Skip to main content

The Multiple Properties and Functions of Nucleolin

  • Chapter
  • First Online:
The Nucleolus

Part of the book series: Protein Reviews ((PRON,volume 15))

Abstract

Nucleolin, one of the most abundant proteins of the nucleolus is a fascinating protein with multiple proposed functions within and outside the nucleoli. Since its discovery almost 40 years ago, it was proposed that nucleolin is involved in ribosome biogenesis but until recently the molecular mechanisms of this involvement were not known. Thanks to the development of new research strategies, it is now clear that nucleolin is an essential protein for RNA polymerase I transcription, ribosome assembly, cell cycle, and cell proliferation, but the mechanisms of these functions have just begun to be unraveled. In this review, we highlight the most recent data on nucleolin’s properties and functions in the nucleolus and nucleoplasm.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 229.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Allain FH, Bouvet P, Dieckmann T, Feigon J (2000a) Molecular basis of sequence-specific recognition of pre-ribosomal RNA by nucleolin. EMBO J 19:6870–6881

    PubMed  CAS  Google Scholar 

  • Allain FH, Gilbert DE, Bouvet P, Feigon J (2000b) Solution structure of the two N-terminal RNA-binding domains of nucleolin and NMR study of the interaction with its RNA target. J Mol Biol 303:227–241

    PubMed  CAS  Google Scholar 

  • Alvarez M, Quezada C, Navarro C, Molina A, Bouvet P, Krauskopf M, Vera MI (2003) An increased expression of nucleolin is associated with a physiological nucleolar segregation. Biochem Biophys Res Commun 301:152–158

    PubMed  CAS  Google Scholar 

  • Angelov D, Bondarenko VA, Almagro S, Menoni H, Mongelard F, Hans F, Mietton F, Studitsky VM, Hamiche A, Dimitrov S, Bouvet P (2006) Nucleolin is a histone chaperone with FACT-like activity and assists remodeling of nucleosomes. EMBO J 25:1669–1679

    PubMed  CAS  Google Scholar 

  • Applegren N, Hickey RJ, Kleinschmidt AM, Zhou Q, Coll J, Wills P, Swaby R, Wei Y, Quan JY, Lee MY et al (1995) Further characterization of the human cell multiprotein DNA replication complex. J Cell Biochem 59:91–107

    PubMed  CAS  Google Scholar 

  • Arends MJ, Morris RG, Wyllie AH (1990) Apoptosis. The role of the endonuclease. Am J Pathol 136:593–608

    PubMed  CAS  Google Scholar 

  • Arumugam S, Miller MC, Maliekal J, Bates PJ, Trent JO, Lane AN (2010) Solution structure of the RBD1,2 domains from human nucleolin. J Biomol NMR 47:79–83

    PubMed  CAS  Google Scholar 

  • Barrijal S, Perros M, Gu Z, Avalosse BL, Belenguer P, Amalric F, Rommelaere J (1992) Nucleolin forms a specific complex with a fragment of the viral (minus) strand of minute virus of mice DNA. Nucleic Acids Res 20:5053–5060

    PubMed  CAS  Google Scholar 

  • Bates PJ, Kahlon JB, Thomas SD, Trent JO, Miller DM (1999) Antiproliferative activity of G-rich oligonucleotides correlates with protein binding. J Biol Chem 274:26369–26377

    PubMed  CAS  Google Scholar 

  • Bates PJ, Laber DA, Miller DM, Thomas SD, Trent JO (2009) Discovery and development of the G-rich oligonucleotide AS1411 as a novel treatment for cancer. Exp Mol Pathol 86:151–164

    PubMed  CAS  Google Scholar 

  • Belenguer P, Baldin V, Mathieu C, Prats H, Bensaid M, Bouche G, Amalric F (1989) Protein kinase NII and the regulation of rDNA transcription in mammalian cells. Nucleic Acids Res 17:6625–6636

    PubMed  CAS  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 

  • Bharti AK, Olson MO, Kufe DW, Rubin EH (1996) Identification of a nucleolin binding site in human topoisomerase I. J Biol Chem 271:1993–1997

    PubMed  CAS  Google Scholar 

  • Birch JL, Zomerdijk JC (2008) Structure and function of ribosomal RNA gene chromatin. Biochem Soc Trans 36:619–624

    PubMed  CAS  Google Scholar 

  • Birch JL, Tan BC, Panov KI, Panova TB, Andersen JS, Owen-Hughes TA, Russell J, Lee SC, Zomerdijk JC (2009) FACT facilitates chromatin transcription by RNA polymerases I and III. EMBO J 28:854–865

    PubMed  CAS  Google Scholar 

  • Bogre L, Jonak C, Mink M, Meskiene I, Traas J, Ha DT, Swoboda I, Plank C, Wagner E, Heberle-Bors E, Hirt H (1996) Developmental and cell cycle regulation of alfalfa nucMs1, a plant homolog of the yeast Nsr1 and mammalian nucleolin. Plant Cell 8:417–428

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Bonnet H, Filhol O, Truchet I, Brethenou P, Cochet C, Amalric F, Bouche G (1996) Fibroblast growth factor-2 binds to the regulatory beta subunit of CK2 and directly stimulates CK2 activity toward nucleolin. J Biol Chem 271:24781–24787

    PubMed  CAS  Google Scholar 

  • Borer RA, Lehner CF, Eppenberger HM, Nigg EA (1989) Major nucleolar proteins shuttle between nucleus and cytoplasm. Cell 56:379–390

    PubMed  CAS  Google Scholar 

  • Borovjagin AV, Gerbi SA (2004) Xenopus U3 snoRNA docks on pre-rRNA through a novel base-pairing interaction. RNA 10:942–953

    PubMed  CAS  Google Scholar 

  • Bouche G, Caizergues-Ferrer M, Bugler B, Amalric F (1984) Interrelations between the maturation of a 100 kDa nucleolar protein and pre rRNA synthesis in CHO cells. Nucleic Acids Res 12:3025–3035

    PubMed  CAS  Google Scholar 

  • Bouche G, Gas N, Prats H, Baldin V, Tauber JP, Teissie J, Amalric F (1987) Basic fibroblast growth factor enters the nucleolus and stimulates the transcription of ribosomal genes in ABAE cells undergoing G0–G1 transition. Proc Natl Acad Sci U S A 84:6770–6774

    PubMed  CAS  Google Scholar 

  • Bourbon H, Bugler B, Caizergues-Ferrer M, Amalric F (1983) Role of phosphorylation on the maturation pathways of a 100 kDa nucleolar protein. FEBS Lett 155:218–222

