Defining structural domains of an intrinsically disordered protein: Sic1, the cyclin-dependent kinase inhibitor of Saccharomyces cerevisiae

Molecular Biotechnology

Volumn 47, Issue 1, 2011, Pages 34-42

  Brocca, Stefania ^a   Testa, Lorenzo ^a   Šamalikova, Maria ^a   Grandori, Rita ^a   Lotti, Marina ^a  

^a UNIVERSITY OF MILANO BICOCCA   (Italy)

Author keywords

Circular dichroism; Disordered domains; Escherichia coli; Heterologous expression; Mass spectrometry

Indexed keywords

BIOLOGICAL FUNCTIONS; C-TERMINAL FRAGMENTS; CIRCULAR DICHROISM; CYCLIN-DEPENDENT KINASE INHIBITORS; DISORDERED DOMAINS; DISORDERED PROTEINS; FULL-LENGTH PROTEINS; HETEROLOGOUS EXPRESSION; IDENTIFICATION OF PROTEINS; IN-CELL; N-TERMINALS; PURIFICATION PROTOCOL; RECOMBINANT PROTEIN; SACCHAROMYCES CEREVISIAE; STRUCTURAL CHARACTERIZATION; STRUCTURAL DIFFERENCES; STRUCTURAL DOMAINS; YEAST SACCHAROMYCES CEREVISIAE;

ENZYMES; ESCHERICHIA COLI; HEAT RESISTANCE; MAGNETIC DOMAINS; MASS SPECTROMETRY; NUCLEAR MAGNETIC RESONANCE; PURIFICATION; RESONANCE; YEAST;

DICHROISM;

CYCLIN DEPENDENT KINASE INHIBITOR; RECOMBINANT PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN; SIC1 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CIRCULAR DICHROISM; HEAT TOLERANCE; HEAT TREATMENT; HETEROLOGOUS EXPRESSION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN PURIFICATION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; SACCHAROMYCES CEREVISIAE;

CIRCULAR DICHROISM; CYCLIN-DEPENDENT KINASE INHIBITOR PROTEINS; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, FUNGAL; MAGNETIC RESONANCE SPECTROSCOPY; PHOSPHORYLATION; PLASMIDS; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

ESCHERICHIA COLI; SACCHAROMYCES CEREVISIAE;

EID: 79551520602     PISSN: 10736085     EISSN: None     Source Type: Journal    
DOI: 10.1007/s12033-010-9309-y     Document Type: Article

References (42)

