Intramolecular interactions stabilizing compact conformations of the intrinsically disordered kinase-inhibitor domain of Sic1: A molecular dynamics investigation

Frontiers in Physiology

Volumn 3 NOV, Issue , 2012, Pages

  Lambrughi, Matteo ^a   Papaleo, Elena ^a   Testa, Lorenzo ^a   Brocca, Stefania ^a   De Gioia, Luca ^a   Grandori, Rita ^a  

^a UNIVERSITY OF MILANO BICOCCA   (Italy)

Author keywords

Cyclin dependent kinase; Electrostatic interactions; Intrinsically disordered proteins; Molecular; Sic1

Indexed keywords

EID: 84870871174     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2012.00435     Document Type: Article

References (92)

1. Altis, A., Otten, M., Phuong, H., Nguyen, P. H., Hegger, R., and Stock, G. (2008). Construction of the free energy landscape of biomolecules via dihedral angle principal component analysis. J. Chem. Phys. 128, 245102.
2. Amadei, A., Ceruso, M. A., and Nola, A. D. (1999). On the convergence of the conformational coordinates basis set obtained by the essen- tial dynamics analysis of proteins' molecular dynamics simulations. Proteins 36, 419-424.
3. Amadei, A., Linssen, A. B., and Berendsen, H. J. (1993). Essential dynamics of proteins. Proteins 17, 412-425.
4. Angelova, K., Felline, A., Lee, M., Patel, M., Puett, D., and Fanelli, F. (2011). Conserved amino acids participate in the structure networks deputed to intramolecular communication in the lutropin receptor. Cell. Mol. Life Sci. 68, 1227-1239.
5. Arrigoni, A., Grillo, B., Vitriolo, A., De Gioia, L., and Papaleo, E. (2012). C-terminal acidic domain of ubiquitin-conjugating enzymes: a multi-functional conserved intrinsi- cally disordered domain in family 3 of E2 enzymes. J. Struct. Biol. 178, 245-259.
6. Barberis, M. (2012). Sic1 as a timer of Clb cyclin waves in the yeast cell cycle - design principle of notjustaninhibitor.FEBS J. 279, 3386-3410.
7. Barberis, M., De Gioia, L., Ruzzene, M., Sarno, S., Coccetti, P., Fantucci, P., et al. (2005). The yeast cyclin- dependent kinase inhibitor Sic1 and mammalian p27Kip1 are functional homologues with a structurally conserved inhibitory domain. Biochem. J. 387, 639-647.
8. Barberis, M., Klipp, E., Vanoni, M., and Alberghina, L. (2007). Cell size at S phase initiation: an emer- gent property of the G1/S net- work. PLoS Comput. Biol. 3:e64. doi: 10.1371/journal.pcbi.0030064
9. Barberis, M., Linke, C., Adrover, M. A., Gonzalez-Novo, A., Lehrach, H., Krobitsch, S., et al. (2012). Sic1 plays a role in timing and oscillatory behaviour of B- type cyclins. Biotechnol. Adv. 30, 108-130.
10. Belle, V., Rouger, S., Costanzo, S., Liquiere, E., Strancar, J., Guigliarelli, B., et al. (2008). Mapping alpha- helical induced folding within the intrinsically disordered C- terminal domain of the measles virus nucleoprotein by site-directed spin-labeling EPR spectroscopy. Proteins 73, 973-988.
11. Bernado, P., and Svergun, D. I. (2012). Structural analysis of intrinsically disordered proteins by small-angle X-ray scattering. Mol. Biosyst. 8, 151-167.
12. Besson,A.,Dowdy,S.F.,andRoberts, J. M. (2008). CDK inhibitors: cell cycle regulators and beyond. Dev. Cell 14, 159-169.
13. Brinda, K. V., and Vishveshwara, S. (2005). A network representation of protein structures: implications for protein stability. Biophys. J. 89, 4159-4170.
14. Brocca, S., Samalikova, M., Uversky, V. N., Lotti, M., Vanoni, M., Alberghina, L., et al. (2009). Order propensity of an intrin- sically disordered protein, the cyclin-dependent-kinase inhibitor Sic1. Proteins 76, 731-746.