    PubMed  CAS  Google Scholar 

  • Bourbon HM, Prudhomme M, Amalric F (1988) Sequence and structure of the nucleolin promoter in rodents: characterization of a strikingly conserved CpG island. Gene 68:73–84

    PubMed  CAS  Google Scholar 

  • Bouvet P, Diaz JJ, Kindbeiter K, Madjar JJ, Amalric F (1998) Nucleolin interacts with several ribosomal proteins through its RGG domain. J Biol Chem 273:19025–19029

    PubMed  CAS  Google Scholar 

  • Bouvet P, Allain FH, Finger LD, Dieckmann T, Feigon J (2001) Recognition of pre-formed and flexible elements of an RNA stem-loop by nucleolin. J Mol Biol 309:763–775

    PubMed  CAS  Google Scholar 

  • Brooks TA, Hurley LH (2010) Targeting MYC expression through G-quadruplexes. Genes Cancer 1:641–649

    PubMed  CAS  Google Scholar 

  • Bugler B, Bourbon H, Lapeyre B, Wallace MO, Chang JH, Amalric F, Olson MO (1987) RNA binding fragments from nucleolin contain the ribonucleoprotein consensus sequence. J Biol Chem 262:10922–10925

    PubMed  CAS  Google Scholar 

  • Bullock PA (1997) The initiation of simian virus 40 DNA replication in vitro. Crit Rev Biochem Mol Biol 32:503–568

    PubMed  CAS  Google Scholar 

  • Caizergues-Ferrer M, Belenguer P, Lapeyre B, Amalric F, Wallace MO, Olson MO (1987) Phosphorylation of nucleolin by a nucleolar type NII protein kinase. Biochemistry 26:7876–7883

    PubMed  CAS  Google Scholar 

  • Caizergues-Ferrer M, Mariottini P, Curie C, Lapeyre B, Gas N, Amalric F, Amaldi F (1989) Nucleolin from Xenopus laevis: cDNA cloning and expression during development. Genes Dev 3:324–333

    PubMed  CAS  Google Scholar 

  • Calle A, Ugrinova I, Epstein AL, Bouvet P, Diaz JJ, Greco A (2008) Nucleolin is required for an efficient herpes simplex virus type 1 infection. J Virol 82:4762–4773

    PubMed  CAS  Google Scholar 

  • Carpentier M, Morelle W, Coddeville B, Pons A, Masson M, Mazurier J, Legrand D (2005) Nucleolin undergoes partial N- and O-glycosylations in the extranuclear cell compartment. Biochemistry 44:5804–5815

    PubMed  CAS  Google Scholar 

  • Chang YI, Hsu SC, Chau GY, Huang CY, Sung JS, Hua WK, Lin WJ (2011) Identification of the methylation preference region in heterogeneous nuclear ribonucleoprotein K by protein arginine methyltransferase 1 and its implication in regulating nuclear/cytoplasmic distribution. Biochem Biophys Res Commun 404:865–869

    PubMed  CAS  Google Scholar 

  • Chathoth KT, Ganesan G, Rao MR (2009) Identification of a novel nucleolin related protein (NRP) gene expressed during rat spermatogenesis. BMC Mol Biol 10:64

    PubMed  Google Scholar 

  • Chen CM, Chiang SY, Yeh NH (1991) Increased stability of nucleolin in proliferating cells by inhibition of its self-cleaving activity. J Biol Chem 266:7754–7758

    PubMed  CAS  Google Scholar 

  • Chen CY, Del Gatto-Konczak F, Wu Z, Karin M (1998) Stabilization of interleukin-2 mRNA by the c-Jun NH2-terminal kinase pathway. Science 280:1945–1949

    PubMed  CAS  Google Scholar 

  • Chen CY, Gherzi R, Andersen JS, Gaietta G, Jurchott K, Royer HD, Mann M, Karin M (2000) Nucleolin and YB-1 are required for JNK-mediated interleukin-2 mRNA stabilization during T-cell activation. Genes Dev 14:1236–1248

    PubMed  CAS  Google Scholar 

  • Chen Y, Zhou X, Liu N, Wang C, Zhang L, Mo W, Hu G (2008) Arginine methylation of hnRNP K enhances p53 transcriptional activity. FEBS Lett 582:1761–1765

    PubMed  CAS  Google Scholar 

  • Choi J, Kim B, Heo K, Kim K, Kim H, Zhan Y, Ranish JA, An W (2007) Purification and characterization of cellular proteins associated with histone H4 tails. J Biol Chem 282:21024–21031

    PubMed  CAS  Google Scholar 

  • Cimato TR, Tang J, Xu Y, Guarnaccia C, Herschman HR, Pongor S, Aletta JM (2002) Nerve growth factor-mediated increases in protein methylation occur predominantly at type I arginine methylation sites and involve protein arginine methyltransferase 1. J Neurosci Res 67:435–442

    PubMed  CAS  Google Scholar 

  • Craig N, Kass S, Sollnerwebb B (1991) Sequence organization and RNA structural motifs directing the mouse primary ribosomal-RNA-processing event. Mol Cell Biol 11:458–467

    PubMed  CAS  Google Scholar 

  • Dambara A, Morinaga T, Fukuda N, Yamakawa Y, Kato T, Enomoto A, Asai N, Murakumo Y, Matsuo S, Takahashi M (2007) Nucleolin modulates the subcellular localization of GDNF-inducible zinc finger protein 1 and its roles in transcription and cell proliferation. Exp Cell Res 313:3755–3766

    PubMed  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

    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

    PubMed  CAS  Google Scholar 

  • de Carcer G, Cerdido A, Medina FJ (1997) NopA64, a novel nucleolar phosphoprotein from proliferating onion cells, sharing immunological determinants with mammalian nucleolin. Planta 201:487–495

    PubMed  Google Scholar 

  • de Verdugo UR, Selinka HC, Huber M, Kramer B, Kellermann J, Hofschneider PH, Kandolf R (1995) Characterization of a 100-kilodalton binding protein for the six serotypes of coxsackie B viruses. J Virol 69:6751–6757

    PubMed  Google Scholar 

  • De A, Donahue SL, Tabah A, Castro NE, Mraz N, Cruise JL, Campbell C (2006) A novel interaction [corrected] of nucleolin with Rad51. Biochem Biophys Res Commun 344:206–213

    PubMed  CAS  Google Scholar 

  • Dear TN, Hainzl T, Follo M, Nehls M, Wilmore H, Matena K, Boehm T (1997) Identification of interaction partners for the basic-helix-loop-helix protein E47. Oncogene 14:891–898

