Functions Of The Histone Chaperone Nucleolin In Diseases

  • Sébastien Storck
  • Manu Shukla
  • Stefan Dimitrov
  • Philippe Bouvet
Part of the Subcellular Biochemistry book series (SCBI, volume 41)

Alteration of nuclear morphology is often used by pathologist as diagnostic marker for malignancies like cancer. In particular, the staining of cells by the silver staining methods (AgNOR) has been proved to be an important tool for predicting the clinical outcome of some cancer diseases. Two major argyrophilic proteins responsible for the strong staining of cells in interphase are the nucleophosmin (B23) and the nucleolin (C23) nucleolar proteins. Interestingly these two proteins have been described as chromatin associated proteins with histone chaperone activities and also as proteins able to regulate chromatin transcription. Nucleolin seems to be over-expressed in highly proliferative cells and is involved in many aspect of gene expression: chromatin remodeling, DNA recombination and replication, RNA transcription by RNA polymerase I and II, rRNA processing, mRNA stabilisation, cytokinesis and apoptosis. Interestingly, nucleolin is also found on the cell surface in a wide range of cancer cells, a property which is being used as a marker for the diagnosis of cancer and for the development of anti-cancer drugs to inhibit proliferation of cancer cells. In addition to its implication in cancer, nucleolin has been described not only as a marker or as a protein being involved in many diseases like viral infections, autoimmune diseases, Alzheimer’s disease pathology but also in drug resistance. In this review we will focus on the chromatin associated functions of nucleolin and discuss the functions of nucleolin or its use as diagnostic marker and as a target for therapy


Nucleolar Protein Histone Chaperone RecQ Helicases rRNA Transcription AgNOR Protein 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


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  1. Allain FH, Bouvet P, Dieckmann T, Feigon J (2000a) Molecular basis of sequence-specific recognition of pre-ribosomal RNA by nucleolin. Embo J 19: 6870–6881Google Scholar
  2. 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 [In Process Citation]. J Mol Biol 303: 227–241Google Scholar
  3. 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: 152–158PubMedGoogle Scholar
  4. Amoura Z, outouzov S, Piette JC (2000) The role of nucleosomes in lupus. Curr Opin Rheumatol 12: 369–373PubMedGoogle Scholar
  5. 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: 1669–1679PubMedGoogle Scholar
  6. 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: 91–107PubMedGoogle Scholar
  7. 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: 5053–5060PubMedGoogle Scholar
  8. Bastress KL, Stajich JM, Speer MC, Gilbert JR (2005) The genes encoding for D4Z4 binding proteins HMGB2, YY1, NCL, and MYOD1 are excluded as candidate genes for FSHD1B. Neuromuscul Disord 15: 316–320PubMedGoogle Scholar
  9. 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: 26369–26377PubMedGoogle Scholar
  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: 3607–3618PubMedGoogle Scholar
  11. Bharti AK, Olson MO, Kufe DW, Rubin EH (1996) Identification of a nucleolin binding site in human topoisomerase I. J Biol Chem 271: 1993–1997PubMedGoogle Scholar
  12. 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(40):24781–24787Google Scholar
  13. Borer RA, Lehner CF, Eppenberger HM, Nigg EA (1989) Major nucleolar proteins shuttle between nucleus and cytoplasm. Cell 56: 379–390PubMedGoogle Scholar
  14. Borggrefe T, Wabl M, Akhmedov AT, Jessberger R (1998) A B-cell-specific DNA recombination complex. J Biol Chem 273: 17025–17035PubMedGoogle Scholar