15. Brocca, S., Testa, L., Samalikova, M., Grandori, R., and Lotti, M. (2011a). Defining structural domains of an intrinsically disordered pro- tein: Sic1, the cyclin-dependent kinase inhibitor of Saccharomyces cerevisiae. Mol. Biotechnol. 47, 34-42.
16. Brocca, S., Testa, L., Sobott, F., Samalikova, M., Natalello, A., Papaleo, E., Lotti, M., et al. (2011b). Compaction properties of an intrinsically disordered protein: Sic1 and its kinase-inhibitor domain. Biophys. J. 100, 2243-2252.
17. Brunger, A. T. (2007). Version 1.2 of the crystallography and NMR system. Nat. Protoc. 2, 2728-2733.
18. Cino, E. A., Wong-ekkabut, J., Karttunen, M., and Choy, W. Y. (2011). Microsecond molec- ular dynamics simulations of intrinsically disordered proteins involved in the oxidative stress response. PLoS ONE 6:e27371. doi: 10.1371/journal.pone.0027371
19. Click, T. H., Ganguly, D., and Chen, J. (2010). Intrinsically disordered pro- teins in a physics-based world. Int. J. Mol. Sci. 11, 5292-5309.
20. Coccetti, P., Rossi, R. L., Sternieri, F., Porro, D., Russo, G. L., Di Fonzo, A., et al. (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.
21. Cormen, T. H., Leiserson, C. E., Rivest, R. L., and Clifford, S. (2009). Introduction to Algorithms. 3rd Edn. Vol. 1, Cambridge, MA: MIT Press, 1292.
22. Darden, T., York, D., and Pedersen, L. (1993). Particle mesh Ewald- an N.LOG(N) method for Ewald sums in large systems. J. Chem. Phys. 98, 10089-10092.
23. Deshaies, R. J., and Ferrell, J. E. Jr. (2001). Multisite phosphorylation and the countdown to S phase. Cell 107, 819-822.
24. Dobo, A., and Kaltashov, I. A. (2001). Detection of multiple protein con- formational ensembles in solution via deconvolution of charge-state distributions in ESI MS. Anal. Chem. 73, 4763-4773.
25. Dunker, A. K., Silman, I., Uversky, V. N., and Sussman, J. L. (2008). Function and structure of inher- ently disordered proteins. Curr. Opin. Struct. Biol. 18, 756-764.
26. Dyson, H. J., and Wright, P. E. (2005). Intrinsically unstructured proteins and their functions. Nat. Rev. Mol. Cell Biol. 6, 197-208.
27. Escote, X., Zapater, M., Clotet, J., and Posas, F. (2004). Hog1 mediates cell- cycle arrest in G1 phase by the dual targeting of Sic1. Nat. Cell Biol. 6, 997-1002.
28. Espinoza-Fonseca, L. M. (2009a). Leucine-rich hydrophobic clus- ters promote folding of the N-terminus of the intrinsi- cally disordered transactivation domain of p53. FEBS Lett. 583, 556-560.
29. Espinoza-Fonseca, L. M. (2009b). Reconciling binding mechanisms of intrinsically disordered proteins. Biochem. Biophys. Res. Commun. 382, 479-482.
30. Espinoza-Fonseca, L. M. (2012). Dynamic optimization of signal transduction via intrinsic disorder. Mol. Biosyst. 8, 194-197.
31. Espinoza-Fonseca, L. M., Ilizaliturri- Flores, I., and Correa-Basurto, J. (2012). Backbone conformational preferences of an intrinsically dis- ordered protein in solution. Mol. Biosyst. 8, 1798-1805.
32. Espinoza-Fonseca, L. M., Kast, D., and Thomas, D. D. (2007). Molecular dynamics simulations reveal a disorder-to-order transition on phosphorylation of smooth muscle myosin. Biophys. J. 93, 2083-2090.
33. Espinoza-Fonseca, L. M., Kast, D., and Thomas, D. D. (2008). Thermodynamic and structural basis of phosphorylation-induced disorder-to-order transition in the regulatory light chain of smooth muscle myosin. J. Am. Chem. Soc. 130, 12208-12209.
34. Esteban-Martin, S., Fenwick, R. B., and Salvatella, X. (2012). Synergistic use of NMR and MD simulations to study the structural heterogeneity of proteins. Wiley Interdiscip. Rev. Comput.Mol.Sci.2, 466-478.
