Compaction properties of an intrinsically disordered protein: Sic1 and its kinase-inhibitor domain

Biophysical Journal

Volumn 100, Issue 9, 2011, Pages 2243-2252

  Brocca, Stefania ^a   Testa, Lorenzo ^a   Sobott, Frank ^b   Šamalikova, Maria ^a   Natalello, Antonino ^a   Papaleo, Elena ^a   Lotti, Marina ^a   De Gioia, Luca ^a   Doglia, Silvia Maria ^a   Alberghina, Lilia ^a   Grandori, Rita ^a  

^a UNIVERSITY OF MILANO BICOCCA   (Italy)

^b UNIVERSITY OF ANTWERP   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

SACCHAROMYCES CEREVISIAE;

EID: 79959728779     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2011.02.055     Document Type: Article

References (52)

1. Alfieri, R., M. Barberis,..., L. Alberghina. 2009. Towards a systems biology approach to mammalian cell cycle: modeling the entrance into S phase of quiescent fibroblasts after serum stimulation. BMC Bioinformatics. 10(Suppl 12):S16.
2. Fink, A. L. 2005. Natively unfolded proteins. Curr. Opin. Struct. Biol. 15:35-41. (Pubitemid 40249507)
3. Turoverov, K. K., I. M. Kuznetsova, and V. N. Uversky. 2010. The protein kingdom extended: ordered and intrinsically disordered proteins, their folding, supramolecular complex formation, and aggregation. Prog. Biophys. Mol. Biol. 102:73-84.
4. Galea, C. A., Y. Wang,..., R. W. Kriwacki. 2008. Regulation of cell division by intrinsically unstructured proteins: intrinsic flexibility, modularity, and signaling conduits. Biochemistry. 47:7598-7609. (Pubitemid 352019491)
5. Schnell, S., S. Fortunato, and S. Roy. 2007. Is the intrinsic disorder of proteins the cause of the scale-free architecture of protein-protein interaction networks? Proteomics. 7:961-964. (Pubitemid 46506742)
6. Eliezer, D. 2009. Biophysical characterization of intrinsically disordered proteins. Curr. Opin. Struct. Biol. 19:23-30.
7. Brocca, S., M. Samalíková,..., R. Grandori. 2009. Order propensity of an intrinsically disordered protein, the cyclin-dependent-kinase inhibitor Sic1. Proteins. 76:731-746.
8. Galea, C. A., A. Nourse,..., R. W. Kriwacki. 2008. Role of intrinsic flexibility in signal transduction mediated by the cell cycle regulator, p27 Kip1. J. Mol. Biol. 376:827-838.
9. Tran, H. T., A. Mao, and R. V. Pappu. 2008. Role of backbone-solvent interactions in determining conformational equilibria of intrinsically disordered proteins. J. Am. Chem. Soc. 130:7380-7392. (Pubitemid 351813231)
10. Mittag, T., J. Marsh,..., J. D. Forman-Kay. 2010. Structure/function implications in a dynamic complex of the intrinsically disordered Sic1 with the Cdc4 subunit of an SCF ubiquitin ligase. Structure. 18:494-506.
11. Ganguly, D., and J. Chen. 2009. Atomistic details of the disordered states of KID and pKID. Implications in coupled binding and folding. J. Am. Chem. Soc. 131:5214-5223.
12. Salmon, L., G. Nodet,..., M. Blackledge. 2010. NMR characterization of long-range order in intrinsically disordered proteins. J. Am. Chem. Soc. 132:8407-8418.
13. Natalello, A., F. Benetti,..., R. Grandori. 2011. Compact conformations of a-synuclein induced by alcohols and copper. Proteins. 79:611-621.
14. Deshaies, R. J. 1997. Phosphorylation and proteolysis: partners in the regulation of cell division in budding yeast. Curr. Opin. Genet. Dev. 7:7-16. (Pubitemid 27092758)
15. Deshaies, R. J., and J. E. Ferrell, Jr. 2001. Multisite phosphorylation and the countdown to S phase. Cell. 107:819-822. (Pubitemid 34084972)