  15. Bose S, Basu M, Banerjee AK (2004) Role of nucleolin in human parainfluenza virus type 3 infection of human lung epithelial cells. J Virol 78: 8146–8158PubMedGoogle Scholar
  16. 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: 3025–3035PubMedGoogle Scholar
  17. 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(19):6770–6774.PubMedGoogle Scholar
  18. 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: 218–222PubMedGoogle Scholar
  19. Bourbon HM, Lapeyre B, Amalric F (1988) Structure of the mouse nucleolin gene. The complete sequence reveals that each RNA binding domain is encoded by two independent exons. J Mol Biol 200: 627–638PubMedGoogle Scholar
  20. 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: 763–775PubMedGoogle Scholar
  21. 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: 19025–19029PubMedGoogle Scholar
  22. Brandt R, Nawka M, Kellermann J, Salazar R, Becher D, Krantz S (2004) Nucleophosmin is a component of the fructoselysine-specific receptor in cell membranes of Mono Mac 6 and U937 monocyte-like cells. 0Biochim Biophys Acta 1670: 132–136Google Scholar
  23. Bugler B, Caizergues-Ferrer M, Bouche G, Bourbon H, Amalric F (1982) Detection and localization of a class of proteins immunologically related to a 100-kDa nucleolar protein. Eur J Biochem 128: 475–480PubMedCrossRefGoogle Scholar
  24. 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: 7876–7883PubMedGoogle Scholar
  25. 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: 324–333PubMedGoogle Scholar
  26. Callebaut C, Blanco J, Benkirane N, Krust B, Jacotot E, Guichard G, Seddiki N, Svab J, Dam E, Muller S, Briand JP, Hovanessian AG (1998a) Identification of V3 loop-binding proteins as potential receptors implicated in the binding of HIV particles to CD4(+) cells. J Biol Chem 273: 21988–21997Google Scholar
  27. Callebaut C, Jacotot E, Blanco J, Krust B, Hovanessian AG (1998b) Increased rate of HIV-1 entry and its cytopathic effect in CD4+/CXCR4+ T cells expressing relatively high levels of CD26. Exp Cell Res 241: 352–362Google Scholar
  28. Callebaut C, Nisole S, Briand JP, Krust B, Hovanessian AG (2001) Inhibition of HIV infection by the cytokine midkine. Virology 281: 248–264PubMedGoogle Scholar
  29. Christian S, Pilch J, Akerman ME, Porkka K, Laakkonen P, Ruoslahti E (2003) Nucleolin expressed at the cell surface is a marker of endothelial cells in angiogenic blood vessels. J Cell Biol 163: 871–878PubMedGoogle Scholar
  30. Chung L, Utz PJ (2004) Antibodies in scleroderma: direct pathogenicity and phenotypic associations. Curr Rheumatol Rep 6: 156–163PubMedGoogle Scholar
  31. Cook PR (1999) The organization of replication and transcription. Science 284: 1790–1795PubMedGoogle Scholar
  32. Dalziel RG, Mendelson SC, Quinn JP (1992) The nuclear autoimmune antigen Ku is also present on the cell surface. Autoimmunity 13: 265–267PubMedGoogle Scholar
  33. 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: 799–810PubMedGoogle Scholar
  34. Daniely Y, Dimitrova DD, Borowiec JA (2002) Stress-dependent nucleolin mobilization mediated by p53-nucleolin complex formation. Mol Cell Biol 22: 6014–6022PubMedGoogle Scholar
  35. Dapic V, Abdomerovic V, Marrington R, Peberdy J, Rodger A, Trent JO, Bates PJ (2003) Biophysical and biological properties of quadruplex oligodeoxyribonucleotides. Nucleic Acids Res 31: 2097–2107PubMedGoogle Scholar
  36. De A, Donahue SL, Tabah A, Castro NE, Mraz N, Cruise JL, Campbell C (2006) A novel interation of nucleolin with Rad51. Biochem Biophys Res Commun 344: 206–213PubMedGoogle Scholar
  37. 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: 6751–6757PubMedGoogle Scholar
  38. Dempsey LA, Hanakahi LA, Maizels N (1998) A specific isoform of hnRNP D interacts with DNA in the LR1 heterodimer: canonical RNA binding motifs in a sequence-specific duplex DNA binding protein. J Biol Chem 273: 29224–29229PubMedGoogle Scholar