35. Eswar,N.,Eramian,D.,Webb,B., Shen, M. Y., and Sali, A. (2008). Protein structure modeling with MODELLER. Methods Mol. Biol. 426, 145-159.
36. Fisher, C. K., and Stultz, C. M. (2011). Constructing ensembles for intrin- sically disordered proteins. Curr. Opin. Struct. Biol. 21, 426-431.
37. Fuhrmans, M., Sanders, B. P., Marrink, S. J., and de Vries, A. H. (2010). Effects of bundling on the properties of the SPC water model. Theor. Chem. Acc. 125, 335-344.
38. Galea, C. A., Wang, Y., Sivakolundu, S. G., and Kriwacki, R. W. (2008). Regulation of cell division by intrinsically unstructured proteins: intrinsic flexibility, modularity, and signaling conduits. Biochemistry 47, 7598-7609.
39. Ganguly,D.,Zhang,W.,andChen, J. (2012). Synergistic folding of two intrinsically disordered pro- teins: searching for conformational selection. Mol. Biosyst. 8, 198-209.
40. Gardebien, F., Thangudu, R. R., Gontero, B., and Offmann, B. (2006). Construction of a 3D model of CP12, a protein linker. J. Mol. Graph. Model. 25, 186-195.
41. Hazy, E., and Tompa, P. (2009). Limitations of induced fold- ing in molecular recognition by intrinsically disordered proteins. Chemphyschem 10, 1415-1419.
42. Hess, B. (2002). Convergence of sam- pling in protein simulations. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 65, 031910.
43. Hess, B., Bekker, H., Berendsen, H. J. C., and Fraaije, J. (1997). LINCS: a linear constraint solver for molec- ular simulations. J. Comput. Chem. 18, 1463-1472.
44. Hodge, A., and Mendenhall, M. (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.
45. Johnson, L. N., and Lewis, R. J. (2001). Structural basis for con- trol by phosphorylation. Chem. Rev. 101, 2209-2242.
46. Kabsch, W., and Sander, C. (1983). Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geomet- rical features. Biopolymers 22, 2577-2637.
47. Kaltashov, I. A., and Abzalimov, R. R. (2008). Do ionic charges in ESI MS provide useful information on macromolecular structure? J. Am. Soc. Mass Spectrom. 19, 1239-1246
48. Keller, B., Daura, X., and van Gunsteren, W. F. (2010). Comparing geometric and kinetic cluster algo- rithms for molecular simulation data. J. Chem. Phys. 132, 074110.
49. Kjaergaard, M., Teilum, K., and Poulsen, F. M. (2010). Conformational selection in the molten globule state of the nuclear coactivator binding domain of CBP. Proc. Natl. Acad. Sci. U.S.A. 107, 12535-12540.
50. Knott, M., and Best, R. B. (2012). A preformed binding interface in the unbound ensemble of an intrinsi- cally disordered protein: evidence from molecular simulations. PLoS Comput. Biol. 8:e1002605. doi: 10.1371/journal.pcbi.1002605
51. Koivomagi, M., Valk, E., Venta, R., Iofik, A., Lepiku, M., Balog, E. R., et al. (2011). Cascades of multi- site phosphorylation control Sic1 destruction at the onset of S phase. Nature 480, 128-131.
52. Lindorff-Larsen, K., Trbovic, N., Maragakis, P., Piana, S., and Shaw, D. E. (2012). Structure and dynamics of an unfolded protein examined by molecular dynamics simulation. J. Am. Chem. Soc. 134, 3787-3791.
53. Lopez-Aviles, S., Kapuy, O., Novak, B., and Uhlmann, F. (2009). Irreversibility of mitotic exit is the consequence of systems-level feedback. Nature 459, 592-595.
54. Mao, A. H., Crick, S. L., Vitalis, A., Chicoine, C. L., and Pappu, R. V. (2010). Net charge per residue modulates conformational ensem- bles of intrinsically disordered pro- teins. Proc. Natl. Acad. Sci. U.S.A. 107, 8183-8188.
55. Marsh, J. A., Neale, C., Jack, F. E., Choy,W.Y.,Lee,A.Y.,Crowhurst, K. A., et al. (2007). Improved struc- tural characterizations of the drkN SH3 domain unfolded state suggest a compact ensemble with native-like and non-native structure. J. Mol. Biol. 367, 1494-1510.