    PubMed  CAS  Google Scholar 

  • Derenzini M (2000) The AgNORs. Micron 31:117–120

    PubMed  CAS  Google Scholar 

  • Derenzini M, Sirri V, Pession A, Trere D, Roussel P, Ochs RL, Hernandez-Verdun D (1995) Quantitative changes of the two major AgNOR proteins, nucleolin and protein B23, related to stimulation of rDNA transcription. Exp Cell Res 219:276–282

    PubMed  CAS  Google Scholar 

  • Dickinson LA, Kohwi-Shigematsu T (1995) Nucleolin is a matrix attachment region DNA-binding protein that specifically recognizes a region with high base-unpairing potential. Mol Cell Biol 15:456–465

    PubMed  CAS  Google Scholar 

  • Didier DK, Klee HJ (1992) Identification of an Arabidopsis DNA-binding protein with homology to nucleolin. Plant Mol Biol 18:977–979

    PubMed  CAS  Google Scholar 

  • Dranovsky A, Vincent I, Gregori L, Schwarzman A, Colflesh D, Enghild J, Strittmatter W, Davies P, Goldgaber D (2001) Cdc2 phosphorylation of nucleolin demarcates mitotic stages and Alzheimer’s disease pathology. Neurobiol Aging 22:517–528

    PubMed  CAS  Google Scholar 

  • Edwards TK, Saleem A, Shaman JA, Dennis T, Gerigk C, Oliveros E, Gartenberg MR, Rubin EH (2000) Role for nucleolin/Nsr1 in the cellular localization of topoisomerase I. J Biol Chem 275:36181–36188

    PubMed  CAS  Google Scholar 

  • Egyhazi E, Pigon A, Chang JH, Ghaffari SH, Dreesen TD, Wellman SE, Case ST, Olson MO (1988) Effects of anti-C23 (nucleolin) antibody on transcription of ribosomal DNA in Chironomus salivary gland cells. Exp Cell Res 178:264–272

    PubMed  CAS  Google Scholar 

  • Erard MS, Belenguer P, Caizergues-Ferrer M, Pantaloni A, Amalric F (1988) A major nucleolar protein, nucleolin, induces chromatin decondensation by binding to histone H1. Eur J Biochem 175:525–530

    PubMed  CAS  Google Scholar 

  • Fang SH, Yeh NH (1993) The self-cleaving activity of nucleolin determines its molecular dynamics in relation to cell proliferation. Exp Cell Res 208:48–53

    PubMed  CAS  Google Scholar 

  • Farin K, Di Segni A, Mor A, Pinkas-Kramarski R (2009) Structure-function analysis of nucleolin and ErbB receptors interactions. PLoS One 4:e6128

    PubMed  Google Scholar 

  • Farin K, Schokoroy S, Haklai R, Cohen-Or I, Elad-Sfadia G, Reyes-Reyes ME, Bates PJ, Cox AD, Kloog Y, Pinkas-Kramarski R (2011) Oncogenic synergism between ErbB1, nucleolin and mutant Ras. Cancer Res 71(6):2140–2151

    PubMed  CAS  Google Scholar 

  • Finger LD, Johansson C, Rinaldi B, Bouvet P, Feigon J (2004) Contributions of the RNA-binding and linker domains and RNA structure to the specificity and affinity of the nucleolin RBD12/NRE interaction. Biochemistry 43:6937–6947

    PubMed  CAS  Google Scholar 

  • Gai D, Roy R, Wu C, Simmons DT (2000) Topoisomerase I associates specifically with simian virus 40 large-T-antigen double hexamer-origin complexes. J Virol 74:5224–5232

    PubMed  CAS  Google Scholar 

  • Garcia MC, Williams J, Johnson K, Olden K, Roberts JD (2011) Arachidonic acid stimulates formation of a novel complex containing nucleolin and RhoA. FEBS Lett 585:618–622

    PubMed  CAS  Google Scholar 

  • Gaudreault I, Guay D, Lebel M (2004) YB-1 promotes strand separation in vitro of duplex DNA containing either mispaired bases or cisplatin modifications, exhibits endonucleolytic activities and binds several DNA repair proteins. Nucleic Acids Res 32:316–327

    PubMed  CAS  Google Scholar 

  • Gaume X, Monier K, Argoul F, Mongelard F, Bouvet P (2011) Biochem Res Int. 2011:187624

    Google Scholar 

  • Geahlen RL, Harrison ML (1984) Induction of a substrate for casein kinase II during lymphocyte mitogenesis. Biochim Biophys Acta 804:169–175

    PubMed  CAS  Google Scholar 

  • Ghisolfi L, Kharrat A, Joseph G, Amalric F, Erard M (1992) Concerted activities of the RNA ­recognition and the glycine-rich C-terminal domains of nucleolin are required for efficient complex formation with pre-ribosomal RNA. Eur J Biochem 209:541–548

    PubMed  CAS  Google Scholar 

  • Ghisolfi-Nieto L, Joseph G, Puvion-Dutilleul F, Amalric F, Bouvet P (1996) Nucleolin is a sequence-specific RNA-binding protein: characterization of targets on pre-ribosomal RNA. J Mol Biol 260:34–53

    PubMed  CAS  Google Scholar 

  • Gilchrist JS, Abrenica B, DiMario PJ, Czubryt MP, Pierce GN (2002) Nucleolin is a calcium-binding protein. J Cell Biochem 85:268–278

    PubMed  CAS  Google Scholar 

  • Gillet G, Michel D, Crisanti P, Guerin M, Herault Y, Pessac B, Calothy G, Brun G, Volovitch M (1993) Serum factors and v-src control two complementary mitogenic pathways in quail ­neuroretinal cells in culture. Oncogene 8:565–574

    PubMed  CAS  Google Scholar 

  • Ginisty H, Amalric F, Bouvet P (1998) Nucleolin functions in the first step of ribosomal RNA processing. EMBO J 17:1476–1486

    PubMed  CAS  Google Scholar 

  • Ginisty H, Sicard H, Roger B, Bouvet P (1999) Structure and functions of nucleolin. J Cell Sci 112(pt 6):761–772

    PubMed  CAS  Google Scholar 

  • Ginisty H, Serin G, Ghisolfi-Nieto L, Roger B, Libante V, Amalric F, Bouvet P (2000) Interaction of nucleolin with an evolutionarily conserved pre-ribosomal RNA sequence is required for the assembly of the primary processing complex. J Biol Chem 275:18845–18850

