N-termini of fungal CSL transcription factors are disordered, enriched in regulatory motifs and inhibit DNA binding in fission yeast

PLoS ONE

Volumn 6, Issue 8, 2011, Pages

  Převorovský, Martin ^a,b   Atkinson, Sophie R ^a   Ptáčková, Martina ^b   McLean, Janel R ^c   Gould, Kathleen ^c   Folk, Petr ^b   Půta, František ^b   Bähler, Jürg ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b CHARLES UNIVERSITY   (Czech Republic)

^c VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN; IMMUNOGLOBULIN J RECOMBINATION SIGNAL SEQUENCE BINDING PROTEIN; PROTEIN CBF1; PROTEIN CBF12; PROTEIN LAG 1; SUPPRESSOR OF HAIRLESS PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; CBF11 PROTEIN, S POMBE; CBF12 PROTEIN, S POMBE; DNA; PHOSPHOPEPTIDE; SCHIZOSACCHAROMYCES POMBE PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; BIOINFORMATICS; CELL ADHESION; CONTROLLED STUDY; DNA BINDING; FUNGAL CELL; GEL MOBILITY SHIFT ASSAY; METAZOON; NONHUMAN; NUCLEAR DIVISION; PROTEIN DEGRADATION; PROTEIN DNA BINDING; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; SCHIZOSACCHAROMYCES POMBE; TRANSCRIPTION REGULATION; AMINO ACID SEQUENCE; BINDING SITE; CHEMISTRY; GENETICS; MASS SPECTROMETRY; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; OLIGONUCLEOTIDE PROBE; PHOSPHORYLATION; PHYLOGENY; POLYMERASE CHAIN REACTION; PROTEIN BINDING; REGULATORY SEQUENCE; SCHIZOSACCHAROMYCES; SEQUENCE HOMOLOGY; WESTERN BLOTTING;

FUNGI; INVERTEBRATA; METAZOA; SCHIZOSACCHAROMYCETACEAE;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; BASE SEQUENCE; BINDING SITES; BLOTTING, WESTERN; CONSERVED SEQUENCE; DNA; ELECTROPHORETIC MOBILITY SHIFT ASSAY; FUNGAL PROTEINS; MASS SPECTROMETRY; MOLECULAR SEQUENCE DATA; OLIGONUCLEOTIDE PROBES; PHOSPHOPEPTIDES; PHOSPHORYLATION; PHYLOGENY; POLYMERASE CHAIN REACTION; PROTEIN BINDING; REGULATORY SEQUENCES, NUCLEIC ACID; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; TRANSCRIPTION FACTORS;

EID: 80051609608     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0023650     Document Type: Article

References (67)

