchenruether M, Dadey DY, Schwope RM, Grisendi S, Townsend RR, Pandolfi PP, Weber JD (2008) Nucleophosmin serves as a rate-limiting nuclear export chaperone for the Mammalian ribosome. Mol Cell Biol 28:7050–7065

    Article  PubMed  CAS  Google Scholar 

  • McKeown PC, Shaw PJ, McKeown PC, Shaw PJ (2009) Chromatin: linking structure and function in the nucleolus. Chromosoma 118:11–23

    Article  PubMed  Google Scholar 

  • Meier UT (2005) The many facets of H/ACA ribonucleoproteins. Chromosoma 114:1–14

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Mongelard F, Bouvet P (2007) Nucleolin: a multiFACeTed protein. Trends Cell Biol 17:80–86

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Morimoto RI (2008) Proteotoxic stress and inducible chaperone networks in neurodegenerative disease and aging. Genes Dev 22:1427–1438

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Okuwaki M (2008) The structure and functions of NPM1/Nucleophsmin/B23, a multifunctional nucleolar acidic protein. J Biochem 143:441–448

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Pederson T, Tsai RY, Pederson T (2009) In search of nonribosomal nucleolar protein function and regulation. J Cell Biol 184:771–776

    Article  PubMed  CAS  Google Scholar 

  • Pelham HR (1984) Hsp70 accelerates the recovery of nucleolar morphology after heat shock. EMBO J 3:3095–3100

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Pellar GJ, DiMario PJ (2003) Deletion and site-specific mutagenesis of nucleolin’s carboxy GAR domain. Chromosoma 111:461–469

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Raska I, Shaw PJ, Cmarko D (2006) New insights into nucleolar architecture and activity. Int Rev Cytol 255:177–235

    Article  PubMed  CAS  Google Scholar 

  • Roth DM, Balch WE (2011) Modeling general proteostasis: proteome balance in health and disease. Curr Opin Cell Biol 23:126–134

    Article  PubMed  CAS  Google Scholar 

  • Sagawa F, Ibrahim H, Morrison AL, Wilusz CJ, Wilusz J (2011) Nucleophosmin deposition during mRNA 3′ end processing influences poly(A) tail length. EMBO J 30:3994–4005

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Schmidt-Zachmann MS, Nigg EA (1993) Protein localization to the nucleolus: a search for targeting domains in nucleolin. J Cell Sci 105:799–806

    PubMed  CAS  Google Scholar 

  • Schwab MS, Dreyer C (1997) Protein phosphorylation sites regulate the function of the bipartite NLS of nucleolin. Eur J Cell Biol 73:287–297

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Scott MS, Boisvert F-M, Lamond AI, Barton GJ (2011a) PNAC: a protein nucleolar association classifier. BMC Genomics 12:74

    Article  PubMed  CAS  Google Scholar 

  • Scott MS, Troshin PV, Barton GJ (2011b) NoD: a nucleolar localization sequence detector for eukaryotic and viral proteins. BMC Bioinformatics 12:317

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Sirri V, Urcuqui-Inchima S, Roussel P, Hernandez-Verdun D (2008) Nucleolus: the fascinating nuclear body. Histochem Cell Biol 129:13–31

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Stark LA, Taliansky M (2009) Old and new faces of the nucleolus. EMBO Rep 10:35–40

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Swaminathan V, Kishore AH, Febitha KK, Kundu TK (2005) Human histone chaperone nucleophosmin enhances acetylation-dependent chromatin transcription. Mol Cell Biol 25:7534–7545

    Article  PubMed  CAS  Google Scholar 

  • Szebeni A, Olson MOJ (1999) Nucleolar protein B23 has molecular chaperone activities. Protein Sci 8:905–912

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Unal E, Kinde B, Amon A (2011) Gametogenesis eliminates age-induced cellular damage and resets life span in yeast. Science 332:1554–1557

    Article  PubMed  CAS  Google Scholar 

  • Voisine C, Pedersen JS, Morimoto RI (2010) Chaperone networks: tipping the balance in protein folding diseases. Neurobiol Dis 40:12–20

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Wang C, Query CC, Meier UT (2002) Immunopurified small nucleolar ribonucleoprotein particles pseudouridylate rRNA independently of their association with phosphorylated Nopp140. Mol Cell Biol 22:8457–8466

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Zhao R, Houry WA (2007) Molecular interaction network of the Hsp90 chaperone system. Adv Exp Med Biol 594:27–36

    Article  PubMed  Google Scholar 

  • Zhu Y, Lu D, DiMario P (1999) Nucleolin, defective for MPF phosphorylation, localizes normally during mitosis and nucleologenesis. Histochem Cell Biol 111:477–487

    Article  PubMed  CAS  Google Scholar 

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  1. Department of Physiology, McGill University, 3655 Promenade Sir William Osler, Montreal, QC, Canada

    Mohamed Kodiha & Ursula Stochaj

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  1. Mohamed Kodiha
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  2. Ursula Stochaj
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Correspondence to Mohamed Kodiha .

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  1. , Biology, University of Toronto at Mississauga, Mississauga Rd. N. 3359, Mississauga, L5L1C6, Ontario, Canada

    Danton H O'Day

  2. , Biology, University of Toronto at Mississauga, Mississauga Rd. 3359, Mississauga, L5L1C6, Ontario, Canada

    Andrew Catalano

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Kodiha, M., Stochaj, U. (2013). Chaperones and Multitasking Proteins in the Nucleolus. In: O'Day, D., Catalano, A. (eds) Proteins of the Nucleolus. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-5818-6_7

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