A Disorder-Induced Domino-Like Destabilization Mechanism Governs the Folding and Functional Dynamics of the Repeat Protein IκBα

PLoS Computational Biology

Volumn 9, Issue 12, 2013, Pages

  Sivanandan, Srinivasan ^a   Naganathan, Athi N ^b  

^a INDIAN INSTITUTE OF TECHNOLOGY   (India)

^b INDIAN INSTITUTE OF TECHNOLOGY MADRAS   (India)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SIGNALING; CONFORMATIONS; MAMMALS; PROTEINS; THERMODYNAMICS;

CELL-BE; CELL/B.E; CELL/BE; CELLULAR PROCESS; DESTABILIZATION MECHANISMS; DISORDERED REGIONS; FOLDINGS; MAMMALIAN CELLS; REPEAT PROTEINS; SIMPLE++;

CELL DEATH;

I KAPPA B ALPHA;

ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DEUTERIUM HYDROGEN EXCHANGE; DIFFERENTIAL SCANNING CALORIMETRY; FLUORESCENCE RESONANCE ENERGY TRANSFER; HALF LIFE TIME; MATHEMATICAL MODEL; PREDICTION; PROTEIN CONFORMATION; PROTEIN DEFECT; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN STABILITY; THERMODYNAMICS; VALIDATION PROCESS;

I-KAPPA B PROTEINS; MODELS, MOLECULAR; PROTEIN FOLDING; THERMODYNAMICS;

EID: 84892706842     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003403     Document Type: Article

References (59)

