Nucleolar localization/retention signal is responsible for transient accumulation of histone H2B in the nucleolus through electrostatic interactions

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1813, Issue 1, 2011, Pages 27-38

  Musinova, Yana R ^a   Lisitsyna, Olga M ^a   Golyshev, Sergey A ^a   Tuzhikov, Alexander I ^a   Polyakov, Vladimir Y ^a   Sheval, Eugene V ^a  

^a MOSCOW STATE UNIVERSITY   (Russian Federation)

Author keywords

Electrostatic interaction; Histone H2B; Nucleolar localization retention signal; Nucleolus

Indexed keywords

DEOXYRIBONUCLEASE I; HISTONE H2B; HYBRID PROTEIN;

ARTICLE; BINDING SITE; CELL NUCLEUS MATRIX; CHROMATIN; ELECTRON MICROSCOPY; GENETIC TRANSFECTION; HELA CELL; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNOCYTOCHEMISTRY; INTERPHASE; NUCLEOLAR LOCALIZATION SIGNAL; PLASMID; PRIORITY JOURNAL; PROTEIN INTERACTION; STATIC ELECTRICITY; WESTERN BLOTTING;

BLOTTING, WESTERN; CELL NUCLEOLUS; CELL NUCLEUS; CHROMATIN; GREEN FLUORESCENT PROTEINS; HELA CELLS; HISTONES; HUMANS; IMMUNOENZYME TECHNIQUES; LYSINE; NUCLEAR LOCALIZATION SIGNALS; NUCLEAR MATRIX; PROTEIN BINDING; RECOMBINANT FUSION PROTEINS; STATIC ELECTRICITY;

EID: 78650065353     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2010.11.003     Document Type: Article

References (54)