56. Matthes, D., and De Groot, B. L. (2009). Secondary structure propensities in peptide folding simulations: a sys- tematic comparison of molecu- lar mechanics interaction schemes. Biophys. J. 97, 599-608.
57. Mendenhall, M. D., and Hodge, A. E. (1998). Regulation of Cdc28 cyclin-dependent protein kinase activity during the cell cycle of the yeast Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 62, 1191-1243.
58. Meszaros, B., Simon, I., and Dosztanyi, Z. (2011). The expanding view of protein-protein interactions: com- plexes involving intrinsically disor- dered proteins. Phys. Biol. 8, 035003
59. Mittag, T., Orlicky, S., Choy, W. Y., Tang, X., Lin, H., Sicheri, F., et al. (2008). Dynamic equilibrium engagement of a polyvalent lig- and with a single-site receptor. Proc. Natl. Acad. Sci. U.S.A. 105, 17772-17777.
60. Morin,B.,Bourhis,J.M.,Belle, V., Woudstra, M., Carriere, F., Guigliarelli, B., et al. (2006). Assessing induced folding of an intrinsically disordered protein by site-directed spin-labeling electron paramagnetic resonance spec- troscopy. J. Phys. Chem. B 110, 20596-20608.
61. Nash,P.,Tang,X.,Orlicky,S.,Chen, Q.,Gertler,F.B.,Mendenhall,M. D., et al. (2001). Multisite phos- phorylation of a CDK inhibitor sets a threshold for the onset of DNA replication. Nature 414, 514-521.
62. Norholm, A.-B., Hendus-Altenburger, R., Bjerre, G., Kjaergaard, M., Pedersen, S. F., and Kragelund, B. B. (2011). The intracellular distal tail of the Na(+)/H(+) exchanger NHE1 Is intrinsically disordered: implications for NHE1 trafficking. Biochemistry 50, 3469-3480.
63. Oldfield, C. J., Cheng, Y., Cortese, M. S.,Brown,C.J.,Uversky,V.N.,and Dunker, A. K. (2005). Comparing and combining predictors of mostly disordered proteins. Biochemistry 44, 1989-2000.
64. Otieno, S., Grace, C. R., and Kriwacki, R. W. (2011). The role of the LH subdomain in the function of the Cip/Kip cyclin-dependent kinase regulators. Biophys. J. 100, 2486-2494.
65. Papaleo, E., Mereghetti, P., Fantucci, P.,Grandori,R.,andDeGioia, L. (2009). Free-energy landscape, principal component analysis, and structural clustering to identify representative conformations from molecular dynamics simulations: the myoglobin case. J. Mol. Graph. Model. 27, 889-899.
66. Pasi, M., Tiberti, M., Arrigoni, A., and Papaleo, E. (2012). xPyder: a PyMOL plugin to analyze coupled residues and their networks in pro- tein structures. J.Chem.Inf.Model. 52, 1865-1874.
67. Qin, Z., Kalinowski, A., Dahl, K. N., and Buehler, M. J. (2011). Structure and stability of the lamin A tail domain and HGPS mutant. J. Struct. Biol. 175, 425-433.
68. Rauscher, S., and Pomes, R. (2010). Molecular simulations of protein disorder. Biochem. Cell Biol. 88, 269-290.
69. Receveur-Bréchot, V., Bourhis, J. M., Uversky, V. N., Canard, B., and Longhi, S. (2006). Assessing pro- tein disorder and induced folding. Proteins 62, 24-45.
70. Russo,A.A.,Jeffrey,P.D.,Patten,A. K., Massague, J., and Pavletich, N. P. (1996). Crystal structure of the p27Kip1 cyclin-dependent-kinase inhibitor bound to the cyclin A-Cdk2 complex. Nature 382, 325-331.
71. Salmon, L., Nodet, G., Ozenne, V., Yin, G., Jensen, M. R., Zweckstetter, M., et al. (2010). NMR characterization of long-range order in intrinsically disordered proteins. J. Am. Chem. Soc. 132, 8407-8418.
72. Schneider, R., Huang, J.-R., Yao, M., Communie, G., Ozenne, V., Mollica, L., et al. (2012). Towards a robust description of intrinsic protein dis- order using nuclear magnetic reso- nance spectroscopy. Mol. Biosyst. 8, 58-68.
