Intrinsically disordered regions of nucleophosmin/B23 regulate its RNA binding activity through their inter-and intra-molecular association

Nucleic Acids Research

Volumn 42, Issue 2, 2014, Pages 1180-1195

  Hisaoka, Miharu ^a   Nagata, Kyosuke ^a   Okuwaki, Mitsuru ^a  

^a UNIVERSITY OF TSUKUBA   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN B; CYCLIN DEPENDENT KINASE 1; DNA; DNA FRAGMENT; FLUORESCENT DYE; NUCLEOPHOSMIN; RECOMBINANT PROTEIN; RNA;

ARTICLE; BINDING AFFINITY; BIOGENESIS; CARBOXY TERMINAL SEQUENCE; CELLULAR DISTRIBUTION; CIRCULAR DICHROISM; CROSS LINKING; DNA BINDING; GENE MUTATION; HUMAN; HYDROPHOBICITY; IMMUNOPRECIPITATION; MOLECULAR RECOGNITION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN PURIFICATION; RNA BINDING; RNA SPLICING; ZINC FINGER MOTIF;

CELL LINE; HELA CELLS; HUMANS; INTRINSICALLY DISORDERED PROTEINS; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN ISOFORMS; PROTEIN STRUCTURE, TERTIARY; RNA; RNA-BINDING PROTEINS;

EID: 84893286454     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt897     Document Type: Article

References (52)