1. Kaiser T.E., Intine R.V., Dundr M. De novo formation of a subnuclear body. Science 2008, 322:1713-1717.
2. Misteli T. Cell biology: nuclear order out of chaos. Nature 2008, 456:333-334.
3. Matera A.G., Izaguire-Sierra M., Praveen K., Rajendra T.K. Nuclear bodies: random aggregates of sticky proteins or crucibles of macromolecular assembly?. Dev. Cell 2009, 17:639-647.
4. Volkova E.G., Kurchashova S.Y., Polyakov V.Y., Sheval E.V. Self-organization of cellular structures induced by the overexpression of nuclear envelope proteins: a correlative light and electron microscopy study. J. Electron Microsc. (Tokyo) 2010, 10.1093/jmicro/dfq067.
5. Misteli T. Physiological importance of RNA and protein mobility in the cell nucleus. Histochem. Cell Biol. 2008, 129:5-11.
6. Seksek O., Biwersi J., Verkman A.S. Translational diffusion of macromolecule-sized solutes in cytoplasm and nucleus. J. Cell Biol. 1997, 138:131-142.
7. Görisch S.M., Lichter P., Rippe K. Mobility of multi-subunit complexes in the nucleus: accessibility and dynamics of chromatin subcompartments. Histochem. Cell Biol. 2005, 123:217-228.
8. Pack C., Saito K., Tamura M., Kinjo M. Microenvironment and effect of energy depletion in the nucleus analyzed by mobility of multiple oligomeric EGFPs. Biophys. J. 2006, 91:3921-3936.
9. Bancaud A., Huet S., Daigle N., Mozziconacci J., Beaudouin J., Ellenberg J. Molecular crowding affects diffusion and binding of nuclear proteins in heterochromatin and reveals the fractal organization of chromatin. EMBO J. 2009, 28:3785-3798.
10. Phair R.D., Misteli T. High mobility of proteins in the mammalian cell nucleus. Nature 2000, 404:604-609.
11. Chen D., Huang S. Nucleolar components involved in ribosome biogenesis cycle between the nucleolus and nucleoplasm in interphase cells. J. Cell Biol. 2001, 153:169-176.
12. Verkman A.S. Solute and macromolecule diffusion in cellular aqueous compartments. Trends Biochem. Sci. 2002, 27:27-33.
13. Phair R.D., Scaffidi P., Elbi C., Vecerová J., Dey A., Ozato K., Brown D.T., Hager G., Bustin M., Misteli T. Global nature of dynamic protein-chromatin interactions in vivo: three-dimensional genome scanning and dynamic interaction networks of chromatin proteins. Mol. Cell. Biol. 2004, 24:6393-6402.
14. Beaudouin J., Mora-Bermúdez F., Klee T., Daigle N., Ellenberg J. Dissecting the contribution of diffusion and interactions to the mobility of nuclear proteins. Biophys. J. 2006, 90:1878-1894.
15. Kimura H., Cook P.R. Kinetics of core histones in living human cells: little exchange of H3 and H4 and some rapid exchange of H2B. J. Cell Biol. 2001, 153:1341-1353.
16. Speil J., Kubitscheck U. Single ovalbumin molecules exploring nucleoplasm and nucleoli of living cell nuclei. Biochim. Biophys. Acta 2010, 1803:396-404.
17. Stoldt S., Wenzel D., Schulze E., Doenecke D., Happel N. G1 phase-dependent nucleolar accumulation of human histone H1x. Biol. Cell 2007, 99:541-552.
18. Takata H., Matsunaga S., Morimoto A., Ono-Maniwa R., Uchiyama S., Fukui K. H1.X with different properties from other linker histones is required for mitotic progression. FEBS Lett. 2007, 581:3783-3788.
19. Gutiyama L.M., da Cunha J.P., Schenkman S. Histone H1 of Trypanosoma cruzi is concentrated in the nucleolus region and disperses upon phosphorylation during progression to mitosis. Eukaryot. Cell 2008, 7:560-568.
20. Kanda T., Sullivan K.F., Wahl G.M. Histone-GFP fusion protein enables sensitive analysis of chromosome dynamics in living mammalian cells. Curr. Biol. 1998, 8:377-385.
21. Sheval E.V., Polyakov V.Y. Visualization of the chromosome scaffold and intermediates of loop domain compaction in extracted mitotic cells. Cell Biol. Int. 2006, 30:1028-1040.
22. Grygoryev A.A., Bulycheva T.I., Sheval E.V., Kalinina I.A., Zatsepina O.V. Cytological indicators of overall suppression of protein synthesis revealed by staining with a new monoclonal antibody. Cell Tissue Biol. 2008, 2:191-199.
23. Rabut G., Ellenberg J. Automatic real-time three-dimensional cell tracking by fluorescence microscopy. J. Microsc. 2004, 216:131-137.
24. Singh R.K., Paik J., Gunjan A. Generation and management of excess histones during the cell cycle. Front. Biosci. 2009, 14:3145-3158.
25. Hernandez-Verdun D. The nucleolus: a model for the organization of nuclear functions. Histochem. Cell Biol. 2006, 126:135-148.
26. Ahmad Y., Boisvert F.M., Gregor P., Cobley A., Lamond A.I. NOPdb: Nucleolar Proteome Database-2008 update. Nucleic Acids Res. 2009, 37:D181-D184.
27. Sheval E.V., Polzikov M.A., Olson M.O.J., Zatsepina O.V. A higher concentration of an antigen within the nucleolus may prevent its proper recognition by specific antibodies. Eur. J. Histochem. 2005, 49:117-124.
28. Feuerstein N., Chan P.K., Mond J.J. Identification of numatrin, the nuclear matrix protein associated with induction of mitogenesis, as the nucleolar protein B23. Implication for the role of the nucleolus in early transduction of mitogenic signals. J. Biol. Chem. 1988, 263:10608-10612.