  39. Deng JS, Ballou B, Hofmeister JK (1996) Internalization of anti-nucleolin antibody into viable HEp-2 cells. Mol Biol Rep 23: 191–195PubMedGoogle Scholar
  40. Derenzini M, Sirri V, Trere D, Ochs RL (1995) The quantity of nucleolar proteins nucleolin and protein B23 is related to cell doubling time in human cancer cells. Lab Invest 73: 497–502PubMedGoogle Scholar
  41. Derenzini M, Trere D, Pession A, Govoni M, Sirri V, Chieco P (2000) Nucleolar size indicates the rapidity of cell proliferation in cancer tissues. J Pathol 191: 181–186PubMedGoogle Scholar
  42. Derenzini M, Trere D, Pession A, Montanaro L, Sirri V, Ochs RL (1998) Nucleolar function and size in cancer cells. Am J Pathol 152: 1291–1297PubMedGoogle Scholar
  43. 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: 456–465PubMedGoogle Scholar
  44. Dumler I, Stepanova V, Jerke U, Mayboroda OA, Vogel F, Bouvet P, Tkachuk V, Haller H, Gulba DC (1999) Urokinase-induced mitogenesis is mediated by casein kinase 2 and nucleolin. Curr Biol 9: 1468–1476PubMedGoogle Scholar
  45. 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: 36181–36188PubMedGoogle Scholar
  46. 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: 264–272PubMedGoogle Scholar
  47. Erard M, Lakhdar-Ghazal F, Amalric F (1990) Repeat peptide motifs which contain beta-turns and modulate DNA condensation in chromatin. Eur J Biochem 191: 19–26PubMedGoogle Scholar
  48. 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: 525–530PubMedGoogle Scholar
  49. Falaschi A (2000) Eukaryotic DNA replication: a model for a fixed double replisome. Trends Genet 16: 88–92PubMedGoogle Scholar
  50. Fischer AH, Bardarov S Jr, Jiang Z (2004) Molecular aspects of diagnostic nucleolar and nuclear envelope changes in prostate cancer. J Cell Biochem 91: 170–184PubMedGoogle Scholar
  51. Gabellini D, Green MR, Tupler R (2002) Inappropriate gene activation in FSHD: a repressor complex binds a chromosomal repeat deleted in dystrophic muscle. Cell 110: 339–348PubMedGoogle Scholar
  52. Galande S (2002) Chromatin (dis)organization and cancer: BUR-binding proteins as biomarkers for cancer. Curr Cancer Drug Targets 2: 157–190PubMedGoogle Scholar
  53. 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: 316–327PubMedGoogle Scholar
  54. Ghirardello A, Doria A, Zampieri S, Tarricone E, Tozzoli R, Villalta D, Bizzaro N, Piccoli A, Gambari PF (2004) Antinucleosome antibodies in SLE: a two-year follow-up study of 101 patients. J Autoimmun 22: 235–240PubMedGoogle Scholar
  55. Ghisolfi L, Joseph G, Amalric F, Erard M (1992a) The glycine-rich domain of nucleolin has an unusual supersecondary structure responsible for its RNA-helix-destabilizing properties. J Biol Chem 267: 2955–2959Google Scholar
  56. Ghisolfi L, Kharrat A, Joseph G, Amalric F, Erard M (1992b) 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: 541–548Google Scholar
  57. 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: 34–53PubMedGoogle Scholar
  58. Ginisty H, Amalric F, Bouvet P (1998) Nucleolin functions in the first step of ribosomal RNA processing. Embo J 17: 1476–1486PubMedGoogle Scholar
  59. 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: 14338–14343PubMedGoogle Scholar
  60. 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: 18845–18850PubMedGoogle Scholar
  61. Ginisty H, Sicard H, Roger B, Bouvet P (1999) Structure and functions of nucleolin. J Cell Sci 112: 761–772PubMedGoogle Scholar
  62. Gotzmann J, Eger A, Meissner M, Grimm R, Gerner C, Sauermann G, Foisner R (1997) Two-dimensional electrophoresis reveals a nuclear matrix-associated nucleolin complex of basic isoelectric point [In Process Citation]. Electrophoresis 18: 2645–2653PubMedGoogle Scholar