1. Tompa, P. (2002) Intrinsically unstructured proteins. Trends Biochem. Sci., 27, 527-533.
2. Wells, M., Tidow, H., Rutherford, T.J., Markwick, P., Jensen, M.R., Mylonas, E., Svergun, D.I., Blackledge, M. and Fersht, A.R. (2008) Structure of tumor suppressor p53 and its intrinsically disordered N-terminal transactivation domain. Proc. Natl Acad. Sci. USA, 105, 5762-5767.
3. Guo, X., Bulyk, M.L. and Hartemink, A.J. (2012) Intrinsic disorder within and flanking the DNA-binding domains of human transcription factors. Biocomputing, 104-115.
4. Dunker, A.K., Brown, C.J., Lawson, J.D., Iakoucheva, L.M. and Obradovic, Z. (2002) Intrinsic disorder and protein function. Biochemistry, 41, 6573-6582.
5. Murano, K., Okuwaki, M., Hisaoka, M. and Nagata, K. (2008) Transcription regulation of the rRNA gene by a multifunctional nucleolar protein, B23/nucleophosmin, through its histone chaperone activity. Mol. Cell. Biol., 28, 3114-3126.
6. Savkur, R.S. and Olson, M.O. (1998) Preferential cleavage in pre-ribosomal RNA byprotein B23 endoribonuclease. Nucleic Acids Res., 26, 4508-4515.
7. Maggi, L.B. Jr, Kuchenruether, M., Dadey, D.Y., Schwope, R.M., Grisendi, S., Townsend, R.R., Pandolfi, P.P. and Weber, J.D. (2008) Nucleophosmin serves as a rate-limiting nuclear export chaperone for the Mammalian ribosome. Mol. Cell. Biol., 28, 7050-7065.
8. Wang, W., Budhu, A., Forgues, M. and Wang, X.W. (2005) Temporal and spatial control of nucleophosmin by the Ran-Crm1 complex in centrosome duplication. Nat. Cell Biol., 7, 823-830.
9. Grisendi, S., Bernardi, R., Rossi, M., Cheng, K., Khandker, L., Manova, K. and Pandolfi, P.P. (2005) Role of nucleophosmin in embryonic development and tumorigenesis. Nature, 437, 147-153.
10. Grisendi, S., Mecucci, C., Falini, B. and Pandolfi, P.P. (2006) Nucleophosmin and cancer. Nat. Rev. Cancer, 6, 493-505.
11. Falini, B., Mecucci, C., Tiacci, E., Alcalay, M., Rosati, R., Pasqualucci, L., La Starza, R., Diverio, D., Colombo, E., Santucci, A. et al. (2005) Cytoplasmic nucleophosmin in acute myelogenous leukemia with a normal karyotype. N. Engl. J. Med., 352, 254-266.
12. Tanaka, M., Sasaki, H., Kino, I., Sugimura, T. and Terada, M. (1992) Genes preferentially expressed in embryo stomach are predominantly expressed in gastric cancer. Cancer Res., 52, 3372-3377.
13. Nozawa, Y., Van Belzen, N., Van der Made, A.C., Dinjens, W.N. and Bosman, F.T. (1996) Expression of nucleophosmin/B23 in normal and neoplastic colorectal mucosa. J. Pathol., 178, 48-52.
14. Shields, L.B., Gercel-Taylor, C., Yashar, C.M., Wan, T.C., Katsanis, W.A., Spinnato, J.A. and Taylor, D.D. (1997) Induction of immune responses to ovarian tumor antigens by multiparity. J. Soc. Gynecol. Investig., 4, 298-304.
15. Subong, E.N., Shue, M.J., Epstein, J.I., Briggman, J.V., Chan, P.K. and Partin, A.W. (1999) Monoclonal antibody to prostate cancer nuclear matrix protein (PRO:4-216) recognizes nucleophosmin/B23. Prostate, 39, 298-304.
16. Tsui, K.H., Cheng, A.J., Chang, P.L., Pan, T.L. and Yung, B.Y. (2004) Association of nucleophosmin/B23 mRNA expression with clinical outcome in patients with bladder carcinoma. Urology, 64, 839-844.
17. Skaar, T.C., Prasad, S.C., Sharareh, S., Lippman, M.E., Brunner, N. and Clarke, R. (1998) Two-dimensional gel electrophoresis analyses identify nucleophosmin as an estrogen regulated protein associated with acquired estrogen-independence in human breast cancer cells. J. Steroid Biochem. Mol. Biol., 67, 391-402.
18. Okuwaki, M., Iwamatsu, A., Tsujimoto, M. and Nagata, K. (2001) Identification of nucleophosmin/B23, an acidic nucleolar protein, as a stimulatory factor for in vitro replication of adenovirus DNA complexed with viral basic core proteins. J. Mol. Biol., 311, 41-55.