29. Sheval E.V., Dudnik O.A., Abramchuk S.S., Polyakov V.Y. Perichromosomal layer proteins associate with chromosome scaffold and nuclear matrix throughout the cell cycle. Biochemistry (Mosc.) 2009, 3:168-183.
30. Zatsepina O.V., Dudnic O.A., Todorov I.T., Thiry M., Spring H., Trendelenburg M.F. Experimental induction of prenucleolar bodies (PNBs) in interphase cells: interphase PNBs show similar characteristics as those typically observed at telophase of mitosis in untreated cells. Chromosoma 1997, 105:418-430.
31. Negi S.S., Olson M.O. Effects of interphase and mitotic phosphorylation on the mobility and location of nucleolar protein B23. J. Cell Sci. 2006, 119:3676-3685.
32. Muro E., Hoang T.Q., Jobart-Malfait A., Hernandez-Verdun D. In nucleoli, the steady state of nucleolar proteins is leptomycin B-sensitive. Biol. Cell 2008, 100:303-313.
33. Emmott E., Hiscox J.A. Nucleolar targeting: the hub of the matter. EMBO Rep. 2009, 10:231-238.
34. Weber J.D., Kuo M.L., Bothner B., Digiammarino E.L., Kriwacki R.W., Roussel M.F., Sherr C.J. Cooperative signals governing ARF-MDM2 interaction and nucleolar localization of the complex. Mol. Cell. Biol. 2000, 20:2517-2528.
35. Kubota S., Copeland T.D., Pomerantz R.J. Nuclear and nucleolar targeting of human ribosomal protein S25: common features shared with HIV-1 regulatory proteins. Oncogene 1999, 18:1503-1514.
36. Rowland R.R., Yoo D. Nucleolar-cytoplasmic shuttling of PRRSV nucleocapsid protein: a simple case of molecular mimicry or the complex regulation by nuclear import, nucleolar localization and nuclear export signal sequences. Virus Res. 2003, 95:23-33.
37. Zemach A., Li Y., Ben-Meir H., Oliva M., Mosquna A., Kiss V., Avivi Y., Ohad N., Grafi G. Different domains control the localization and mobility of like heterochromatin protein1 in Arabidopsis nuclei. Plant Cell 2006, 18:133-145.
38. Melén K., Kinnunen L., Fagerlund R., Ikonen N., Twu K.Y., Krug R.M., Julkunen I. Nuclear and nucleolar targeting of influenza A virus NS1 protein: striking differences between different virus subtypes. J. Virol. 2007, 81:5995-6006.
39. Wang Y., Chen B., Li Y., Zhou D., Chen S. PNRC accumulates in the nucleolus by interaction with B23/nucleophosmin via its nucleolar localization sequence. Biochim. Biophys. Acta 2010, 10.1016/j.bbamcr.2010.09.017.
40. Cokol M., Nair R., Rost B. Finding nuclear localization signals. EMBO Rep. 2000, 1:411-415.
41. Scott M.S., Boisvert F.-M., McDowall M.D., Lamond A.I., Barton G.J. Characterization and prediction of protein nucleolar localization sequences. Nucleic Acids Res. 2010, 10.1093/nar/gkq653.
42. Sheval E.V., Polyakov V.Y. Immunocytochemical study of PCNA distribution in nuclei with stabilized and non-stabilized nuclear matrix. Biol. Membr. 2002, 19:237-242. (in Russian).
43. Lange A., Mills R.E., Lange C.J., Stewart M., Devine S.E., Corbett A.H. Classical nuclear localization signals: definition, function, and interaction with importin alpha. J. Biol. Chem. 2007, 282:5101-5105.
44. Conti E., Kuriyan J. Crystallographic analysis of the specific yet versatile recognition of distinct nuclear localization signals by karyopherin alpha. Structure 2000, 8:329-338.
45. Fontes M.R., Teh T., Kobe B. Structural basis of recognition of monopartite and bipartite nuclear localization sequences by mammalian importin-alpha. J. Mol. Biol. 2000, 297:1183-1194.
46. Hodel M.R., Corbett A.H., Hodel A.E. Dissection of a nuclear localization signal. J. Biol. Chem. 2001, 276:1317-1325.
47. Reed M.L., Dove B.K., Jackson R.M., Collins R., Brooks G., Hiscox J.A. Delineation and modelling of a nucleolar retention signal in the coronavirus nucleocapsid protein. Traffic 2006, 7:833-848.
48. Favre D., Studer E., Michel M. Two nucleolar targeting signals present in the N-terminal part of Semliki Forest virus capsid protein. Arch. Virol. 1994, 137:149-155.
49. Shu-Nu C., Lin C.H., Lin A. An acidic amino acid cluster regulates the nucleolar localization and ribosome assembly of human ribosomal protein L22. FEBS Lett. 2000, 484:22-28.
50. Carmo-Fonseca M., Mendes-Soares L., Campos I. To be or not to be in the nucleolus. Nat. Cell Biol. 2000, 2:107-112.
51. Houmani J.L., Ruf I.K. Clusters of basic amino acids contribute to RNA binding and nucleolar localization of ribosomal protein L22. PLoS ONE 2009, 4:5306.
52. Lechertier T., Sirri V., Hernandez-Verdun D., Roussel P. A B23-interacting sequence as a tool to visualize protein interactions in a cellular context. J. Cell Sci. 2007, 120:265-275.
53. Endo A., Kitamura N., Komada M. Nucleophosmin/B23 regulates ubiquitin dynamics in nucleoli by recruiting deubiquitylating enzyme USP36. J. Biol. Chem. 2009, 284:27918-27923.
54. Schmidt-Zachmann M.S., Nigg E.A. Protein localization to the nucleolus: a search for targeting domains in nucleolin. J. Cell Sci. 1993, 105:799-806.