  63. 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: 1067–1078PubMedGoogle Scholar
  64. Grisendi S, Bernardi R, Rossi M, Cheng K, Khandker L, Manova K, Pandolfi PP (2005) Role of nucleophosmin in embryonic development and tumorigenesis. Nature 437: 147–153PubMedGoogle Scholar
  65. Hanakahi LA, Bu Z, Maizels N (2000) The C-terminal domain of nucleolin accelerates nucleic acid annealing. Biochemistry 39: 15493–15499PubMedGoogle Scholar
  66. 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 USA 94:3605–3610PubMedGoogle Scholar
  67. Hanakahi LA, Maizels N (2000) Transcriptional activation by LR1 at the Emu enhancer and switch region sites. Nucleic Acids Res 28: 2651–2657PubMedGoogle Scholar
  68. Hanakahi LA, Sun H, Maizels N (1999) High affinity interactions of nucleolin with G-G-paired rDNA. J Biol Chem 274: 15908–15912PubMedGoogle Scholar
  69. Harms G, Kraft R, Grelle G, Volz B, Dernedde J, Tauber R (2001) Identification of nucleolin as a new L-selectin ligand. Biochem J 360: 531–538PubMedGoogle Scholar
  70. Hickson ID (2003) RecQ helicases: caretakers of the genome. Nat Rev Cancer 3: 169–178PubMedGoogle Scholar
  71. Hirano K, Miki Y, Hirai Y, Sato R, Itoh T, Hayashi A, Yamanaka M, Eda S, Beppu M (2005) A multifunctional shuttling protein nucleolin is a macrophage receptor for apoptotic cells. J Biol Chem 280: 39284–39293PubMedGoogle Scholar
  72. Hovanessian AG, Puvion-Dutilleul F, Nisole S, Svab J, Perret E, Deng JS, Krust B (2000) The cell-surface-expressed nucleolin is associated with the actin cytoskeleton. Exp Cell Res 261: 312–328PubMedGoogle Scholar
  73. Iftode C, Daniely Y, Borowiec JA (1999) Replication protein A (RPA): the eukaryotic SSB. Crit Rev Biochem Mol Biol 34: 141–180PubMedGoogle Scholar
  74. 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: 4301–4310PubMedGoogle Scholar
  75. Issinger OG, Martin T, Richter WW, Olson M and Fujiki H (1988) Hyperphosphorylation of N-60, a protein structurally and immunologically related to nucleolin after tumour-promoter treatment. EMBO J. 7:1621–1626PubMedGoogle Scholar
  76. Joo EJ, ten Dam GB, van Kuppevelt TH, Toida T, Linhardt RJ, Kim YS (2005) Nucleolin: acharan sulfate-binding protein on the surface of cancer cells. Glycobiology 15: 1–9PubMedGoogle Scholar
  77. Jordan P, Heid H, Kinzel V, Kubler D (1994) Major cell surface-located protein substrates of an ecto-protein kinase are homologs of known nuclear proteins. Biochemistry 33: 14696–14706PubMedGoogle Scholar
  78. Kelavkar U, Wang S, Badr K (2002) KU 70/80 lupus autoantigen is the transcription factor induced by interleukins (IL)-13 and -4 leading to induction of 15-lipoxygenase (15-LO) in human cells. Adv Exp Med Biol 507: 469–481PubMedGoogle Scholar
  79. 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: 51508–51515PubMedGoogle Scholar
  80. 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: 2463–2474PubMedGoogle Scholar
  81. Kinzler KW, Vogelstein B (1997) Cancer-susceptibility genes. Gatekeepers and caretakers. Nature 386: 761, 763PubMedGoogle Scholar
  82. Kubler D (2001) Ecto-protein kinase substrate p120 revealed as the cell-surface-expressed nucleolar phosphoprotein Nopp140: a candidate protein for extracellular Ca2+-sensing. Biochem J 360: 579–587PubMedGoogle Scholar
  83. Legrand D, Vigie K, Said EA, Elass E, Masson M, Slomianny MC, Carpentier M, Briand JP, Mazurier J, Hovanessian AG (2004) Surface nucleolin participates in both the binding and endocytosis of lactoferrin in target cells. Eur J Biochem 271: 303–317PubMedGoogle Scholar
  84. Lischwe MA, Roberts KD, Yeoman LC, Busch H (1982) Nucleolar specific acidic phosphoprotein C23 is highly methylated. J Biol Chem 257: 14600–14602PubMedGoogle Scholar
  85. Lotze MT, Tracey KJ (2005) High-mobility group box 1 protein (HMGB1): nuclear weapon in the immune arsenal. Nat Rev Immunol 5: 331–342PubMedGoogle Scholar