19. Strausberg, R.L., Feingold, E.A., Grouse, L.H., Derge, J.G., Klausner, R.D., Collins, F.S., Wagner, L., Shenmen, C.M., Schuler, G.D., Altschul, S.F. et al. (2002) Generation and initial analysis of more than 15, 000 full-length human and mouse cDNA sequences. Proc. Natl Acad. Sci. USA, 99, 16899-16903.
20. Namboodiri, V.M., Akey, I.V., Schmidt-Zachmann, M.S., Head, J.F. and Akey, C.W. (2004) The structure and function of Xenopus NO38-core, a histone chaperone in the nucleolus. Structure, 12, 2149-2160.
21. Grummitt, C.G., Townsley, F.M., Johnson, C.M., Warren, A.J. and Bycroft, M. (2008) Structural consequences of nucleophosmin mutations in acute myeloid leukemia. J. Biol. Chem., 283, 23326-23332.
22. Wang, D., Baumann, A., Szebeni, A. and Olson, M.O. (1994) The nucleic acid binding activity of nucleolar protein B23.1 resides in its carboxyl-terminal end. J. Biol. Chem., 269, 30994-30998.
23. Federici, L., Arcovito, A., Scaglione, G.L., Scaloni, F., Lo Sterzo, C., Di Matteo, A., Falini, B., Giardina, B. and Brunori, M. (2010) Nucleophosmin C-terminal leukemia-associated domain interacts with G-rich quadruplex forming DNA. J. Biol. Chem., 285, 37138-37149.
24. Gallo, A., Lo Sterzo, C., Mori, M., Di Matteo, A., Bertini, I., Banci, L., Brunori, M. and Federici, L. (2012) Structure of nucleophosmin DNA-binding domain and analysis of its complex with a G-quadruplex sequence from the c-MYC promoter. J. Biol. Chem., 287, 26539-26548.
25. Marasco, D., Ruggiero, A., Vascotto, C., Poletto, M., Scognamiglio, P.L., Tell, G. and Vitagliano, L. (2012) Role of mutual interactions in the chemical and thermal stability of nucleophosmin NPM1 domains. Biochem. Biophys. Res. Commun., 430, 523-528.
26. Okuwaki, M., Tsujimoto, M. and Nagata, K. (2002) The RNA binding activity of a ribosome biogenesis factor, nucleophosmin/B23, is modulated by phosphorylation with a cell cycle-dependent kinase and by association with its subtype. Mol. Biol. Cell, 13, 2016-2030.
27. Okuwaki, M., Matsumoto, K., Tsujimoto, M. and Nagata, K. (2001) Function of nucleophosmin/B23, a nucleolar acidic protein, as a histone chaperone. FEBS Lett., 506, 272-276.
28. Hisaoka, M., Ueshima, S., Murano, K., Nagata, K. and Okuwaki, M. (2010) Regulation of nucleolar chromatin by B23/nucleophosmin jointly depends upon its RNA binding activity and transcription factor UBF. Mol. Cell. Biol., 30, 4952-4964.
29. Kinoshita, E., Kinoshita-Kikuta, E., Takiyama, K. and Koike, T. (2006) Phosphate-binding tag, a new tool to visualize phosphorylated proteins. Mol. Cell. Proteomics, 5, 749-757.
30. Okuwaki, M., Sumi, A., Hisaoka, M., Saotome-Nakamura, A., Akashi, S., Nishimura, Y. and Nagata, K. (2012) Function of homo-and hetero-oligomers of human nucleoplasmin/nucleophosmin family proteins NPM1, NPM2 and NPM3 during sperm chromatin remodeling. Nucleic Acids Res., 40, 4861-4878.
31. Hirose, S., Shimizu, K. and Noguchi, T. (2010) POODLE-I: disordered region prediction by integrating POODLE series and structural information predictors based on a workflow approach. In Silico Biol., 10, 185-191.
32. Lee, H.H., Kim, H.S., Kang, J.Y., Lee, B.I., Ha, J.Y., Yoon, H.J., Lim, S.O., Jung, G. and Suh, S.W. (2007) Crystal structure of human nucleophosmin-core reveals plasticity of the pentamerpentamer interface. Proteins, 69, 672-678.
33. Griffin, B.A., Adams, S.R. and Tsien, R.Y. (1998) Specific covalent labeling of recombinant protein molecules inside live cells. Science, 281, 269-272.
34. Luedtke, N.W., Dexter, R.J., Fried, D.B. and Schepartz, A. (2007) Surveying polypeptide and protein domain conformation and association with FlAsH and ReAsH. Nat. Chem. Biol., 3, 779-784.