16. Lopez-Aviles, S., O. Kapuy,..., F. Uhlmann. 2009. Irreversibility of mitotic exit is the consequence of systems-level feedback. Nature. 459:592-595.
17. Coccetti, P., R. L. Rossi,..., L. Alberghina. 2004. Mutations of the CK2 phosphorylation site of Sic1 affect cell size and S-Cdk kinase activity in Saccharomyces cerevisiae. Mol. Microbiol. 51:447-460. (Pubitemid 38145588)
18. Barberis, M., E. Klipp,..., L. Alberghina. 2007. Cell size at S phase initiation: an emergent property of the G1/S network. PLOS Comput. Biol. 3:e64.
19. Yaakov, G., A. Duch,..., F Posas. 2009. The stress-activated protein kinase Hog1 mediates S phase delay in response to osmostress. Mol. Biol. Cell. 20:3572-3582.
20. Hodge, A., and M. Mendenhall. 1999. The cyclin-dependent kinase inhibitory domain of the yeast Sic1 protein is contained within the C-terminal 70 amino acids. Mol. Gen. Genet. 262:55-64. (Pubitemid 29423902)
21. Brocca, S., L. Testa,..., M. Lotti. 2011. Defining structural domains of an intrinsically disordered protein: Sic1, the cyclin-dependent kinase inhibitor of Saccharomyces cerevisiae. Mol. Biotechnol. 47:34-42.
22. Testa, L., S. Brocca,..., R. Grandori. 2011. Electrospray ionizationmass spectrometry conformational analysis of isolated domains of an intrinsically disordered protein. Biotechnol. J. 6:96-100.
23. Barberis, M., L. De Gioia,..., L. Alberghina. 2005. The yeast cyclindependent kinase inhibitor Sic1 and mammalian p27Kip1 are functional homologues with a structurally conserved inhibitory domain. Biochem. J. 387:639-647. (Pubitemid 40685697)
24. Russo, A. A., P. D. Jeffrey,..., N. P. Pavletich. 1996. Crystal structure of the p27Kip1 cyclin-dependent-kinase inhibitor bound to the cyclin A-Cdk2 complex. Nature. 382:325-331. (Pubitemid 26260452)
25. Sivakolundu, S. G., D. Bashford, and R. W. Kriwacki. 2005. Disordered p27Kip1 exhibits intrinsic structure resembling the Cdk2/cyclin Aβound conformation. J. Mol. Biol. 353:1118-1128. (Pubitemid 41503276)
26. Bowman, P., C. A. Galea,..., R. W. Kriwacki. 2006. Thermodynamic characterization of interactions between p27 (Kip1) and activated and non-activated Cdk2: intrinsically unstructured proteins as thermodynamic tethers. Biochim. Biophys. Acta. 1764:182-189.
27. Samalikova, M., C. Santambrogio, and R. Grandori. 2010. Mass-spectometry tools for the investigation of structural disorder and conformational transitions in proteins. In Instrumental Analysis of Intrinsically Disordered Proteins. V. N. Uversky and S. Longhi, editors. John Wiley & Sons, Hoboken, NJ. 629-652.
28. Kaltashov, I. A., and R. R. Abzalimov. 2008. Do ionic charges in ESI MS provide useful information on macromolecular structure? J. Am. Soc. Mass Spectrom. 19:1239-1246.
29. Borysik, A. J., S. E. Radford, and A. E. Ashcroft. 2004. Co-populated conformational ensembles of beta2-microglobulin uncovered quantitatively by electrospray ionization mass spectrometry. J. Biol. Chem. 279:27069-27077. (Pubitemid 38812543)
30. Smith, D. P., K. Giles,..., A. E. Ashcroft. 2007. Monitoring copopulated conformational states during protein folding events using electrospray ionization-ion mobility spectrometry-mass spectrometry. J. Am. Soc. Mass Spectrom. 18:2180-2190. (Pubitemid 350161334)
31. Smith, D. P., T. W. Knapman,..., A. E. Ashcroft. 2009. Deciphering drift time measurements from travelling wave ion mobility spectrometry-mass spectrometry studies. Eur. J. Mass Spectrom. (Chichester, Eng.). 15:113-130.
32. Uetrecht, C., R. J. Rose,..., A. J. Heck. 2010. Ion mobility mass spectrometry of proteins and protein assemblies. Chem. Soc. Rev. 39:1633-1655.
