Characterization and prediction of protein nucleolar localization sequences

Nucleic Acids Research

Volumn 38, Issue 21, 2010, Pages 7388-7399

  Scott, Michelle S ^a   Boisvert, François Michel ^a   McDowall, Mark D ^a   Lamond, Angus I ^a   Barton, Geoffrey J ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHOPROTEIN PHOSPHATASE 1;

ALPHA HELIX; AMINO ACID SEQUENCE; ARTICLE; ARTIFICIAL NEURAL NETWORK; CELL CULTURE; CONTROLLED STUDY; CYTOPLASM; FALSE POSITIVE RESULT; HUMAN; HUMAN CELL; MOLECULAR CLONING; NUCLEAR LOCALIZATION SIGNAL; NUCLEOLUS; NUCLEOTIDE SEQUENCE; PREDICTION; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN SECONDARY STRUCTURE; RECEIVER OPERATING CHARACTERISTIC; VALIDATION STUDY;

CELL LINE, TUMOR; CELL NUCLEOLUS; COMPUTATIONAL BIOLOGY; HUMANS; NEURAL NETWORKS (COMPUTER); NUCLEAR LOCALIZATION SIGNALS; NUCLEAR PROTEINS; PROTEIN SORTING SIGNALS; VIRAL PROTEINS;

EID: 78649820071     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkq653     Document Type: Article

References (58)