  86. Maridor G, Nigg EA (1990) cDna sequences of chicken nucleolin/C23 and No38/B23, two major nucleolar proteins. Nucleic Acids Res 18: 1286PubMedGoogle Scholar
  87. Martens JA, Winston F (2003) Recent advances in understanding chromatin remodeling by Swi/Snf complexes. Curr Opin Genet Dev 13: 136–142PubMedGoogle Scholar
  88. Mehes G, Pajor L (1995) Nucleolin and fibrillarin expression in stimulated lymphocytes and differentiating HL-60 cells. A flow cytometric assay. Cell Prolif 28: 329–336PubMedGoogle Scholar
  89. 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: 306–315PubMedGoogle Scholar
  90. Nickel W (2005) Unconventional secretory routes: direct protein export across the plasma membrane of mammalian cells. Traffic 6: 607–614PubMedGoogle Scholar
  91. Nisole S, Krust B, Hovanessian AG (2002a) Anchorage of HIV on Permissive Cells Leads to Coaggregation of Viral Particles with Surface Nucleolin at Membrane Raft Microdomains. Exp Cell Res 276: 155–173Google Scholar
  92. Nisole S, Said EA, Mische C, Prevost MC, Krust B, Bouvet P, Bianco A, Briand JP, Hovanessian AG (2002b) The anti-HIV pentameric pseudopeptide HB-19 binds the C-terminal end of nucleolin and prevents anchorage of virus particles in the plasma membrane of target cells. J Biol Chem 277: 20877–20886Google Scholar
  93. 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: 611–619PubMedGoogle Scholar
  94. 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: 3345–3351PubMedGoogle Scholar
  95. Olson MO, Thompson BA (1983) Distribution of proteins among chromatin components of nucleoli. Biochemistry 22: 3187–3193PubMedGoogle Scholar
  96. Orphanides G, LeRoy G, Chang CH, Luse DS, Reinberg D (1998) FACT, a factor that facilitates transcript elongation through nucleosomes. Cell 92: 105–116PubMedGoogle Scholar
  97. Orrick LR, Olson MO, usch 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 USA 70: 1316–1320PubMedGoogle Scholar
  98. Pederson T (2002) Proteomics of the nucleolus: more proteins, more functions? Trends Biochem Sci 27: 111–112PubMedGoogle Scholar
  99. 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: 791–801PubMedGoogle Scholar
  100. Philpott A, Krude T, Laskey RA (2000) Nuclear chaperones. Semin Cell Dev Biol 11: 7–14PubMedGoogle Scholar
  101. 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: 909–915PubMedGoogle Scholar
  102. Reeves WH, Pierani A, Chou CH, Ng T, Nicastri C, Roeder RG, Sthoeger ZM (1991) Epitopes of the p70 and p80 (Ku) lupus autoantigens. J Immunol 146: 2678–2686PubMedGoogle Scholar
  103. 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: 10209–10219PubMedGoogle Scholar
  104. Roussel P, Sirri V, Hernandez-Verdun D (1994) Quantification of Ag-NOR proteins using Ag-NOR staining on western blots. J Histochem Cytochem 42: 1513–1517PubMedGoogle Scholar
  105. Ruggero D, Pandolfi PP (2003) Does the ribosome translate cancer? Nat Rev Cancer 3: 179–192PubMedGoogle Scholar
  106. 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: 4646–4659PubMedGoogle Scholar
  107. Said EA, Krust B, Nisole S, Svab J, Briand JP, Hovanessian AG (2002) The anti-HIV cytokine midkine binds the cell surface-expressed nucleolin as a low affinity receptor. J Biol Chem 277: 37492–37502PubMedGoogle Scholar
  108. Sapp M, Knippers R, Richter A (1986) DNA binding properties of a 110 kDa nucleolar protein. Nucleic Acids Res 14: 6803–6820PubMedGoogle Scholar
  109. Sapp M, Richter A, Weisshart K, Caizergues-Ferrer M, Amalric F, Wallace MO, Kirstein MN, Olson MO (1989) Characterization of a 48-kDa nucleic-acid-binding fragment of nucleolin. Eur J Biochem 179: 541–548PubMedGoogle Scholar
  110. 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: 263–268PubMedGoogle Scholar
  111. 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: 530–538PubMedGoogle Scholar