1. AL Fink 2005 Natively unfolded proteins Current Opinion in Structural Biology 15 35 41 1:CAS:528:DC%2BD2MXhsFSht7o%3D 10.1016/j.sbi.2005.01.002 (Pubitemid 40249507)
2. VN Uversky JR Gillespie AL Fink 2000 Why are "natively unfolded" proteins unstructured under physiologic conditions? Proteins 41 415 427 1:CAS:528:DC%2BD3cXnslGnsLs%3D 10.1002/1097-0134(20001115)41:3<415:: AID-PROT130>3.0.CO;2-7
3. LM Iakoucheva P Radivojac CJ Brown TR O'Connor JG Sikes Z Obradovic, et al. 2004 The importance of intrinsic disorder for protein phosphorylation Nucleic Acids Research 32 1037 1049 1:CAS:528:DC%2BD2cXhslWktLg%3D 10.1093/nar/gkh253 (Pubitemid 38854704)
4. AK Dunker JD Lawson CJ Brown RM Williams P Romero JS Oh, et al. 2001 Intrinsically disordered protein Journal of Molecular Graphics and Modelling 19 26 59 1:CAS:528:DC%2BD3MXjtFGmsro%3D 10.1016/S1093-3263(00)00138-8 (Pubitemid 32411501)
5. V Vacic CJ Oldfield A Mohan P Radivojac MS Cortese VN Uversky, et al. 2007 Characterization of molecular recognition features, MoRFs, and their binding partners Journal of Proteome Research 6 2351 2366 1:CAS:528: DC%2BD2sXltVajtL8%3D 10.1021/pr0701411 (Pubitemid 46985123)
6. VN Uversky CJ Oldfield AK Dunker 2005 Showing your ID: Intrinsic disorder as an ID for recognition, regulation and cell signaling Journal of Molecular Recognition 18 343 384 1:CAS:528:DC%2BD2MXhtVCgt73F 10.1002/jmr.747 (Pubitemid 41341287)
7. AK Dunker CJ Brown JD Lawson LM Iakoucheva Z Obradovic 2002 Intrinsic disorder and protein function Biochemistry 41 6573 6582 1:CAS:528: DC%2BD38Xjt1aitbc%3D 10.1021/bi012159+ (Pubitemid 34547347)
8. AK Dunker Z Obradovic 2001 The protein trinity-linking function and disorder Nature Biotechnology 19 805 806 1:CAS:528:DC%2BD3MXmvVWrtLc%3D 10.1038/nbt0901-805 (Pubitemid 32816745)
9. HJ Dyson PE Wright 2005 Intrinsically unstructured proteins and their functions Nature Reviews Molecular Cell Biology 6 197 208 1:CAS:528: DC%2BD2MXhslSlsLo%3D 10.1038/nrm1589 (Pubitemid 40314921)
10. PE Wright HJ Dyson 1999 Intrinsically unstructured proteins: Re-assessing the protein structure-function paradigm Journal of Molecular Biology 293 321 331 1:CAS:528:DyaK1MXms12rtbw%3D 10.1006/jmbi.1999.3110 (Pubitemid 29516173)
11. HJ Dyson PE Wright 2002 Coupling of folding and binding for unstructured proteins Current Opinion in Structural Biology 12 54 60 1:CAS:528: DC%2BD38XhtF2it7c%3D 10.1016/S0959-440X(02)00289-0 (Pubitemid 34142721)
12. VN Uversky CJ Oldfield U Midic H Xie B Xue S Vucetic, et al. 2009 Unfoldomics of human diseases: Linking protein intrinsic disorder with diseases BMC Genomics 10 1 S7 10.1186/1471-2164-10-S1-S7
13. LM Iakoucheva CJ Brown JD Lawson Z Obradovic AK Dunker 2002 Intrinsic disorder in cell-signaling and cancer-associated proteins Journal of Molecular Biology 323 573 584 1:CAS:528:DC%2BD38XnslGrtLw%3D 10.1016/S0022-2836(02)00969-5 (Pubitemid 35283681)
14. E Schwob T Bohm M Mendenhall K Nasmyth 1994 The B-type cyclin kinase inhibitor p40SIC1 controls the G1 to S transition in S. cerevisiae Cell 79 233 244 1:CAS:528:DyaK2cXmslKnurc%3D 10.1016/0092-8674(94)90193-7 (Pubitemid 24324914)
15. MD Mendenhall AE Hodge 1998 Regulation of Cdc28 cyclin-dependent protein kinase activity during the cell cycle of the yeast Saccharomyces cerevisiae Microbiology and Molecular Biology Reviews 62 1191 1243 1:CAS:528: DyaK1MXhs1OnsA%3D%3D
16. R Verma RS Annan MJ Huddleston SA Carr G Reynard RJ Deshaies 1997 Phosphorylation of Sic1p by G1 Cdk required for its degradation and entry into S phase Science 278 455 460 1:CAS:528:DyaK2sXmslKit78%3D 10.1126/science.278. 5337.455 (Pubitemid 27454428)
17. RJ Deshaies JE Ferrell Jr 2001 Multisite phosphorylation and the countdown to S phase Cell 107 819 822 1:CAS:528:DC%2BD38XjtlKmsQ%3D%3D 10.1016/S0092-8674(01)00620-1 (Pubitemid 34084972)
18. A Hodge M Mendenhall 1999 The cyclin-dependent kinase inhibitory domain of the yeast Sic1 protein is contained within the C-terminal 70 amino acids Molecular and General Genetics 262 55 64 1:CAS:528:DyaK1MXmt1yitL4%3D 10.1007/s004380051059 (Pubitemid 29423902)
19. M Borg T Mittag T Pawson M Tyers JD Forman-Kay HS Chan 2007 Polyelectrostatic interactions of disordered ligands suggest a physical basis for ultrasensitivity Proceedings of the National Academy of Sciences of the United States of America 104 9650 9655 1:CAS:528:DC%2BD2sXmsFWjsbg%3D 10.1073/pnas.0702580104 (Pubitemid 47175321)
20. P Klein T Pawson M Tyers 2003 Mathematical modeling suggests cooperative interactions between a disordered polyvalent ligand and a single receptor site Current Biology 13 1669 1678 1:CAS:528:DC%2BD3sXnvVOmt7Y%3D 10.1016/j.cub.2003. 09.027 (Pubitemid 37216244)