1. Scheer, U. and Hock, R. (1999) Structure and function of the nucleolus. Curr. Opin. Cell Biol., 11, 385-390.
2. Boisvert, F. M., van Koningsbruggen, S., Navascues, J. and Lamond, A. I. (2007) The multifunctional nucleolus. Nat. Rev. Mol. Cell Biol., 8, 574-585.
3. Olson, M. O., Dundr, M. and Szebeni, A. (2000) The nucleolus: an old factory with unexpected capabilities. Trends Cell Biol., 10, 189-196.
4. Olson, M. O., Hingorani, K. and Szebeni, A. (2002) Conventional and nonconventional roles of the nucleolus. Int. Rev. Cytol., 219, 199-266.
5. Pederson, T. (1998) The plurifunctional nucleolus. Nucleic Acids Res., 26, 3871-3876.
6. Pederson, T. and Tsai, R. Y. (2009) In search of nonribosomal nucleolar protein function and regulation. J. Cell Biol., 184, 771-776.
7. Pederson, T. (1998) Growth factors in the nucleolus? J. Cell Biol., 143, 279-281.
8. Ahmad, Y., Boisvert, F. M., Gregor, P., Cobley, A. and Lamond, A. I. (2009) NOPdb: Nucleolar Proteome Database-2008 update. Nucleic Acids Res., 37, D181-184.
9. Andersen, J. S., Lam, Y. W., Leung, A. K., Ong, S. E., Lyon, C. E., Lamond, A. I. and Mann, M. (2005) Nucleolar proteome dynamics. Nature, 433, 77-83.
10. Boisvert, F. M., Lam, Y. W., Lamont, D. and Lamont, A. I. (2010) A quantitative proteomic analysis of subcellular proteome localization and changes induced by DNA damage. Mol. Cell Proteomics, 9, 457-470.
11. Emmott, E. and Hiscox, J. A. (2009) Nucleolar targeting: the hub of the matter. EMBO Rep., 10, 231-238.
12. Boulikas, T. (1993) Nuclear localization signals (NLS). Crit. Rev. Eukaryot. Gene Expr., 3, 193-227.
13. Von Heijne, G. (1990) The signal peptide. J. Membr. Biol., 115, 195-201.
14. Gavel, Y., Nilsson, L. and von Heijne, G. (1988) Mitochondrial targeting sequences. Why 'non-amphiphilic' peptides may still be amphiphilic. FEBS Lett., 235, 173-177.
15. Gould, S. J., Keller, G. A., Hosken, N., Wilkinson, J. and Subramani, S. (1989) A conserved tripeptide sorts proteins to peroxisomes. J. Cell Biol., 108, 1657-1664.
16. Carmo-Fonseca, M., Mendes-Soares, L. and Campos, I. (2000) To be or not to be in the nucleolus. Nat. Cell Biol., 2, E107-E112.
17. Nair, R., Carter, P. and Rost, B. (2003) NLSdb: database of nuclear localization signals. Nucleic Acids Res., 31, 397-399.
18. The Universal Protein Resource. (2010) (UniProt) in 2010. Nucleic Acids Res., 38, D142-D148.
19. Hobohm, U., Scharf, M., Schneider, R. and Sander, C. (1992) Selection of representative protein data sets. Protein Sci., 1, 409-417.
20. Nielsen, H., Engelbrecht, J., von Heijne, G. and Brunak, S. (1996) Defining a similarity threshold for a functional protein sequence pattern: the signal peptide cleavage site. Proteins, 24, 165-177.
21. Pearson, W. R. and Lipman, D. J. (1988) Improved tools for biological sequence comparison. Proc. Natl Acad. Sci. USA, 85, 2444-2448.
22. Sigrist, C. J., Cerutti, L., de Castro, E., Langendijk-Genevaux, P. S., Bulliard, V., Bairoch, A. and Hulo, N. (2010) PROSITE, a protein domain database for functional characterization and annotation. Nucleic Acids Res., 38, D161-D166.
23. Kersey, P. J., Duarte, J., Williams, A., Karavidopoulou, Y., Birney, E. and Apweiler, R. (2004) The International Protein Index: an integrated database for proteomics experiments. Proteomics, 4, 1985-1988.
24. Cole, C., Barber, J. D. and Barton, G. J. (2008) The Jpred 3 secondary structure prediction server. Nucleic Acids Res., 36, W197-W201.
25. Huang da, W., Sherman, B. T. and Lempicki, R. A. (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc., 4, 44-57.
26. Cokol, M., Nair, R. and Rost, B. (2000) Finding nuclear localization signals. EMBO Rep., 1, 411-415.
27. Rubtsov, Y. P., Zolotukhin, A. S., Vorobjev, I. A., Chichkova, N. V., Pavlov, N. A., Karger, E. M., Evstafieva, A. G., Felber, B. K. and Vartapetian, A. B. (1997) Mutational analysis of human prothymosin alpha reveals a bipartite nuclear localization signal. FEBS Lett., 413, 135-141.
28. Valdez, B. C., Perlaky, L., Henning, D., Saijo, Y., Chan, P. K. and Busch, H. (1994) Identification of the nuclear and nucleolar localization signals of the protein p120. Interaction with translocation protein B23. J. Biol. Chem., 269, 23776-23783.
29. Liu, J., Du, X. and Ke, Y. (2006) Mapping nucleolar localization sequences of 1A6/DRIM. FEBS Lett., 580, 1405-1410.
30. Huang, H. S., Pozarowski, P., Gao, Y., Darzynkiewicz, Z. and Lee, E. Y. (2005) Protein phosphatase-1 inhibitor-3 is co-localized to the nucleoli and centrosomes with PP1gamma1 and PP1alpha, respectively. Arch. Biochem. Biophys., 443, 33-44.
31. Baldi, P. and Brunak, S. (2001) Bioinformatics: The Machine Learning Approach, 2nd edn. MIT Press, Cambridge, MA.
32. Nielsen, H., Engelbrecht, J., Brunak, S. and von Heijne, G. (1997) Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng., 10, 1-6.
33. Prieve, M. G., Guttridge, K. L., Munguia, J. and Waterman, M. L. (1998) Differential importin-alpha recognition and nuclear transport by nuclear localization signals within the high-mobility-group DNA binding domains of lymphoid enhancer factor 1 and T-cell factor 1. Mol. Cell Biol., 18, 4819-4832.
34. Hiscox, J. A. (2007) RNA viruses: hijacking the dynamic nucleolus. Nat. Rev. Microbiol., 5, 119-127.
