Functional dissection of an intrinsically disordered protein: Understanding the roles of different domains of Knr4 protein in protein-protein interactions

Protein Science

Volumn 19, Issue 7, 2010, Pages 1376-1385

  Dagkessamanskaia, Adilia ^a,b   Durand, Fabien ^a,b   Uversky, Vladimir N ^c,d,e   Binda, Matteo ^f   Lopez, Frédè́ric ^g   El Azzouzi, Karim ^a,b   Francois, Jean Marie ^a,b   Martin Yken, Hélène ^a,b  

^a UNIVERSITÉ DE TOULOUSE   (France)

^b CNRS   (France)

^c INDIANA UNIVERSITY   (United States)

^d INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e INSTITUTE FOR BIOLOGICAL INSTRUMENTATION   (Russian Federation)

^f UNIVERSITY OF FRIBOURG   (Switzerland)

^g INSERM   (France)

Author keywords

Disordered protein regions; Intrinsically unstructured (disordered); Protein protein interactions; Proteins; Surface plasmon resonance; Two hybrid system

Indexed keywords

FUNGAL PROTEIN; PROTEIN KNR4; UNCLASSIFIED DRUG; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE; STRUCTURE ACTIVITY RELATION; SURFACE PLASMON RESONANCE; TWO HYBRID SYSTEM; CHEMISTRY; GENETICS; METABOLISM;

SACCHAROMYCES CEREVISIAE;

PROTEIN BINDING; SACCHAROMYCES CEREVISIAE PROTEINS; SURFACE PLASMON RESONANCE; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 77953965777     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.418     Document Type: Article

References (55)