73. Schwob, E., Bohm, T., Mendenhall, M. D., and Nasmyth, K. (1994). The B-type cyclin kinase inhibitor p40SIC1 controls the G1 to S transition in S. cerevisiae. Cell 79, 233-244.
74. Sivakolundu, S. G., Bashford, D., and Kriwacki, R. W. (2005). Disordered p27(Kip1) exhibits intrinsic struc- ture resembling the Cdk2/cyclin A- bound conformation. J. Mol. Biol. 353, 1118-1128.
75. Szasz, C., Alexa, A., Toth, K., Rakacs, M., Langowski, J., and Tompa, P. (2011). Protein disorder pre- vails under crowded conditions. Biochemistry 50, 5834-5844.
76. Testa, L., Brocca, S., and Grandori, R. (2011a). Charge-surface correlation in electrospray ionization of folded andunfoldedproteins.Anal. Chem. 83, 6459-6463.
77. Testa, L., Brocca, S., Samalikova, M., Santambrogio, C., Alberghina, L., and Grandori, R. (2011b). Electrospray ionization-mass spec- trometry conformational analysis of isolated domains of an intrinsically disordered protein. Biotechnol. J. 6, 96-100.
78. Tiberti, M., and Papaleo, E. (2011). Dynamic properties of extremophilic subtilisin-like serine- proteases. J. Struct. Biol. 174, 69-83.
79. Tompa, P. (2005). The inter- play between structure and function in intrinsically unstruc- tured proteins. FEBS Lett. 579, 3346-3354.
80. Tompa, P., and Fuxreiter, M. (2008). Fuzzy complexes: polymor- phism and structural disorder in protein-protein interactions. Trends Biochem. Sci. 33, 2-8.
81. Toyoshima, H., and Hunter, T. (1994). p27, a novel inhibitor of G1 cyclin-Cdk protein kinase activ- ity, is related to p21. Cell 78, 67-74.
82. Turoverov, K. K., Kuznetsova, I. M., and Uversky, V. N. (2010). The protein kingdom extended: ordered and intrinsically disordered pro- teins, their folding, supramolecular complex formation, and aggrega- tion. Prog. Biophys. Mol. Biol. 102, 73-84.
83. Uversky, V. N. (2002). Natively unfolded proteins: a point where biology waits for physics. Protein Sci. 11, 739-756.
84. Uversky,V.N.,andDunker,A.K. (2010). Understanding protein non-folding. Biochim. Biophys. Acta 1804, 1231-1264.
85. Uversky, V. N., Gillespie, J. R., and Fink, A. L. (2000). Why are "natively unfolded" proteins unstructured under physio- logic conditions? Proteins 41, 415-427.
86. Verma, R., Feldman, R. M., and Deshaies, R. J. (1997). SIC1 is ubiquitinated in vitro by a pathway that requires CDC4, CDC34, and cyclin/CDK activities. Mol. Biol. Cell 8, 1427-1437.
87. Vishveshwara, S., Ghosh, A., and Hansia, P. (2009). Intra and inter-molecular communications through protein structure network. Curr. Protein Pept. Sci. 10, 146-160.
88. Wostenberg, C., Kumar, S., Noid, W. G., and Showalter, S. A. (2011). Atomistic simulations reveal struc- tural disorder in the RAP74-FCP1 complex. J. Phys. Chem. B 115, 13731-13739.
89. Wright, P. E., and Dyson, H. J. (2009). Linking folding and binding. Curr. Opin. Struct. Biol. 19, 31-38.
90. Yaakov, G., Duch, A., Garcia-Rubio, M., Clotet, J., Jimenez, J., Aguilera, A., et al. (2009). The stress-activated protein kinase Hog1 mediates S phase delay in response to osmostress. Mol. Biol. Cell 20, 3572-3582.
91. Yoon, M.-K., Venkatachalam, V., Huang, A., Choi, B.-S., Stultz, C. M., and Chou, J. J. (2009). Residual structure within the dis- ordered C-terminal segment of p21(Waf1/Cip1/Sdi1) and its impli- cations for molecular recognition. Protein Sci. 18, 337-347.
92. Zhuravlev, P. I., Materese, C. K., and Papoian, G. A. (2009). Deconstructing the native state: energy landscapes, function, and dynamics of globular proteins. J. Phys. Chem. B 113, 8800-8812.