    PubMed  CAS  Google Scholar 

  • Ginisty H, Amalric F, Bouvet P (2001) Two different combinations of RNA-binding domains determine the RNA binding specificity of nucleolin. J Biol Chem 276:14338–14343

    PubMed  CAS  Google Scholar 

  • Gonzalez V, Hurley LH (2010) The C-terminus of nucleolin promotes the formation of the c-MYC G-quadruplex and inhibits c-MYC promoter activity. Biochemistry 49:9706–9714

    PubMed  CAS  Google Scholar 

  • Gottlieb S, Esposito RE (1989) A new role for a yeast transcriptional silencer gene, SIR2, in regulation of recombination in ribosomal DNA. Cell 56:771–776

    PubMed  CAS  Google Scholar 

  • Grinstein E, Wernet P, Snijders PJ, Rosl F, Weinert I, Jia W, Kraft R, Schewe C, Schwabe M, Hauptmann S, Dietel M, Meijer CJ, Royer HD (2002) Nucleolin as activator of human papillomavirus type 18 oncogene transcription in cervical cancer. J Exp Med 196:1067–1078

    PubMed  CAS  Google Scholar 

  • Grinstein E, Shan Y, Karawajew L, Snijders PJ, Meijer CJ, Royer HD, Wernet P (2006) Cell cycle-controlled interaction of nucleolin with the retinoblastoma protein and cancerous cell transformation. J Biol Chem 281:22223–22235

    PubMed  CAS  Google Scholar 

  • Grinstein E, Du Y, Santourlidis S, Christ J, Uhrberg M, Wernet P (2007) Nucleolin regulates gene expression in CD34-positive hematopoietic cells. J Biol Chem 282:12439–12449

    PubMed  CAS  Google Scholar 

  • Grummt I (2003) Life on a planet of its own: regulation of RNA polymerase I transcription in the nucleolus. Genes Dev 17:1691–1702

    PubMed  CAS  Google Scholar 

  • Guderian G, Peter C, Wiesner J, Sickmann A, Schulze-Osthoff K, Fischer U, Grimmler M (2011) RioK1, a new interactor of protein arginine methyltransferase 5 (PRMT5), competes with pICln for binding and modulates PRMT5 complex composition and substrate specificity. J Biol Chem 286:1976–1986

    PubMed  CAS  Google Scholar 

  • Gulli MP, Girard JP, Zabetakis D, Lapeyre B, Melese T, Caizergues-Ferrer M (1995a) gar2 is a nucleolar protein from Schizosaccharomyces pombe required for 18S rRNA and 40S ribosomal subunit accumulation. Nucleic Acids Res 23:1912–1918

    PubMed  CAS  Google Scholar 

  • Gulli MP, Girard JP, Zabetakis D, Lapeyre B, Melese T, Caizerguesferrer M (1995b) Gar2 Is a nucleolar protein from Schizosaccharomyces pombe required for 18s ribosomal-RNA and 40s ribosomal-subunit accumulation. Nucleic Acids Res 23:1912–1918

    PubMed  CAS  Google Scholar 

  • Gulli MP, Faubladier M, Sicard H, Caizergues-Ferrer M (1997) Mitosis-specific phosphorylation of gar2, a fission yeast nucleolar protein structurally related to nucleolin. Chromosoma 105:532–541

    PubMed  CAS  Google Scholar 

  • Hanakahi LA, Dempsey LA, Li MJ, Maizels N (1997) Nucleolin is one component of the B cell-specific transcription factor and switch region binding protein, LR1. Proc Natl Acad Sci U S A 94:3605–3610

    PubMed  CAS  Google Scholar 

  • Hanakahi LA, Sun H, Maizels N (1999) High affinity interactions of nucleolin with G-G-paired rDNA. J Biol Chem 274:15908–15912

    PubMed  CAS  Google Scholar 

  • Hanakahi LA, Bu Z, Maizels N (2000) The C-terminal domain of nucleolin accelerates nucleic acid annealing. Biochemistry 39:15493–15499

    PubMed  CAS  Google Scholar 

  • Hannan RD, Cavanaugh A, Hempel WM, Moss T, Rothblum L (1999) Identification of a mammalian RNA polymerase I holoenzyme containing components of the DNA repair/replication system. Nucleic Acids Res 27:3720–3727

    PubMed  CAS  Google Scholar 

  • Hatfield DL, Carlson BA, Xu XM, Mix H, Gladyshev VN (2006) Selenocysteine incorporation machinery and the role of selenoproteins in development and health. Prog Nucleic Acid Res Mol Biol 81:97–142

    PubMed  CAS  Google Scholar 

  • Heo K, Kim B, Kim K, Choi J, Kim H, Zhan Y, Ranish JA, An W (2007) Isolation and characterization of proteins associated with histone H3 tails in vivo. J Biol Chem 282:15476–15483

    PubMed  CAS  Google Scholar 

  • Hernandez-Verdun D (1991) The nucleolus today. J Cell Sci 99(pt 3):465–471

    PubMed  Google Scholar 

  • Herrera AH, Olson MO (1986) Association of protein C23 with rapidly labeled nucleolar RNA. Biochemistry 25:6258–6264

    PubMed  CAS  Google Scholar 

  • Hirano M, Kaneko S, Yamashita T, Luo H, Qin W, Shirota Y, Nomura T, Kobayashi K, Murakami S (2003) Direct interaction between nucleolin and hepatitis C virus NS5B. J Biol Chem 278:5109–5115

    PubMed  CAS  Google Scholar 

  • Hovanessian AG (2006) Midkine, a cytokine that inhibits HIV infection by binding to the cell surface expressed nucleolin. Cell Res 16:174–181

    PubMed  CAS  Google Scholar 

  • Huddleson JP, Ahmad N, Lingrel JB (2006) Up-regulation of the KLF2 transcription factor by fluid shear stress requires nucleolin. J Biol Chem 281:15121–15128

    PubMed  CAS  Google Scholar 

  • Iftode C, Daniely Y, Borowiec JA (1999) Replication protein A (RPA): the eukaryotic SSB. Crit Rev Biochem Mol Biol 34:141–180

    PubMed  CAS  Google Scholar 

  • Ishikawa F, Matunis MJ, Dreyfuss G, Cech TR (1993) Nuclear proteins that bind the pre-mRNA 3′ splice site sequence r(UUAG/G) and the human telomeric DNA sequence d(TTAGGG)n. Mol Cell Biol 13:4301–4310