1. Martin H, Dagkessamanskaia A, Satchanska G, Dallies N, Francois J (1999) KNR4, a suppressor of Saccharomyces cerevisiae cwh mutants, is involved in the transcriptional control of chitin synthase genes. Microbiology 145:249-258. (Pubitemid 29043597)
2. Martin-Yken H, Dagkessamanskaia A, Basmaji F, Lagorce A, Francois J (2003) The interaction of Slt2 MAP kinase with Knr4 is necessary for signalling through the cell wall integrity pathway in Saccharomyces cerevisiae. Mol Microbiol 49:23-35. (Pubitemid 36792001)
3. Lesage G, Bussey H (2006) Cell wall assembly in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 70: 317-343. (Pubitemid 43895030)
4. Uetz P, Giot L, Cagney G, Mansfield TA, Judson RS, Knight JR, Lockshon D, Narayan V, Srinivasan M, Pochart P, Qureshi-Emili A, Li Y, Godwi B, Conover D, Kalbfleisch T, Vijayadamodar G, Yang M, Johnston M, Fields S, Rothberg JM (2000) A comprehensive analysis of protein-protein interactions in Saccharomyces cerevisiae. Nature 403:623-627. (Pubitemid 30103994)
5. Dagkessamanskaia A, Martin-Yken H, Basmaji F, Briza P, Francois J (2001) Interaction of Knr4 protein, a protein involved in cell wall synthesis, with tyrosine tRNA synthetase encoded by TYS1 in Saccharomyces cerevisiae. FEMS Microbiol Lett 200:53-58.
6. Basmaji F, Martin-Yken H, Durand F, Dagkessamanskaia A, Pichereaux C, Rossignol M, Francois J (2006) The 'interactome' of the Knr4/Smi1, a protein implicated in coordinating cell wall synthesis with bud emergence in Saccharomyces cerevisiae. Mol Genet Genomics 275:217-230.
7. Krogan NJ, Cagney G, Yu H, Zhong G, Guo X, Ignatchenko A, Li J, Pu S, Datta N, Tikuisis AP, Punna T, Peregrín-Alvarez JM, Shales M, Zhang X, Davey M, Robinson MD, Paccanaro A, Bray JE, Sheung A, Beattie B, Richards DP, Canadien V, Lalev A, Mena F, Wong P, Starostine A, Canete MM, Vlasblom J, Wu S, Orsi C, Collins SR, Chandran S, Haw R, Rilstone JJ, Gandi K, Thompson NJ, Musso G, St Onge P, Ghanny S, Lam MH, Butland G, Altaf-Ul AM, Kanaya S, Shilatifard A, O'Shea E, Weissman JS, Ingles CJ, Hughes TR, Parkinson J, Gerstein M, Wodak SJ, Emili A, Greenblatt JF (2006) Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature 440:637-643.
8. Tarassov K, Messier V, Landry CR, Radinovic S, Serna Molina MM, Shames I, Malitskaya Y, Vogel J, Bussey H, Michnick SW (2008) An in vivo map of the yeast protein interactome. Science 320:1465-1470. (Pubitemid 351929421)
9. Durand F, Dagkessamanskaia A, Martin-Yken H, Graille M, Van Tilbeurgh H, Uversky VN, Francois JM (2008) Structure-function analysis of Knr4/Smi1, a newly member of intrinsically disordered proteins family, indispensable in the absence of a functional PKC1-SLT2 pathway in Saccharomyces cerevisiae. Yeast 25:563-576.
10. Uversky VN, Gillespie JR, Fink AL (2000) Why are "natively unfolded" proteins unstructured under physiologic conditions? Proteins 41:415-427.
11. Dunker AK, Lawson JD, Brown CJ, Williams RM, Romero P, Oh JS, Oldfield CJ, Campen AM, Ratliff CM, Hipps KW, Ausio J, Nissen MS, Reeves R, Kang C, Kissinger CR, Bailey RW, Griswold MD, Chiu W, Garner EC, Obradovic Z (2001) Intrinsically disordered protein. J Mol Graph Model 19:26-59.
12. Tompa P (2002) Intrinsically unstructured proteins. Trends Biochem Sci 27:527-533.
13. Uversky VN (2002) What does it mean to be natively unfolded? Eur J Biochem 269:2-12.
14. Dyson HJ, Wright PE (2005) Intrinsically unstructured proteins and their functions. Nat Rev Mol Cell Biol 6: 197-208. (Pubitemid 40314921)
15. Uversky VN (2002) Natively unfolded proteins: a point where biology waits for physics. Protein Sci 11: 739-756.
16. Dunker AK, Silman I, Uversky VN, Sussman JL (2008) Function and structure of inherently disordered proteins. Curr Opin Struct Biol 18:756-764.
17. Dunker AK, Oldfield CJ, Meng J, Romero P, Yang JY, Chen JW, Vacic V, Obradovic Z, Uversky VN (2008) The unfoldomics decade: an update on intrinsically disordered proteins. BMC Genomics 9: Suppl 1, S1.
18. Iakoucheva LM, Brown CJ, Lawson JD, Obradovic Z, Dunker AK (2002) Intrinsic disorder in cell-signaling and cancer-associated proteins. J Mol Biol 323:573-584. (Pubitemid 35283681)
19. Uversky VN, Oldfield CJ, Dunker AK (2005) Showing your ID: intrinsic disorder as an ID for recognition, regulation and cell signaling. J Mol Recognit 18: 343-384.
20. Xie H, Vucetic S, Iakoucheva LM, Oldfield CJ, Dunker AK, Uversky VN, Obradovic Z (2007) Functional anthology of intrinsic disorder. 1. Biological processes and functions of proteins with long disordered regions. J Proteome Res 6:1882-1898. (Pubitemid 46814512)
21. Vucetic S, Xie H, Iakoucheva LM, Oldfield CJ, Dunker AK, Obradovic Z, Uversky VN (2007) Functional anthology of intrinsic disorder. 2. Cellular components, domains, technical terms, developmental processes, and coding sequence diversities correlated with long disordered regions. J Proteome Res 6:1899-1916. (Pubitemid 46814513)
22. Xie H, Vucetic S, Iakoucheva LM, Oldfield CJ, Dunker AK, Obradovic Z, Uversky VN (2007) Functional anthology of intrinsic disorder. 3. Ligands, post-translational modifications, and diseases associated with intrinsically disordered proteins. J Proteome Res 6: 1917-1932. (Pubitemid 46814514)
23. Cagney G, Uetz P (2001) High-throughput screening for protein-protein interactions using yeast two-hybrid arrays. Curr Protoc Protein Sci Chapter 19, Unit 19.6.
24. Vacic V, Oldfield CJ, Mohan A, Radivojac P, Cortese MS, Uversky VN, Dunker AK (2007) Characterization of molecular recognition features, MoRFs, and their binding partners. J Proteome Res 6:2351-2366. (Pubitemid 46985123)