33. Mao, A. H., S. L. Crick,..., R. V. Pappu. 2010. Net charge per residue modulates conformational ensembles of intrinsically disordered proteins. Proc. Natl. Acad. Sci. USA. 107:8183-8188.
34. Marsh, J. A., and J. D. Forman-Kay. 2010. Sequence determinants of compaction in intrinsically disordered proteins. Biophys. J. 98:2383-2390.
35. Kyte, J., and R. F. Doolittle. 1982. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157:105-132.
36. Natalello, A., D. Ami,..., S. M. Doglia. 2005. Secondary structure, conformational stability and glycosylation of a recombinant Candida rugosa lipase studied by Fourier-transform infrared spectroscopy. Biochem. J. 385:511-517. (Pubitemid 40165084)
37. Vila, R., I. Ponte,..., P. Suau. 2001. Induction of secondary structure in a COOH-terminal peptide of histone H1 by interaction with the DNA: an infrared spectroscopy study. J. Biol. Chem. 276:30898-30903.
38. Irvine, G. B. 2001. Determination of molecular size by size-exclusion chromatography (gel filtration). Curr. Protoc. Cell. Biol., 5. 5.
39. Mohr, D., S. Frey,..., D. Görlich. 2009. Characterisation of the passive permeability barrier of nuclear pore complexes. EMBO J. 28:2541-2553.
40. Uversky, V. N. 1993. Use of fast protein size-exclusion liquid chromatography to study the unfolding of proteins which denature through the molten globule. Biochemistry. 32:13288-13298. (Pubitemid 24005939)
41. Uversky, V. N. 2002. What does it mean to be natively unfolded? Eur. J. Biochem. 269:2-12. (Pubitemid 34107333)
42. Uversky, V. N., J. R. Gillespie, and A. L. Fink. 2000. Why are "natively unfolded" proteins unstructured under physiologic conditions? Proteins. 41:415-427.
43. Müller-Späth, S., A. Soranno,..., B. Schuler. 2010. From the Cover: Charge interactions can dominate the dimensions of intrinsically disordered proteins. Proc. Natl. Acad. Sci. USA. 107:14609-14614.
44. Arrondo, J. L. R., and F. M. Goñi. 1999. Structure and dynamics of membrane proteins as studied by infrared spectroscopy. Prog. Biophys. Mol. Biol. 72:367-405.
45. Susi, H., and D. M. Byler. 1986. Resolution-enhanced Fourier transform infrared spectroscopy of enzymes. Methods Enzymol. 130:290-311.
46. Ashcroft, A. E. 2010. Mass spectrometry and the amyloid problem - how far can we go in the gas phase? J. Am. Soc. Mass Spectrom. 21:1087-1096.
47. Kuprowski, M. C., and L. Konermann. 2007. Signal response of coexisting protein conformers in electrospray mass spectrometry. Anal. Chem. 79:2499-2506. (Pubitemid 46449032)
48. Heck, A. J., and R. H. Van Den Heuvel. 2004. Investigation of intact protein complexes by mass spectrometry. Mass Spectrom. Rev. 23:368-389.
49. Bernadó, P., E. Mylonas,..., D. I. Svergun. 2007. Structural characterization of flexible proteins using small-angle X-ray scattering. J. Am. Chem. Soc. 129:5656-5664. (Pubitemid 46697655)
50. Brucale, M., M. Sandal,..., B. Samorì. 2009. Pathogenic mutations shift the equilibria of alpha-synuclein single molecules towards structured conformers. ChemBioChem. 10:176-183.
51. Nettels, D., S. Müller-Späth,..., B. Schuler. 2009. Single-molecule spectroscopy of the temperature-induced collapse of unfolded proteins. Proc. Natl. Acad. Sci. USA. 106:20740-20745.
52. Bernstein, S. L., D. Liu,..., J. R. Winkler. 2004. Alpha-synuclein: stable compact and extended monomeric structures and pH dependence of dimer formation. J. Am. Soc. Mass Spectrom. 15:1435-1443. (Pubitemid 39311694)