35. Endo, A., Kitamura, N. and Komada, M. (2009) Nucleophosmin/ B23 regulates ubiquitin dynamics in nucleoli by recruiting deubiquitylating enzyme USP36. J. Biol. Chem., 284, 27918-27923.
36. Dang, C. V. and Lee, W. M. (1989) Nuclear and nucleolar targeting sequences of c-erb-A, c-myb, N-myc, p53, HSP70, and HIV tat proteins. J. Biol. Chem., 264, 18019-18023.
37. Henderson, J. E., Amizuka, N., Warshawsky, H., Biasotto, D., Lanske, B. M., Goltzman, D. and Karaplis, A. C. (1995) Nucleolar localization of parathyroid hormone-related peptide enhances survival of chondrocytes under conditions that promote apoptotic cell death. Mol. Cell Biol., 15, 4064-4075.
38. Stegh, A. H., Schickling, O., Ehret, A., Scaffidi, C., Peterhansel, C., Hofmann, T. G., Grummt, I., Krammer, P. H. and Peter, M. E. (1998) DEDD, a novel death effector domain-containing protein, targeted to the nucleolus. Embo J., 17, 5974-5986.
39. Caron, E., Cote, C., Parisien, M., Major, F. and Perreault, C. (2006) Identification of two distinct intracellular localization signals in STT3-B. Arch. Biochem. Biophys., 445, 108-114.
40. Stark, L. A. and Dunlop, M. G. (2005) Nucleolar sequestration of RelA (p65) regulates NF-kappaB-driven transcription and apoptosis. Mol. Cell Biol., 25, 5985-6004.
41. Antoine, M., Reimers, K., Dickson, C. and Kiefer, P. (1997) Fibroblast growth factor 3, a protein with dual subcellular localization, is targeted to the nucleus and nucleolus by the concerted action of two nuclear localization signals and a nucleolar retention signal. J. Biol. Chem., 272, 29475-29481.
42. Goyal, P., Pandey, D. and Siess, W. (2006) Phosphorylation-dependent regulation of unique nuclear and nucleolar localization signals of LIM kinase 2 in endothelial cells. J. Biol. Chem., 281, 25223-25230.
43. Siomi, H., Shida, H., Maki, M. and Hatanaka, M. (1990) Effects of a highly basic region of human immunodeficiency virus Tat protein on nucleolar localization. J. Virol., 64, 1803-1807.
44. Bohnlein, E., Berger, J. and Hauber, J. (1991) Functional mapping of the human immunodeficiency virus type 1 Rev RNA binding domain: new insights into the domain structure of Rev and Rex. J. Virol., 65, 7051-7055.
45. Nosaka, T., Siomi, H., Adachi, Y., Ishibashi, M., Kubota, S., Maki, M. and Hatanaka, M. (1989) Nucleolar targeting signal of human T-cell leukemia virus type I rex-encoded protein is essential for cytoplasmic accumulation of unspliced viral mRNA. Proc. Natl Acad. Sci. USA, 86, 9798-9802.
46. Melen, K., Kinnunen, L., Fagerlund, R., Ikonen, N., Twu, K. Y., Krug, R. M. and Julkunen, I. (2007) Nuclear and nucleolar targeting of influenza A virus NS1 protein: striking differences between different virus subtypes. J. Virol., 81, 5995-6006.
47. Catez, F., Erard, M., Schaerer-Uthurralt, N., Kindbeiter, K., Madjar, J. J. and Diaz, J. J. (2002) Unique motif for nucleolar retention and nuclear export regulated by phosphorylation. Mol. Cell Biol., 22, 1126-1139.
48. Cheng, G., Brett, M. E. and He, B. (2002) Signals that dictate nuclear, nucleolar, and cytoplasmic shuttling of the gamma(1)34. 5 protein of herpes simplex virus type 1. J. Virol., 76, 9434-9445.
49. Boyne, J. R. and Whitehouse, A. (2006) Nucleolar trafficking is essential for nuclear export of intronless herpesvirus mRNA. Proc. Natl Acad. Sci. USA, 103, 15190-15195.
50. Savitsky, K., Ziv, Y., Bar-Shira, A., Gilad, S., Tagle, D. A., Smith, S., Uziel, T., Sfez, S., Nahmias, J., Sartiel, A. et al. (1996) A human gene (DDX10) encoding a putative DEAD-box RNA helicase at 11q22-q23. Genomics, 33, 199-206.
51. Gozani, O., Feld, R. and Reed, R. (1996) Evidence that sequence-independent binding of highly conserved U2 snRNP proteins upstream of the branch site is required for assembly of spliceosomal complex A. Genes Dev., 10, 233-243.
52. Neubauer, G., King, A., Rappsilber, J., Calvio, C., Watson, M., Ajuh, P., Sleeman, J., Lamond, A. and Mann, M. (1998) Mass spectrometry and EST-database searching allows characterization of the multi-protein spliceosome complex. Nat. Genet., 20, 46-50.
53. Zhou, Z., Licklider, L. J., Gygi, S. P. and Reed, R. (2002) Comprehensive proteomic analysis of the human spliceosome. Nature, 419, 182-185.
54. Lum, L. S., Sultzman, L. A., Kaufman, R. J., Linzer, D. I. and Wu, B. J. (1990) A cloned human CCAAT-box-binding factor stimulates transcription from the human hsp70 promoter. Mol. Cell Biol., 10, 6709-6717.
55. Muchardt, C., Reyes, J. C., Bourachot, B., Leguoy, E. and Yaniv, M. (1996) The hbrm and BRG-1 proteins, components of the human SNF/SWI complex, are phosphorylated and excluded from the condensed chromosomes during mitosis. EMBO J., 15, 3394-3402.
56. Simpson, F., Peden, A. A., Christopoulou, L. and Robinson, M. S. (1997) Characterization of the adaptor-related protein complex, AP-3. J. Cell Biol., 137, 835-845.
57. Politz, J. C., Yarovoi, S., Kilroy, S. M., Gowda, K., Zwieb, C. and Pederson, T. (2000) Signal recognition particle components in the nucleolus. Proc. Natl Acad. Sci. USA, 97, 55-60.
58. Barbe, L., Lundberg, E., Oksvold, P., Stenius, A., Lewin, E., Bjorling, E., Asplund, A., Ponten, F., Brismar, H., Uhlen, M. et al. (2008) Toward a confocal subcellular atlas of the human proteome. Mol. Cell Proteomics, 7, 499-508.