    PubMed  CAS  Google Scholar 

  • Ishimaru D, Zuraw L, Ramalingam S, Sengupta TK, Bandyopadhyay S, Reuben A, Fernandes DJ, Spicer EK (2010) Mechanism of regulation of bcl-2 mRNA by nucleolin and A  +  U-rich ­element-binding factor 1 (AUF1). J Biol Chem 285:27182–27191

    PubMed  CAS  Google Scholar 

  • Issinger OG, Martin T, Richter WW, Olson M, Fujiki H (1988) Hyperphosphorylation of N-60, a protein structurally and immunologically related to nucleolin after tumour-promoter treatment. EMBO J 7:1621–1626

    PubMed  CAS  Google Scholar 

  • Jiang Y, Xu XS, Russell JE (2006) A nucleolin-binding 3′ untranslated region element stabilizes beta-globin mRNA in vivo. Mol Cell Biol 26:2419–2429

    PubMed  CAS  Google Scholar 

  • Jiang B, Zhang B, Liang P, Song J, Deng H, Tu Z, Deng G, Xiao X (2010a) Nucleolin/C23 mediates the antiapoptotic effect of heat shock protein 70 during oxidative stress. FEBS J 277:642–652

    PubMed  CAS  Google Scholar 

  • Jiang Y, Li Z, Nagy PD (2010b) Nucleolin/Nsr1p binds to the 3′ noncoding region of the tombusvirus RNA and inhibits replication. Virology 396:10–20

    PubMed  CAS  Google Scholar 

  • Johansson C, Finger LD, Trantirek L, Mueller TD, Kim S, Laird-Offringa IA, Feigon J (2004) Solution structure of the complex formed by the two N-terminal RNA-binding domains of nucleolin and a pre-rRNA target. J Mol Biol 337:799–816

    PubMed  CAS  Google Scholar 

  • Johansson H, Svensson F, Runnberg R, Simonsson T, Simonsson S (2010) Phosphorylated nucleolin interacts with translationally controlled tumor protein during mitosis and with Oct4 during interphase in ES cells. PLoS One 5:e13678

    PubMed  Google Scholar 

  • Johnson FB, Marciniak RA, Guarente L (1998) Telomeres, the nucleolus and aging. Curr Opin Cell Biol 10:332–338

    PubMed  CAS  Google Scholar 

  • Kass S, Tyc K, Steitz JA, Sollner-Webb B (1990) The U3 small nucleolar ribonucleoprotein functions in the first step of preribosomal RNA processing. Cell 60:897–908

    PubMed  CAS  Google Scholar 

  • Khurts S, Masutomi K, Delgermaa L, Arai K, Oishi N, Mizuno H, Hayashi N, Hahn WC, Murakami S (2004) Nucleolin interacts with telomerase. J Biol Chem 279:51508–51515

    PubMed  CAS  Google Scholar 

  • Kojima H, Suzuki T, Kato T, Enomoto K, Sato S, Tabata S, Saez-Vasquez J, Echeverria M, Nakagawa T, Ishiguro S, Nakamura K (2007) Sugar-inducible expression of the nucleolin-1 gene of Arabidopsis thaliana and its role in ribosome synthesis, growth and development. Plant J 49:1053–1063

    PubMed  CAS  Google Scholar 

  • Kondo K, Inouye M (1992) Yeast NSR1 protein that has structural similarity to mammalian nucleolin is involved in pre-rRNA processing. J Biol Chem 267:16252–16258

    PubMed  CAS  Google Scholar 

  • Lapeyre B, Amalric F (1985) A powerful method for the preparation of cDNA libraries: isolation of cDNA encoding a 100-kDal nucleolar protein. Gene 37:215–220

    PubMed  CAS  Google Scholar 

  • Lapeyre B, Bourbon H, Amalric F (1987) Nucleolin, the major nucleolar protein of growing eukaryotic cells: an unusual protein structure revealed by the nucleotide sequence. Proc Natl Acad Sci U S A 84:1472–1476

    PubMed  CAS  Google Scholar 

  • Lee WC, Zabetakis D, Melese T (1992) NSR1 is required for pre-rRNA processing and for the proper maintenance of steady-state levels of ribosomal subunits. Mol Cell Biol 12:3865–3871

    PubMed  CAS  Google Scholar 

  • Leitinger N, Wesierska-Gadek J (1993) ADP-ribosylation of nucleolar proteins in HeLa tumor cells. J Cell Biochem 52:153–158

    PubMed  CAS  Google Scholar 

  • Lischwe MA, Smetana K, Olson MOJ, Busch H (1979) Protein-C23 and protein-B23 are the major nucleolar silver staining proteins. Life Sci 25:701–708

    PubMed  CAS  Google Scholar 

  • Lischwe MA, Richards RL, Busch RK, Busch H (1981) Localization of phosphoprotein C23 to nucleolar structures and to the nucleolus organizer regions. Exp Cell Res 136:101–109

    PubMed  CAS  Google Scholar 

  • Lischwe MA, Roberts KD, Yeoman LC, Busch H (1982) Nucleolar specific acidic phosphoprotein C23 is highly methylated. J Biol Chem 257:4600–4602

    Google Scholar 

  • Lischwe MA, Cook RG, Ahn YS, Yeoman LC, Busch H (1985) Clustering of glycine and NG, NG-dimethylarginine in nucleolar protein C23. Biochemistry 24:6025–6028

    PubMed  CAS  Google Scholar 

  • Liu HT, Yung BY (1999) In vivo interaction of nucleophosmin/B23 and protein C23 during cell cycle progression in HeLa cells. Cancer Lett 144:45–54

    PubMed  CAS  Google Scholar 

  • Losfeld ME, Khoury DE, Mariot P, Carpentier M, Krust B, Briand JP, Mazurier J, Hovanessian AG, Legrand D (2009) The cell surface expressed nucleolin is a glycoprotein that triggers ­calcium entry into mammalian cells. Exp Cell Res 315:357–369

    PubMed  CAS  Google Scholar 

  • Loyola A, Almouzni G (2004) Histone chaperones, a supporting role in the limelight. Biochim Biophys Acta 1677:3–11

    PubMed  CAS  Google Scholar 

  • Ma N, Matsunaga S, Takata H, Ono-Maniwa R, Uchiyama S, Fukui K (2007) Nucleolin functions in nucleolus formation and chromosome congression. J Cell Sci 120:2091–2105

    PubMed  CAS  Google Scholar 

  • Mamrack MD, Olson MO, Busch H (1979) Amino acid sequence and sites of phosphorylation in a highly acidic region of nucleolar nonhistone protein C23. Biochemistry 18:3381–3386