35. Adams, S.R., Campbell, R.E., Gross, L.A., Martin, B.R., Walkup, G.K., Yao, Y., Llopis, J. and Tsien, R.Y. (2002) New biarsenical ligands and tetracysteine motifs for protein labeling in vitro and in vivo: synthesis and biological applications. J. Am. Chem. Soc., 124, 6063-6076.
36. Allan, J., Hartman, P.G., Crane-Robinson, C. and Aviles, F.X. (1980) The structure of histone H1 and its location in chromatin. Nature, 288, 675-679.
37. Simpson, R.T. (1978) Structure of the chromatosome, a chromatin particle containing 160 base pairs of DNA and all the histones. Biochemistry, 17, 5524-5531.
38. Lever, M.A., Th'ng, J.P., Sun, X. and Hendzel, M.J. (2000) Rapid exchange of histone H1.1 on chromatin in living human cells. Nature, 408, 873-876.
39. Chiarella, S., De Cola, A., Scaglione, G.L., Carletti, E., Graziano, V., Barcaroli, D., Lo Sterzo, C., Di Matteo, A., Di Ilio, C., Falini, B. et al. (2013) Nucleophosmin mutations alter its nucleolar localization by impairing G-quadruplex binding at ribosomal DNA. Nucleic Acids Res., 41, 3228-3239.
40. Pene, J.J., Knight, E. Jr and Darnell, J.E. Jr (1968) Characterization of a new low molecular weight RNA in HeLa cell ribosomes. J. Mol. Biol., 33, 609-623.
41. Pace, N.R., Walker, T.A. and Schroeder, E. (1977) Structure of the 5.8S RNA component of the 5.8S-28S ribosomal RNA junction complex. Biochemistry, 16, 5321-5328.
42. Peter, M., Nakagawa, J., Doree, M., Labbe, J.C. and Nigg, E.A. (1990) Identification of major nucleolar proteins as candidate mitotic substrates of cdc2 kinase. Cell, 60, 791-801.
43. Chan, P.K., Aldrich, M., Cook, R.G. and Busch, H. (1986) Amino acid sequence of protein B23 phosphorylation site. J. Biol. Chem., 261, 1868-1872.
44. Krause, A. and Hoffmann, I. (2010) Polo-like kinase 2-dependent phosphorylation of NPM/B23 on serine 4 triggers centriole duplication. PLoS One, 5, e9849.
45. Kang, Y.J., Olson, M.O., Jones, C. and Busch, H. (1975) Nucleolar phosphoproteins of normal rat liver and Novikoff hepatoma ascites cells. Cancer Res., 35, 1470-1475.
46. Shandilya, J., Swaminathan, V., Gadad, S.S., Choudhari, R., Kodaganur, G.S. and Kundu, T.K. (2009) Acetylated NPM1 localizes in the nucleoplasm and regulates transcriptional activation of genes implicated in oral cancer manifestation. Mol. Cell. Biol., 29, 5115-5127.
47. Liu, X., Liu, Z., Jang, S.W., Ma, Z., Shinmura, K., Kang, S., Dong, S., Chen, J., Fukasawa, K. and Ye, K. (2007) Sumoylation of nucleophosmin/B23 regulates its subcellular localization, mediating cell proliferation and survival. Proc. Natl Acad. Sci. USA, 104, 9679-9684.
48. Negi, S.S. and Olson, M.O. (2006) Effects of interphase and mitotic phosphorylation on the mobility and location of nucleolar protein B23. J. Cell Sci., 119, 3676-3685.
49. Itahana, K., Bhat, K.P., Jin, A., Itahana, Y., Hawke, D., Kobayashi, R. and Zhang, Y. (2003) Tumor suppressor ARF degrades B23, a nucleolar protein involved in ribosome biogenesis and cell proliferation. Mol. Cell, 12, 1151-1164.
50. Gadad, S.S., Senapati, P., Syed, S.H., Rajan, R.E., Shandilya, J., Swaminathan, V., Chatterjee, S., Colombo, E., Dimitrov, S., Pelicci, P.G. et al. (2011) The multifunctional protein nucleophosmin (NPM1) is a human linker histone H1 chaperone. Biochemistry, 50, 2780-2789.
51. Lambert, B. and Buckle, M. (2006) Characterisation of the interface between nucleophosmin (NPM) and p53: potential role in p53 stabilisation. FEBS Lett., 580, 345-350.
52. Colombo, E., Marine, J.C., Danovi, D., Falini, B. and Pelicci, P.G. (2002) Nucleophosmin regulates the stability and transcriptional activity of p53. Nat. Cell Biol., 4, 529-533.