25. Radivojac P, Iakoucheva LM, Oldfield CJ, Obradovic Z, Uversky VN, Dunker AK (2007) Intrinsic disorder and functional proteomics. Biophys J 92:1439-1456.
26. Deleage G, Blanchet C, Geourjon C (1997) Protein structure prediction. Implications for the biologist. Biochimie 79:681-686.
27. Sickmeier M, Hamilton JA, LeGall T, Vacic V, Cortese MS, Tantos A, Szabo B, Tompa P, Chen J, Uversky VN, Obradovic Z, Dunker AK (2007) DisProt: the database of disordered proteins. Nucleic Acids Res 35: D786-D793.
28. Xue B, Dunbrack RL, Williams RW, Dunker AK, Uversky VN (2010) PONDR-FIT: a meta-predictor of intrinsically disordered amino acids. Biochim Biophys Acta 1804:996-1010.
29. Romero P, Obradovic Z, Li X, Garner EC, Brown CJ, Dunker AK (2001) Sequencecomplexity of disordered protein. Proteins 42:38-48.
30. Obradovic Z, Peng K, Vucetic S, Radivojac P, Dunker AK (2005) Exploiting heterogeneous sequence properties improves prediction of protein disorder. Proteins 61:176-182. (Pubitemid 43069972)
31. Obradovic Z, Peng K, Vucetic S, Radivojac P, Brown CJ, Dunker AK (2003) Predicting intrinsic disorder from amino acid sequence. Proteins 53:566-572. (Pubitemid 37352217)
32. Prilusky J, Felder CE, Zeev-Ben-Mordehai T, Rydberg EH, Man O, Beckmann JS, Silman I, Sussman JL (2005) FoldIndex: a simple tool to predict whether a given protein sequence is intrinsically unfolded. Bioinformatics 21:3435-3438. (Pubitemid 41222454)
33. Dosztanyi Z, Csizmok V, Tompa P, Simon I (2005) The pairwise energy content estimated from amino acid composition discriminates between folded and intrinsically unstructured proteins. J Mol Biol 347:827-839. (Pubitemid 40357923)
34. Campen A, Williams RM, Brown CJ, Meng J, Uversky VN, Dunker AK (2008) TOP-IDP-scale: a new amino acid scale measuring propensity for intrinsic disorder. Protein Pept Lett 15:956-963.
35. Callaghan AJ, Aurikko JP, Ilag LL, Gunter Grossmann J, Chandran V, Kuhnel K, Poljak L, Carpousis AJ, Robinson CV, Symmons MF, Luisi BF (2004) Studies of the RNA degradosome-organizing domain of the Escherichia coli ribonuclease RNase E. J Mol Biol 340:965-979.
36. Oldfield CJ, Cheng Y, Cortese MS, Romero P, Uversky VN, Dunker AK (2005) Coupled folding and binding with alpha-helix-forming molecular recognition elements. Biochemistry 44:12454-12470.
37. Mohan A, Oldfield CJ, Radivojac P, Vacic V, Cortese MS, Dunker AK, Uversky VN (2006) Analysis of molecular recognition features (MoRFs). J Mol Biol 362:1043-1059.
38. Cheng Y, Oldfield CJ, Meng J, Romero P, Uversky VN, Dunker AK (2007) Mining alpha-helix-forming molecular recognition features with cross species sequence alignments. Biochemistry 46:13468-13477.
39. Ng KP, Potikyan G, Savene RO, Denny CT, Uversky VN, Lee KA (2007) Multiple aromatic side chains within a disordered structure are critical for transcription and transforming activity of EWS family oncoproteins. Proc Natl Acad Sci USA 104:479-484.
40. Han JD, Bertin N, Hao T, Goldberg DS, Berriz GF, Zhang LV, Dupuy D, Walhout AJ, Cusick ME, Roth FP, Vidal M (2004) Evidence for dynamically organized modularity in the yeast protein-protein interaction network. Nature 430:88-93.
41. Dunker AK, Cortese MS, Romero P, Iakoucheva LM, Uversky VN (2005) Flexible nets. The roles of intrinsic disorder in protein interaction networks. FEBS J 272: 5129-5148.
42. Gsponer J, Futschik ME, Teichmann SA, Babu MM (2008) Tight regulation of unstructured proteins: from transcript synthesis to protein degradation. Science 322:1365-1368.
43. Wright PE, Dyson HJ (1999) Intrinsically, unstructured proteins: reassessing the protein structure-function paradigm. J Mol Biol 293:321-331.
44. Dyson HJ, Wright PE (2002) Coupling of folding and binding for unstructured proteins. Curr Opin Struct Biol 12:54-60.
45. Wright PE, Dyson HJ (2009) Linking folding and binding. Curr Opin Struct Biol 19:31-38.
46. Patil A, Nakamura H (2006) Disordered domains and high surface charge confer hubs with the ability to interact with multiple proteins in interaction networks. FEBS Lett 580:2041-2045.
47. Ekman D, Light S, Bjorklund AK, Elofsson A (2006) What properties characterize the hub proteins of the protein-protein interaction network of Saccharomyces cerevisiae? Genome Biol 7:R45.
48. Higurashi M, Ishida T, Kinoshita K (2008) Identification of transient hub proteins and the possible structural basis for their multiple interactions. Protein Sci 17:72-78.
49. Singh GP, Ganapathi M, Dash D (2007) Role of intrinsic disorder in transient interactions of hub proteins. Proteins 66:761-765.
50. Uversky VN, Dunker AK (2008) Biochemistry. Controlled chaos. Science 322:1340-1341.
51. Grimmler M, Wang Y, Mund T, Cilensek Z, Keidel EM, Waddell MB, Jakel H, Kullmann M, Kriwacki RW, Hengst L (2007) Cdk-inhibitory activity and stability of p27Kip1 are directly regulated by oncogenic tyrosine kinases. Cell 128:269-280.
52. 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.
53. James P, Halladay J, Craig EA (1996) Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics 144:1425-1436. (Pubitemid 26427892)
54. Ishida T, Kinoshita K (2008) Prediction of disordered regions in proteins based on the meta approach. Bioinformatics 24:1344-1348. (Pubitemid 351737139)
55. Schlessinger A, Punta M, Yachdav G, Kajan L, Rost B (2009) Improved disorder prediction by combination of orthogonal approaches. PLoS One 4:e4433.