1. Hollstein M, Hainaut P, (2010) Massively regulated genes: the example of TP53. The Journal of pathology 220: 164-73 doi:10.1002/path.2637.
2. Osborne TF, Espenshade PJ, (2009) Evolutionary conservation and adaptation in the mechanism that regulates SREBP action: what a long, strange tRIP it's been. Genes & development 23: 2578-91 doi:10.1101/gad.1854309.
3. Ward JJ, Sodhi JS, McGuffin LJ, Buxton BF, Jones DT, (2004) Prediction and functional analysis of native disorder in proteins from the three kingdoms of life. Journal of Molecular Biology 337: 635-645.
4. Vavouri T, Semple JI, Garcia-Verdugo R, Lehner B, (2009) Intrinsic protein disorder and interaction promiscuity are widely associated with dosage sensitivity. Cell 138: 198-208 doi:10.1016/j.cell.2009.04.029.
5. Gsponer J, Futschik ME, Teichmann SA, Babu MM, (2008) Tight regulation of unstructured proteins: from transcript synthesis to protein degradation. Science 322: 1365-1368.
6. Dunker AK, Oldfield CJ, Meng J, Romero P, Yang JY, et al. (2008) The unfoldomics decade: an update on intrinsically disordered proteins. BMC Genomics 9 (Suppl 2): S1.
7. Pursglove SE, Mackay JP, (2005) CSL: a notch above the rest. Int J Biochem Cell Biol 37: 2472-2477.
8. Bray SJ, (2006) Notch signalling: a simple pathway becomes complex. Nat Rev Mol Cell Biol 7: 678-689.
9. Lai EC, (2004) Notch signaling: control of cell communication and cell fate. Development (Cambridge, England) 131: 965-973.
10. Weng AP, Aster JC, (2004) Multiple niches for Notch in cancer: context is everything. Current opinion in genetics & development 14: 48-54 doi:10.1016/j.gde.2003.11.004.
11. Hayward SD, (2004) Viral interactions with the Notch pathway. Semin Cancer Biol 14: 387-396.
12. Gazave E, Lapébie P, Richards GS, Brunet F, Ereskovsky AV, et al. (2009) Origin and evolution of the Notch signalling pathway: an overview from eukaryotic genomes. BMC evolutionary biology 9: 249 doi:10.1186/1471-2148-9-249.
13. Převorovský M, Půta F, Folk P, (2007) Fungal CSL transcription factors. BMC Genomics 8: 233.
14. Koelzer S, Klein T, (2003) A Notch-independent function of Suppressor of Hairless during the development of the bristle sensory organ precursor cell of Drosophila. Development (Cambridge, England) 130: 1973-1988.
15. Barolo S, Walker RG, Polyanovsky AD, Freschi G, Keil T, et al. (2000) A notch-independent activity of suppressor of hairless is required for normal mechanoreceptor physiology. Cell 103: 957-969.
16. Beres TM, Masui T, Swift GH, Shi L, Henke RM, et al. (2006) PTF1 is an organ-specific and Notch-independent basic helix-loop-helix complex containing the mammalian Suppressor of Hairless (RBP-J) or its paralogue, RBP-L. Mol Cell Biol 26: 117-130.
17. Převorovský M, Groušl T, Staňurová J, Ryneš J, Nellen W, et al. (2009) Cbf11 and Cbf12, the fission yeast CSL proteins, play opposing roles in cell adhesion and coordination of cell and nuclear division. Experimental Cell Research 315: 1533-1547.
18. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics (Oxford, England) 23: 2947-8 doi:10.1093/bioinformatics/btm404.
19. Kovall RA, Hendrickson WA, (2004) Crystal structure of the nuclear effector of Notch signaling, CSL, bound to DNA. The EMBO Journal 23: 3441-3451.
20. Tamura K, Dudley J, Nei M, Kumar S, (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular biology and evolution 24: 1596-9 doi:10.1093/molbev/msm092.
21. Li X, Kahveci T, (2006) A Novel algorithm for identifying low-complexity regions in a protein sequence. Bioinformatics (Oxford, England) 22: 2980-7 doi:10.1093/bioinformatics/btl495.
22. Kelley LA, Sternberg MJE, (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nature Protocols 4: 363-371.
23. Buchan DWa, Ward SM, Lobley aE, Nugent TCO, Bryson K, et al. (2010) Protein annotation and modelling servers at University College London. Nucleic acids research 38 (Suppl): W563-8 doi:10.1093/nar/gkq427.
24. Huang H-D, Lee T-Y, Tzeng S-W, Horng J-T, (2005) KinasePhos: a web tool for identifying protein kinase-specific phosphorylation sites. Nucleic acids research 33: W226-9 doi:10.1093/nar/gki471.
25. Blom N, Gammeltoft S, Brunak S, (1999) Sequence and structure-based prediction of eukaryotic protein phosphorylation sites. Journal of molecular biology 294: 1351-62 doi:10.1006/jmbi.1999.3310.