    PubMed  CAS  Google Scholar 

  • Maridor G, Nigg EA (1990) cDNA sequences of chicken nucleolin/C23 and NO38/B23, two major nucleolar proteins. Nucleic Acids Res 18:1286

    PubMed  CAS  Google Scholar 

  • McGrath KE, Smothers JF, Dadd CA, Madireddi MT, Gorovsky MA, Allis CD (1997) An abundant nucleolar phosphoprotein is associated with ribosomal DNA in Tetrahymena macronuclei. Mol Biol Cell 8:97–108

    PubMed  CAS  Google Scholar 

  • McStay B, Grummt I (2008) The epigenetics of rRNA genes: from molecular to chromosome ­biology. Annu Rev Cell Dev Biol 24:131–157

    PubMed  CAS  Google Scholar 

  • Miniard AC, Middleton LM, Budiman ME, Gerber CA, Driscoll DM (2010) Nucleolin binds to a subset of selenoprotein mRNAs and regulates their expression. Nucleic Acids Res 38:4807–4820

    PubMed  CAS  Google Scholar 

  • Miranda GA, Chokler I, Aguilera RJ (1995) The murine nucleolin protein is an inducible DNA and ATP binding protein which is readily detected in nuclear extracts of lipopolysaccharide-treated splenocytes. Exp Cell Res 217:294–308

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Mongelard F, Bouvet P (2010) AS-1411, a guanosine-rich oligonucleotide aptamer targeting nucleolin for the potential treatment of cancer, including acute myeloid leukemia. Curr Opin Mol Ther 12:107–114

    PubMed  CAS  Google Scholar 

  • Morimoto H, Okamura H, Haneji T (2002) Interaction of protein phosphatase 1 delta with nucleolin in human osteoblastic cells. J Histochem Cytochem 50:1187–1193

    PubMed  CAS  Google Scholar 

  • Murayama R, Harada Y, Shibata T, Kuroda K, Hayakawa S, Shimizu K, Tanaka T (2007) Influenza A virus non-structural protein 1 (NS1) interacts with cellular multifunctional protein nucleolin during infection. Biochem Biophys Res Commun 362:880–885

    PubMed  CAS  Google Scholar 

  • Nasirudin KM, Ehtesham NZ, Tuteja R, Sopory SK, Tuteja N (2005) The Gly-Arg-rich C-terminal domain of pea nucleolin is a DNA helicase that catalytically translocates in the 5′- to 3′-direction. Arch Biochem Biophys 434:306–315

    PubMed  CAS  Google Scholar 

  • Olson MO, Thompson BA (1983) Distribution of proteins among chromatin components of nucleoli. Biochemistry 22:3187–3193

    PubMed  CAS  Google Scholar 

  • Olson MO, Ezrailson EG, Guetzow K, Busch H (1975) Localization and phosphorylation of nuclear, nucleolar and extranucleolar non-histone proteins of Novikoff hepatoma ascites cells. J Mol Biol 97:611–619

    PubMed  CAS  Google Scholar 

  • Olson MO, Rivers ZM, Thompson BA, Kao WY, Case ST (1983) Interaction of nucleolar phosphoprotein C23 with cloned segments of rat ribosomal deoxyribonucleic acid. Biochemistry 22:3345–3351

    PubMed  CAS  Google Scholar 

  • Orrick LR, Olson MO, Busch H (1973) Comparison of nucleolar proteins of normal rat liver and Novikoff hepatoma ascites cells by two-dimensional polyacrylamide gel electrophoresis. Proc Natl Acad Sci U S A 70:1316–1320

    PubMed  CAS  Google Scholar 

  • Pasternack MS, Bleier KJ, McInerney TN (1991) Granzyme A binding to target cell proteins. Granzyme A binds to and cleaves nucleolin in vitro. J Biol Chem 266:14703–14708

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Peter M, Nakagawa J, Doree M, Labbe JC, Nigg EA (1990) Identification of major nucleolar proteins as candidate mitotic substrates of cdc2 kinase. Cell 60:791–801

    PubMed  CAS  Google Scholar 

  • Petricka JJ, Nelson TM (2007) Arabidopsis nucleolin affects plant development and patterning. Plant Physiol 144:173–186

    PubMed  CAS  Google Scholar 

  • Pollice A, Zibella MP, Bilaud T, Laroche T, Pulitzer JF, Gilson E (2000) In vitro binding of nucleolin to double-stranded telomeric DNA. Biochem Biophys Res Commun 268:909–915

    PubMed  CAS  Google Scholar 

  • Pontvianne F, Matia I, Douet J, Tourmente S, Medina FJ, Echeverria M, Saez-Vasquez J (2007) Characterization of AtNUC-L1 reveals a central role of nucleolin in nucleolus organization and silencing of AtNUC-L2 gene in Arabidopsis. Mol Biol Cell 18:369–379

    PubMed  CAS  Google Scholar 

  • Pontvianne F, Abou-Ellail M, Douet J, Comella P, Matia I, Chandrasekhara C, Debures A, Blevins T, Cooke R, Medina FJ, Tourmente S, Pikaard CS, Saez-Vasquez J (2010) Nucleolin is required for DNA methylation state and the expression of rRNA gene variants in Arabidopsis thaliana. PLoS Genet 6:e1001225

    PubMed  Google Scholar 

  • Puvion-Dutilleul F, Puvion E, Bachellerie JP (1997) Early stages of pre-rRNA formation within the nucleolar ultrastructure of mouse cells studied by in situ hybridization with a 5′ETS leader probe. Chromosoma 105:496–505

    PubMed  CAS  Google Scholar 

  • Raman B, Guarnaccia C, Nadassy K, Zakhariev S, Pintar A, Zanuttin F, Frigyes D, Acatrinei C, Vindigni A, Pongor G, Pongor S (2001) N(omega)-arginine dimethylation modulates the interaction between a Gly/Arg-rich peptide from human nucleolin and nucleic acids. Nucleic Acids Res 29:3377–3384

    PubMed  CAS  Google Scholar 

  • Rankin ML, Heine MA, Xiao S, LeBlanc MD, Nelson JW, DiMario PJ (1993) A complete nucleolin cDNA sequence from Xenopus laevis. Nucleic Acids Res 21:169

    PubMed  CAS  Google Scholar 

  • Rao SV, Mamrack MD, Olson MO (1982) Localization of phosphorylated highly acidic regions in the NH2-terminal half of nucleolar protein C23. J Biol Chem 257:15035–15041

    PubMed  CAS  Google Scholar 

  • Reboud JP, Reboud AM, Madjar JJ, Buisson M (1974) Study of protein reactivity in rat liver ribosomes. Effect of RNA addition to autodigested ribosomes. Acta Biol Med Ger 33:661–666