21. X Escoté M Zapater J Clotet F Posas 2004 Hog1 mediates cell-cycle arrest in G1 phase by the dual targeting of Sic1 Nature Cell Biology 10 997 1002 10.1038/ncb1174 (Pubitemid 39359853)
22. S Brocca M Šamalikova VN Uversky M Lotti M Vanoni L Alberghina, et al. 2009 Order propensity of an intrinsically disordered protein, the cyclin-dependent-kinase inhibitor Sic1 Proteins 76 731 746 1:CAS:528: DC%2BD1MXns1ertL8%3D 10.1002/prot.22385
23. T Mittag S Orlicky WY Choy X Tang H Lin F Sicheri, et al. 2008 Dynamic equilibrium engagement of a polyvalent ligand with a single-site receptor Proceedings of the National Academy of Sciences of the United States of America 105 17772 17777 1:CAS:528:DC%2BD1cXhsVCmurzM 10.1073/pnas.0809222105
24. Sambrook, J., Fritsch, E. F., & Maniatis, T. (1989). Molecular cloning. A laboratory manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
25. I Matsumura LA Rowe 2005 Whole plasmid mutagenic PCR for directed protein evolution. Order propensity of a disordered protein, Sic1 Biomolecular Engineering 22 73 79 1:CAS:528:DC%2BD2MXjs1Ogs7k%3D 10.1016/j.bioeng.2004.10.004 (Pubitemid 40602596)
26. Hanahan, D. (1985). Techniques for transformation of E. coli. In D. M. Glover (Ed.), DNA cloning: A practical approach (p. 109). Mc Lean, VA: IRL press.
27. Promega Subcloning Notebook 44. http://www.promega.com./guides/ subcloning-guide/.
28. The Qiaexpressionist (June 2003). http://qiagen.com/literature/default.
29. UK Laemmli 1970 Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 227 680 685 1:CAS:528:DC%2BD3MXlsFags7s%3D 10.1038/227680a0
30. N Sreerama RW Woody 2000 Estimation of protein secondary structure from CD spectra: Comparison of CONTIN, SELCON and CDSSTR methods with an expanded reference set Analytical Biochemistry 282 252 260 10.1006/abio.2000.4880 (Pubitemid 32006234)
31. A Hodge M Mendenhall 1999 The cyclin-dependent kinase inhibitory domain of the yeast Sic1 protein is contained within the C-terminal 70 amino acids Molecular and General Genetics 1 55 64
32. P Tompa 2002 Intrinsically unstructured proteins Trends in Biochemical Sciences 27 527 533 1:CAS:528:DC%2BD38XnsVWqsbo%3D 10.1016/S0968-0004(02)02169-2 (Pubitemid 35279598)
33. MS Cortese JP Baird VN Uversky AK Dunker 2005 Uncovering the unfoldome: Enriching cell extracts for unstructured proteins by acids treatment Journal of Proteome Research 4 1610 1618 1:CAS:528:DC%2BD2MXmsVylsrk%3D 10.1021/pr050119c (Pubitemid 41464787)
34. V Csizmok E Szollosi P Friedriich P Tompa 2006 A novel two-dimensional electrophoresis technique for the identification of intrinsically unstructured proteins Molecular and Cellular Proteomics 5 265 273 1:CAS:528: DC%2BD28XitVagsLs%3D 10.1074/mcp.M500181-MCP200 (Pubitemid 43329305)
35. CA Galea VR Pagala JC Obenauer CG Park CA Slaughter RW Kriwacki 2006 Proteomic studies of the intrinsically unstructured mammalian proteome Journal of Proteome Research 5 2839 2848 1:CAS:528:DC%2BD28XpsleitLg%3D 10.1021/pr060328c (Pubitemid 44595184)
36. F Frottin A Martinez P Peynot S Mitra RC Holz C Giglione, et al. 2006 The proteomics of N-terminal methionine cleavage Molecular and Cellular Proteomics 5 2336 2349 1:CAS:528:DC%2BD28XhtlCgu7zJ 10.1074/mcp.M600225-MCP200 (Pubitemid 46040638)
37. Woody, R. W. (2009). Circular dichroism of intrinsically disordered proteins. In V. N. Uversky, S. Longhi (Eds.), Instrumental analysis of intrinsically disordered proteins: Assessing structure and conformation (pp. 303-321). New York, NY: John Wiley and Sons Ltd.
38. Mulder, F. A. A., Lundqvist, M., & Scheek, R. (2009). Nuclear magnetic resonance spectroscopy applied to (intrinsically) disordered proteins. In V. N. Uversky, S. Longhi (Eds.), Instrumental analysis of intrinsically disordered proteins: Assessing structure and conformation (pp. 61-87). New York, NY: John Wiley and Sons Ltd.
39. DL Crimmins JL Kao 2007 The human cardiac hormone fragment N-terminal pro B-type natriuretic peptide is an intrinsically unstructured protein Archives of Biochemistry and Biophysics 461 242 246 1:CAS:528:DC%2BD2sXkvFOrsbc%3D 10.1016/j.abb.2007.02.024 (Pubitemid 46677891)
40. E Hébrard Y Bessin T Michon S Longhi VN Uversky F Delalande A Van Dorsselaer P Romero J Walter N Declerck D Fargette 2009 Intrinsic disorder in viral proteins genome-linked: Experimental and predictive analyses Virology Journal 16 6 23
41. P Tompa M Fuxreiter CJ Oldfield I Simon AK Dunker VN Uversky 2009 Close encounters of the third kind: disordered domains and the interactions of proteins Bioessays 31 328 335 1:CAS:528:DC%2BD1MXkslGktbk%3D 10.1002/bies.200800151
42. CA Galea A Nourse Y Wang SG Sivakolundu WT Heller RW Kriwacki 2008 Role of intrinsic flexibility in signal transduction mediated by the cell cycle regulator, p27Kip1 Journal of Molecular Biology 376 3 827 838 1:CAS:528:DC%2BD1cXhsVSnsbY%3D 10.1016/j.jmb.2007.12.016