26. Iakoucheva LM, Radivojac P, Brown CJ, O'Connor TR, Sikes JG, et al. (2004) The importance of intrinsic disorder for protein phosphorylation. Nucleic acids research 32: 1037-49 doi:10.1093/nar/gkh253.
27. Rice P, Longden I, Bleasby A, (2000) EMBOSS: the European Molecular Biology Open Software Suite. Trends in genetics: TIG 16: 276-7.
28. Van DB, Tafforeau L, Hentges P, Carr AM, Vandenhaute J, (2005) Additional vectors for PCR-based gene tagging in Saccharomyces cerevisiae and Schizosaccharomyces pombe using nourseothricin resistance. Yeast (Chichester, England) 22: 1061-1068.
29. Moreno S, Klar A, Nurse P, (1991) Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods in enzymology 194: 795-823 doi:10.1534/genetics.107.076315.
30. Bähler J, Wu JQ, Longtine MS, Shah NG, McKenzie a, et al. (1998) Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast (Chichester, England) 14: 943-51 doi:10.1002/(SICI)1097-0061(199807)14:10<943::AID-YEA292>3.0.CO;2-Y/.
31. Basi G, Schmid E, Maundrell K, (1993) TATA box mutations in the Schizosaccharomyces pombe nmt1 promoter affect transcription efficiency but not the transcription start point or thiamine repressibility. Gene 123: 131-136.
32. Rigaut G, Shevchenko A, Rutz B, Wilm M, Mann M, et al. (1999) A generic protein purification method for protein complex characterization and proteome exploration. Nat Biotechnol 17: 1030-1032.
33. McDonald WH, Ohi R, Miyamoto DT, Mitchison TJ, Yates JR, (2002) Comparison of three directly coupled HPLC MS/MS strategies for identification of proteins from complex mixtures: single-dimension LC-MS/MS, 2-phase MudPIT, and 3-phase MudPIT. International Journal of Mass Spectrometry 219: 245-251 doi:10.1016/S1387-3806(02)00563-8.
34. Roberts-Galbraith RH, Chen J-S, Wang J, Gould KL, (2009) The SH3 domains of two PCH family members cooperate in assembly of the Schizosaccharomyces pombe contractile ring. The Journal of cell biology 184: 113-27 doi:10.1083/jcb.200806044.
35. Tabb DL, Fernando CG, Chambers MC, (2007) MyriMatch: highly accurate tandem mass spectral peptide identification by multivariate hypergeometric analysis. Journal of proteome research 6: 654-61 doi:10.1021/pr0604054.
36. Zhang B, Chambers MC, Tabb DL, (2007) Proteomic parsimony through bipartite graph analysis improves accuracy and transparency. Journal of proteome research 6: 3549-57 doi:10.1021/pr070230d.
37. Ma Z-Q, Dasari S, Chambers MC, Litton MD, Sobecki SM, et al. (2009) IDPicker 2.0: Improved protein assembly with high discrimination peptide identification filtering. Journal of proteome research 8: 3872-81 doi:10.1021/pr900360j.
38. Wilson JJ, Kovall RA, (2006) Crystal structure of the CSL-Notch-Mastermind ternary complex bound to DNA. Cell 124: 985-996.
39. Nam Y, Sliz P, Song L, Aster JC, Blacklow SC, (2006) Structural basis for cooperativity in recruitment of MAML coactivators to Notch transcription complexes. Cell 124: 973-983.
40. Wilhelm BT, Marguerat S, Watt S, Schubert F, Wood V, et al. (2008) Dynamic repertoire of a eukaryotic transcriptome surveyed at single-nucleotide resolution. Nature 453: 1239-1243.
41. Finn RD, Mistry J, Tate J, Coggill P, Heger A, et al. (2010) The Pfam protein families database. Nucleic acids research 38: D211-22 doi:10.1093/nar/gkp985.
42. Peng K, Radivojac P, Vucetic S, Dunker AK, Obradovic Z, (2006) Length-dependent prediction of protein intrinsic disorder. BMC Bioinformatics 7: 208.
43. Galea Ca, Wang Y, Sivakolundu SG, Kriwacki RW, (2008) Regulation of cell division by intrinsically unstructured proteins: intrinsic flexibility, modularity, and signaling conduits. Biochemistry 47: 7598-609 doi:10.1021/bi8006803.
44. Vacic V, Uversky VN, Dunker AK, Lonardi S, (2007) Composition Profiler: a tool for discovery and visualization of amino acid composition differences. BMC Bioinformatics 8: 211.
45. Rechsteiner M, Rogers SW, (1996) PEST sequences and regulation by proteolysis. Trends in biochemical sciences 21: 267-71.
46. Singh GP, Ganapathi M, Sandhu KS, Dash D, (2006) Intrinsic unstructuredness and abundance of PEST motifs in eukaryotic proteomes. Proteins 62: 309-15 doi:10.1002/prot.20746.