    PubMed  CAS  Google Scholar 

  • Reeder RH (1990) rRNA synthesis in the nucleolus. Trends Genet 6:390–395

    PubMed  CAS  Google Scholar 

  • Rickards B, Flint SJ, Cole MD, LeRoy G (2007) Nucleolin is required for RNA polymerase I transcription in vivo. Mol Cell Biol 27:937–948

    PubMed  CAS  Google Scholar 

  • Roger B, Moisand A, Amalric F, Bouvet P (2002) Repression of RNA polymerase I transcription by nucleolin is independent of the RNA sequence that is transcribed. J Biol Chem 277:10209–10219

    PubMed  CAS  Google Scholar 

  • Roger B, Moisand A, Amalric F, Bouvet P (2003) Nucleolin provides a link between RNA polymerase I transcription and pre-ribosome assembly. Chromosoma 111:399–407

    PubMed  CAS  Google Scholar 

  • Roussel P, Hernandez-Verdun D (1994) Identification of Ag-NOR proteins, markers of proliferation related to ribosomal gene activity. Exp Cell Res 214:465–472

    PubMed  CAS  Google Scholar 

  • Roussel P, Belenguer P, Amalric F, Hernandez-Verdun D (1992) Nucleolin is an Ag-NOR protein; this property is determined by its amino-terminal domain independently of its phosphorylation state. Exp Cell Res 203:259–269

    PubMed  CAS  Google Scholar 

  • Rubbi CP, Milner J (2003) Disruption of the nucleolus mediates stabilization of p53 in response to DNA damage and other stresses. EMBO J 22:6068–6077

    PubMed  CAS  Google Scholar 

  • Saez-Vasquez J, Caparros-Ruiz D, Barneche F, Echeverria M (2004) A plant snoRNP complex containing snoRNAs, fibrillarin, and nucleolin-like proteins is competent for both rRNA gene binding and pre-rRNA processing in vitro. Mol Cell Biol 24:7284–7297

    PubMed  CAS  Google Scholar 

  • Said EA, Courty J, Svab J, Delbe J, Krust B, Hovanessian AG (2005) Pleiotrophin inhibits HIV infection by binding the cell surface-expressed nucleolin. FEBS J 272:4646–4659

    PubMed  CAS  Google Scholar 

  • Salazar R, Brandt R, Kellermann J, Krantz S (2000) Purification and characterization of a 200 kDa fructosyllysine-specific binding protein from cell membranes of U937 cells. Glycoconj J 17:713–716

    PubMed  CAS  Google Scholar 

  • Sapp M, Knippers R, Richter A (1986) DNA binding properties of a 110 kDa nucleolar protein. Nucleic Acids Res 14:6803–6820

    PubMed  CAS  Google Scholar 

  • Sato H, Kusumoto-Matsuo R, Ishii Y, Mori S, Nakahara T, Shinkai-Ouchi F, Kawana K, Fujii T, Taketani Y, Kanda T, Kukimoto I (2009) Identification of nucleolin as a protein that binds to human papillomavirus type 16 DNA. Biochem Biophys Res Commun 387:525–530

    PubMed  CAS  Google Scholar 

  • Scheer U, Benavente R (1990) Functional and dynamic aspects of the mammalian nucleolus. Bioessays 12:14–21

    PubMed  CAS  Google Scholar 

  • Schmidt-Zachmann MS, Dargemont C, Kuhn LC, Nigg EA (1993) Nuclear export of proteins: the role of nuclear retention. Cell 74:493–504

    PubMed  CAS  Google Scholar 

  • Schrick JJ, Hughes MJ, Anderson KP, Croyle ML, Lingrel JB (1999) Characterization of the lung Kruppel-like transcription factor gene and upstream regulatory elements. Gene 236:185–195

    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 

  • Seinsoth S, Uhlmann-Schiffler H, Stahl H (2003) Bidirectional DNA unwinding by a ternary complex of T antigen, nucleolin and topoisomerase I. EMBO Rep 4:263–268

    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

    PubMed  CAS  Google Scholar 

  • Serin G, Joseph G, Faucher C, Ghisolfi L, Bouche G, Amalric F, Bouvet P (1996) Localization of nucleolin binding sites on human and mouse pre-ribosomal RNA. Biochimie 78:530–538

    PubMed  CAS  Google Scholar 

  • Serin G, Joseph G, Ghisolfi L, Bauzan M, Erard M, Amalric F, Bouvet P (1997) Two RNA-binding domains determine the RNA-binding specificity of nucleolin. J Biol Chem 272:13109–13116

    PubMed  CAS  Google Scholar 

  • Shi H, Huang Y, Zhou H, Song X, Yuan S, Fu Y, Luo Y (2007) Nucleolin is a receptor that mediates antiangiogenic and antitumor activity of endostatin. Blood 110:2899–2906

    PubMed  CAS  Google Scholar 

  • Sicard H, Faubladier M, Noaillac-Depeyre J, Leger-Silvestre I, Gas N, Caizergues-Ferrer M (1998) The role of the Schizosaccharomyces pombe gar2 protein in nucleolar structure and function depends on the concerted action of its highly charged N terminus and its RNA-binding domains. Mol Biol Cell 9:2011–2023

    PubMed  CAS  Google Scholar 

  • Singh K, Laughlin J, Kosinski PA, Covey LR (2004) Nucleolin is a second component of the CD154 mRNA stability complex that regulates mRNA turnover in activated T cells. J Immunol 173:976–985

    PubMed  CAS  Google Scholar 

  • Sipos K, Olson MO (1991) Nucleolin promotes secondary structure in ribosomal RNA. Biochem Biophys Res Commun 177:673–678

    PubMed  CAS  Google Scholar 

  • Sirri V, Roussel P, Trere D, Derenzini M, Hernandez-Verdun D (1995) Amount variability of total and individual Ag-NOR proteins in cells stimulated to proliferate. J Histochem Cytochem 43:887–893

    PubMed  CAS  Google Scholar 

  • Smyth MJ, Browne KA, Thia KY, Apostolidis VA, Kershaw MH, Trapani JA (1994) Hypothesis: cytotoxic lymphocyte granule serine proteases activate target cell endonucleases to trigger apoptosis. Clin Exp Pharmacol Physiol 21:67–70

    PubMed  CAS  Google Scholar 

  • Srivastava M, Fleming PJ, Pollard HB, Burns AL (1989) Cloning and sequencing of the human nucleolin cDNA. FEBS Lett 250:99–105