  112. 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: 13109–13116PubMedGoogle Scholar
  113. 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: 2011–2023PubMedGoogle Scholar
  114. Sinclair JF, Dean-Nystrom EA, O’Brien AD (2006), The established intimin receptor Tir and the putative eucaryotic intimin receptors nucleolin and beta1 integrin localize at or near the site of enterohemorrhagic Escherichia coli O157:H7 adherence to enterocytes in vivo. Infect Immun 74: 1255–1265PubMedGoogle Scholar
  115. Sinclair JF, O’Brien AD (2002), Cell surface-localized nucleolin is a eukaryotic receptor for the adhesin intimin-gamma of enterohemorrhagic Escherichia coli O157:H7. J Biol Chem 277: 2876–2885PubMedGoogle Scholar
  116. Sinclair JF, O’Brien AD (2004), Intimin types alpha, beta, and gamma bind to nucleolin with equivalent affinity but lower avidity than to the translocated intimin receptor. J Biol Chem 279: 33751–33758PubMedGoogle Scholar
  117. Sirri V, Roussel P, Gendron MC, Hernandez-Verdun D (1997), Amount of the two major Ag-NOR proteins, nucleolin, and protein B23 is cell-cycle dependent. Cytometry 28: 147–156PubMedGoogle Scholar
  118. 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: 887–893PubMedGoogle Scholar
  119. Srivastava M, Fleming PJ, Pollard HB, Burns AL (1989), Cloning and sequencing of the human nucleolin cDNA. FEBS Lett 250: 99–105PubMedGoogle Scholar
  120. Suzuki N, Kobayashi M, Sakara 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 1092:367–375PubMedGoogle Scholar
  121. Suzuki N, Matsui H, Hosoya T (1985), Effects of androgen and polyamines on the phosphorylation of nucleolar proteins from rat ventral prostates with particular reference to 110-kDa phosphoprotein. J Biol Chem 260:8050–8055PubMedGoogle Scholar
  122. 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: 49–63PubMedGoogle Scholar
  123. 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.PubMedGoogle Scholar
  124. 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: 143–148PubMedGoogle Scholar
  125. Valdez BC, Henning D, Busch RK, Srivastava M, Busch H (1995), Immunodominant RNA recognition motifs of human nucleolin/C23. Mol Immunol 32: 1207–1213PubMedGoogle Scholar
  126. Wang Y, Guan J, Wang H, Leeper D, Iliakis G (2001), Regulation of dna replication vafter heat shock by replication protein a-nucleolin interactions. J Biol Chem 276: 20579–20588PubMedGoogle Scholar
  127. Wang Y, Perrault AR, Iliakis G (1998), Replication protein A as a potential regulator of DNA replication in cells exposed to hyperthermia. Radiat Res 149: 284–293PubMedGoogle Scholar
  128. Warrener P, Petryshyn R (1991), Phosphorylation and proteolytic degradation of nucleolin from 3T3-F442A cells. Biochem Biophys Res Commun 180: 716–723PubMedGoogle Scholar
  129. 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: 43221–43230PubMedGoogle Scholar
  130. Yang C, Maiguel DA, Carrier F (2002), Identification of nucleolin and nucleophosmin as genotoxic stress-responsive RNA-binding proteins. Nucleic Acids Res 30: 2251–2260PubMedGoogle Scholar
  131. 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: 6068–6074PubMedGoogle Scholar

Copyright information

© Springer 2007

Authors and Affiliations

  • Sébastien Storck
    • Manu Shukla
      • 1
      • 3
    • Stefan Dimitrov
      • 1
      • 3
    • Philippe Bouvet
      • 1
      • 2
    1. 1.Laboratoire Joliot-Curie, Ecole Normale Supérieure de Lyon46 Allée d’ItalieFrance
    2. 2.Laboratoire de Biologie Moléculaire de la Cellule, CNRS-UMR 5161/INRA 1237/IFR128 Biosciences Lyon-Gerland Ecole Normale Supérieure de Lyon46 Allée d’ItalieFrance
    3. 3.Institut Albert Bonniot, INSERM U30938706 La Tronche cedexFrance

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