47. Wood V, Gwilliam R, Rajandream MA, Lyne M, Lyne R, et al. (2002) The genome sequence of Schizosaccharomyces pombe. Nature 415: 871-880.
48. Kämper J, Kahmann R, Bölker M, Ma L-J, Brefort T, et al. (2006) Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444: 97-101 doi:10.1038/nature05248.
49. Loftus BJ, Fung E, Roncaglia P, Rowley D, Amedeo P, et al. (2005) The genome of the basidiomycetous yeast and human pathogen Cryptococcus neoformans. Science (New York, N Y) 307: 1321-4 doi:10.1126/science.1103773.
50. Warringer J, Blomberg A, (2006) Evolutionary constraints on yeast protein size. BMC evolutionary biology 6: 61 doi:10.1186/1471-2148-6-61.
51. Beltrao P, Trinidad JC, Fiedler D, Roguev A, Lim WA, et al. (2009) Evolution of phosphoregulation: comparison of phosphorylation patterns across yeast species. PLoS Biology 7: e1000134.
52. Sandoval A, Oviedo N, Tadmouri A, Avila T, De Waard M, et al. (2006) Two PEST-like motifs regulate Ca2+/calpain-mediated cleavage of the CaVbeta3 subunit and provide important determinants for neuronal Ca2+ channel activity. The European journal of neuroscience 23: 2311-20 doi:10.1111/j.1460-9568.2006.04749.x.
53. Liu F, Dowling M, Yang X-J, Kao GD, (2004) Caspase-mediated specific cleavage of human histone deacetylase 4. The Journal of biological chemistry 279: 34537-46 doi:10.1074/jbc.M402475200.
54. Edwards YJK, Lobley AE, Pentony MM, Jones DT, (2009) Insights into the regulation of intrinsically disordered proteins in the human proteome by analyzing sequence and gene expression data. Genome Biology 10: R50.
55. Gsponer J, Madan BM, (2009) The rules of disorder or why disorder rules. Progress in Biophysics and Molecular Biology.
56. Walowitz JL, Bradley ME, Chen S, Lee T, (1998) Proteolytic regulation of the zinc finger transcription factor YY1, a repressor of muscle-restricted gene expression. The Journal of biological chemistry 273: 6656-61.
57. Liu ZQ, Kunimatsu M, Yang JP, Ozaki Y, Sasaki M, et al. (1996) Proteolytic processing of nuclear factor kappa B by calpain in vitro. FEBS letters 385: 109-13.
58. Zhao S, Xu W, Jiang W, Yu W, Lin Y, et al. (2010) Regulation of cellular metabolism by protein lysine acetylation. Science (New York, N Y) 327: 1000-4 doi:10.1126/science.1179689.
59. Raijmakers R, Kraiczek K, Jong AP de, Mohammed S, Heck AJR, (2010) Exploring the human leukocyte phosphoproteome using a microfluidic reversed-phase-TiO2-reversed-phase high-performance liquid chromatography phosphochip coupled to a quadrupole time-of-flight mass spectrometer. Analytical chemistry 82: 824-32 doi:10.1021/ac901764g.
60. Wesley CS, Mok LP, (2003) Regulation of Notch signaling by a novel mechanism involving suppressor of hairless stability and carboxyl terminus-truncated notch. Mol Cell Biol 23: 5581-5593.
61. Kovall RA, (2008) More complicated than it looks: assembly of Notch pathway transcription complexes. Oncogene 27: 5099-5109.
62. Jarvis JN, Harrison TS, (2007) HIV-associated cryptococcal meningitis. AIDS (London, England) 21: 2119-29 doi:10.1097/QAD.0b013e3282a4a64d.
63. Crespo Erchiga V, Delgado Florencio V, (2002) Malassezia species in skin diseases. Current opinion in infectious diseases 15: 133-42.
64. Prabhu RM, Patel R, (2004) Mucormycosis and entomophthoramycosis: a review of the clinical manifestations, diagnosis and treatment. Clinical microbiology and infection: the official publication of the European Society of Clinical Microbiology and Infectious Diseases 10 (Suppl 1): 31-47.
65. Martinez D, Challacombe J, Morgenstern I, Hibbett D, Schmoll M, et al. (2009) Genome, transcriptome, and secretome analysis of wood decay fungus Postia placenta supports unique mechanisms of lignocellulose conversion. Proceedings of the National Academy of Sciences of the United States of America 106: 1954-9 doi:10.1073/pnas.0809575106.
66. Snellinx Z, Nepovím A, Taghavi S, Vangronsveld J, Vanek T, et al. (2002) Biological remediation of explosives and related nitroaromatic compounds. Environmental science and pollution research international 9: 48-61.
67. Mendes-Giannini MJ, Soares CP, Silva JL da, Andreotti PF, (2005) Interaction of pathogenic fungi with host cells: Molecular and cellular approaches. FEMS Immunol Med Microbiol 45: 383-394.