    PubMed  CAS  Google Scholar 

  • Storck S, Shukla M, Dimitrov S, Bouvet P (2007) Functions of the histone chaperone nucleolin in diseases. Subcell Biochem 41:125–144

    PubMed  Google Scholar 

  • Storck S, Thiry M, Bouvet P (2009) Conditional knockout of nucleolin in DT40 cells reveals the functional redundancy of its RNA-binding domains. Biol Cell 101:153–167

    PubMed  CAS  Google Scholar 

  • Strang BL, Boulant S, Coen DM (2010) Nucleolin associates with the human cytomegalovirus DNA polymerase accessory subunit UL44 and is necessary for efficient viral replication. J Virol 84:1771–1784

    PubMed  CAS  Google Scholar 

  • Sun D, Guo K, Shin YJ (2011) Evidence of the formation of G-quadruplex structures in the promoter region of the human vascular endothelial growth factor gene. Nucleic Acids Res 39(4):1256–1265

    PubMed  CAS  Google Scholar 

  • Suzuki N, Kobayashi M, Sakata K, Suzuki T, Hosoya T (1991) Synergistic stimulatory effect of glucocorticoid, EGF and insulin on the synthesis of ribosomal RNA and phosphorylation of nucleolin in primary cultured rat hepatocytes. Biochim Biophys Acta 1092:367–375

    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

    PubMed  CAS  Google Scholar 

  • Tang L, Nogales E, Ciferri C (2010) Structure and function of SWI/SNF chromatin remodeling complexes and mechanistic implications for transcription. Prog Biophys Mol Biol 102:122–128

    PubMed  CAS  Google Scholar 

  • Tawfic S, Goueli SA, Olson MO, Ahmed K (1994) Androgenic regulation of phosphorylation and stability of nucleolar protein nucleolin in rat ventral prostate. Prostate 24:101–106

    PubMed  CAS  Google Scholar 

  • Tediose T, Kolev M, Sivasankar B, Brennan P, Morgan BP, Donev R (2010) Interplay between REST and nucleolin transcription factors: a key mechanism in the overexpression of genes upon increased phosphorylation. Nucleic Acids Res 38:2799–2812

    PubMed  CAS  Google Scholar 

  • Teng Y, Girvan AC, Casson LK, Pierce WM Jr, Qian M, Thomas SD, Bates PJ (2007) AS1411 alters the localization of a complex containing protein arginine methyltransferase 5 and nucleolin. Cancer Res 67:10491–10500

    PubMed  CAS  Google Scholar 

  • Tong CG, Reichler S, Blumenthal S, Balk J, Hsieh HL, Roux SJ (1997) Light regulation of the abundance of mRNA encoding a nucleolin-like protein localized in the nucleoli of pea nuclei. Plant Physiol 114:643–652

    PubMed  CAS  Google Scholar 

  • Tuteja N, Huang NW, Skopac D, Tuteja R, Hrvatic S, Zhang J, Pongor S, Joseph G, Faucher C, Amalric F et al (1995) Human DNA helicase IV is nucleolin, an RNA helicase modulated by phosphorylation. Gene 160:143–148

    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

    PubMed  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

    PubMed  CAS  Google Scholar 

  • Warner JR (1989) Synthesis of ribosomes in Saccharomyces cerevisiae. Microbiol Rev 53:256–271

    PubMed  CAS  Google Scholar 

  • Welfle H, Henkel B, Bielka H (1976) Ionic interactions in eukaryotic ribosomes: splitting of the subunits of rat liver ribosomes by treatment with monovalent cations. Acta Biol Med Ger 35:401–411

    PubMed  CAS  Google Scholar 

  • Xu X, Hamhouyia F, Thomas SD, Burke TJ, Girvan AC, McGregor WG, Trent JO, Miller DM, Bates PJ (2001) Inhibition of DNA replication and induction of S phase cell cycle arrest by G-rich oligonucleotides. J Biol Chem 276:43221–43230

    PubMed  CAS  Google Scholar 

  • Yanagida M, Shimamoto A, Nishikawa K, Furuichi Y, Isobe T, Takahashi N (2001) Isolation and proteomic characterization of the major proteins of the nucleolin-binding ribonucleoprotein complexes. Proteomics 1:1390–1404

    PubMed  CAS  Google Scholar 

  • Yang TH, Tsai WH, Lee YM, Lei HY, Lai MY, Chen DS, Yeh NH, Lee SC (1994) Purification and characterization of nucleolin and its identification as a transcription repressor. Mol Cell Biol 14:6068–6074

    PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • Yang C, Kim MS, Chakravarty D, Indig FE, Carrier F (2009) Nucleolin binds to the proliferating cell nuclear antigen and inhibits nucleotide excision repair. Mol Cell Pharmacol 1:130–137

    PubMed  CAS  Google Scholar 

  • Yuan X, Zhou Y, Casanova E, Chai M, Kiss E, Grone HJ, Schutz G, Grummt I (2005) Genetic inactivation of the transcription factor TIF-IA leads to nucleolar disruption, cell cycle arrest, and p53-mediated apoptosis. Mol Cell 19:77–87

    PubMed  CAS  Google Scholar 

  • Zhang Y, Bhatia D, Xia H, Castranova V, Shi X, Chen F (2006) Nucleolin links to arsenic-induced stabilization of GADD45alpha mRNA. Nucleic Acids Res 34:485–495

    PubMed  CAS  Google Scholar 

  • Zhang J, Tsaprailis G, Bowden GT (2008) Nucleolin stabilizes Bcl-X L messenger RNA in response to UVA irradiation. Cancer Res 68:1046–1054

    PubMed  CAS  Google Scholar 

  • Zhou G, Seibenhener ML, Wooten MW (1997) Nucleolin is a protein kinase C-zeta substrate. Connection between cell surface signaling and nucleus in PC12 cells. J Biol Chem 272:31130–31137

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The author’s work is supported by grants from Agence Nationale de la Recherche (ANR-07-BLAN-0062-01), Région Rhône-Alpes MIRA 2007 and 2010, Association pour la Recherche sur le Cancer n° ECL2010R01122, CEFIPRA n° 3803-1, and CNRS.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Philippe Bouvet .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2011 Springer Science+Business Media, LLC

About this chapter

Cite this chapter

Cong, R., Das, S., Bouvet, P. (2011). The Multiple Properties and Functions of Nucleolin. In: Olson, M. (eds) The Nucleolus. Protein Reviews, vol 15. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-0514-6_9

Download citation

Publish with us

Policies and ethics