1. Courtois G, Gilmore TD, (2006) Mutations in the NF-kappa B signaling pathway: implications for human disease. Oncogene 25: 6831-6843.
2. Orange JS, Levy O, Geha RS, (2005) Human disease resulting from gene mutations that interfere with appropriate nuclear factor-kB activation. Immun Rev 203: 21-37.
3. Phelps CB, Sengchanthalangsy LL, Huxford T, Ghosh G, (2000) Mechanism of IκBα binding to NF-κB dimers. J Biol Chem 275: 29840-29846.
4. Bergqvist S, Croy CH, Kjaergaard M, Huxford T, Ghosh G, et al. (2006) Thermodynamics reveal that helix four in the NLS of NF-kappaB p65 anchors IkappaBalpha, forming a very stable complex. J Mol Biol pp. 421-434.
5. Cabannes E, Khan G, Aillet F, Jarrett RF, Hay RT, (1999) Mutations in the IkBa gene in Hodgkin's disease suggest a tumour suppressor role for IkBa. Oncogene 18: 3063-3070.
6. Huxford T, Huang DB, Malek S, Ghosh G, (1998) The crystal structure of the IkBa/NF-kB complex reveals mechanisms of NF-kB inactivation. Cell 95: 759-770.
7. Ferreiro DU, Komives EA, (2010) Molecular Mechanisms of System Control of NF-kappa B Signaling by I kappa B alpha. Biochemistry 49: 1560-1567.
8. Michel F, Soler-Lopez M, Petosa C, Cramer P, Siebenlist U, et al. (2001) Crystal structure of the ankyrin repeat domain of Bcl-3: a unique member of the IkB family. EMBO J 22: 6180-6190.
9. Pando MP, Verma IM, (2000) Signal-dependent and-independent degradation of free and NF-kB bound IkBa. J Biol Chem 275: 21278-21286.
10. Croy CH, Bergqvist S, Huxford T, Ghosh G, Komives EA, (2004) Biophysical characterization of the free I kappa B alpha ankyrin repeat domain in solution. Prot Sci 13: 1767-1777.
11. Truhlar SME, Torpey JW, Komives EA, (2006) Regions of I kappa B alpha that are critical for its inhibition of NF-kappa B- DNA interaction fold upon binding to NF-kappa B. Proc Natl Acad Sci USA 103: 18951-18956.
12. Truhlar SME, Mathes E, Cervantes CF, Ghosh G, Komives EA, (2008) Pre-folding I kappa B alpha alters control of NF-kappa B signaling. J Mol Biol 380: 67-82.
13. DeVries I, Ferreiro DU, Sanchez IE, Komives EA, (2011) Folding Kinetics of the Cooperatively Folded Subdomain of the IkB alpha Ankyrin Repeat Domain. J Mol Biol 408: 163-176.
14. Lamboy JA, Kim H, Lee KS, Ha T, Komives EA, (2011) Visualization of the nanospring dynamics of the I kappa B alpha ankyrin repeat domain in real time. Proc Natl Acad Sci USA 108: 10178-10183.
15. Lamboy JA, Kim H, Dembinski H, Ha T, Komives EA, (2013) Single-Molecule FRET Reveals the Native-State Dynamics of the IκBα Ankyrin Repeat Domain. J Mol Biol 425: 2578-2590.
16. Wako H, Saito N, (1978) Statistical Mechanical Theory of Protein Conformation.1. General Considerations and Application to Homopolymers. J Phys Soc Japan 44: 1931-1938.
17. Wako H, Saito N, (1978) Statistical Mechanical Theory of Protein Conformation.2. Folding Pathway for Protein. J Phys Soc Japan 44: 1939-1945.
18. Muñoz V, Eaton WA, (1999) A simple model for calculating the kinetics of protein folding from three-dimensional structures. Proc Natl Acad Sci USA 96: 11311-11316.
19. Naganathan AN, (2012) Predictions from an Ising-like Statistical Mechanical Model on the Dynamic and Thermodynamic Effects of Protein Surface Electrostatics. J Chem Theory Comput 8: 4646-4656.
20. Bruscolini P, Naganathan AN, (2011) Quantitative Prediction of Protein Folding Behaviors from a Simple Statistical Model. J Am Chem Soc 133: 5372-5379.
21. Naganathan AN, (2013) A Rapid, Ensemble and Free Energy Based Method for Engineering Protein Stabilities. J Phys Chem B 117: 4956-4964.
22. Kajander T, Cortajarena AL, Main ER, Mochrie SG, Regan L, (2005) A new folding paradigm for repeat proteins. J Am Chem Soc 127: 10188-10190.
23. Wetzel SK, Settanni G, Kenig M, Binz HK, Pluckthun A, (2008) Folding and unfolding mechanism of highly stable full-consensus ankyrin repeat proteins. J Mol Biol 376: 241-257.
24. Ferreiro DU, Walczak AM, Komives EA, Wolynes PG, (2008) The energy landscapes of repeat-containing proteins: Topology, cooperativity, and the folding funnels of one-dimensional architectures. PLOS Comp Biol 4: e1000070.
25. Street TO, Barrick D, (2009) Predicting repeat protein folding kinetics from an experimentally determined folding energy landscape. Prot Sci 18: 58-68.
26. Aksel T, Barrick D, (2009) Analysis of repeat-protein folding using nearest-neighbor statistical mechanical models. Methods Enzymol 455: 95-125.
27. Faccin M, Bruscolini P, Pelizzola A, (2011) Analysis of the equilibrium and kinetics of the ankyrin repeat protein myotrophin. J Chem Phys 134: 075102.
28. Bryngelson JD, Onuchic JN, Socci ND, Wolynes PG, (1995) Funnels, Pathways, and the Energy Landscape of Protein-Folding- a Synthesis. Proteins 21: 167-195.
29. Garcia-Mira MM, Sadqi M, Fischer N, Sanchez-Ruiz JM, Muñoz V, (2002) Experimental identification of downhill protein folding. Science 298: 2191-2195.
30. Kubelka J, Henry ER, Cellmer T, Hofrichter J, Eaton WA, (2008) Chemical, physical, and theoretical kinetics of an ultrafast folding protein. Proc Natl Acad Sci USA 105: 18655-18662.
31. Imparato A, Pelizzola A, Zamparo M, (2007) Ising-like model for protein mechanical unfolding. Phys Rev Lett 98: 148102.
32. Aioanei D, Brucale M, Tessari I, Bubacco L, Samori B, (2012) Worm-like Ising model for protein mechanical unfolding under the effect of osmolytes. Biophys J 102: 342-350.
33. Caraglio M, Pelizzola A, (2012) Effects of confinement on thermal stability and folding kinetics in a simple Ising-like model. Phys Biol 9: 016006.
34. Robertson AD, Murphy KP, (1997) Protein structure and the energetics of protein stability. Chem Rev 97: 1251-1267.
35. Flory P (1989) Statistical Mechanics of Chain Molecules. New York: Interscience.
36. Soranno A, Buchli B, Nettels D, Cheng RR, Muller-Spath S, et al. (2012) Quantifying internal friction in unfolded and intrinsically disordered proteins with single-molecule spectroscopy. Proc Natl Acad Sci USA 109: 17800-17806.
37. Ferreiro DU, Cervantes CF, Truhlar SME, Cho SS, Wolynes PG, et al. (2007) Stabilizing I kappa B alpha by "consensus" design. J Mol Biol 365: 1201-1216.
38. Low C, Weininger U, Neumann P, Klepsch M, Lilie H, et al. (2008) Structural insights into an equilibrium folding intermediate of an archaeal ankyrin repeat protein. Proc Natl Acad Sci USA 105: 3779-3784.
39. Naganathan AN, Perez-Jimenez R, Sanchez-Ruiz JM, Muñoz V, (2005) Robustness of downhill folding: Guidelines for the analysis of equilibrium folding experiments on small proteins. Biochemistry 44: 7435-7449.
40. Naganathan AN, Li P, Perez-Jimenez R, Sanchez-Ruiz JM, Muñoz V, (2010) Navigating the downhill protein folding regime via structural homologues. J Am Chem Soc 132: 11183-11190.
41. Ternstrom T, Mayor U, Akke M, Oliveberg M, (1999) From snapshot to movie: phi analysis of protein folding transition states taken one step further. Proc Natl Acad Sci USA 96: 14854-14859.
42. Sanchez IE, Kiefhaber T, (2003) Hammond behavior versus ground state effects in protein folding: evidence for narrow free energy barriers and residual structure in unfolded states. J Mol Biol 327: 867-884.
43. Lapidus LJ, Steinbach PJ, Eaton WA, Szabo A, Hofrichter J, (2002) Effects of chain stiffness on the dynamics of loop formation in polypeptides. Appendix: Testing a 1-dimensional diffusion model for peptide dynamics. J Phys Chem B 106: 11628-11640.
44. Bradley CM, Barrick D, (2006) The notch ankyrin domain folds via a discrete, centralized pathway. Structure 14: 1303-1312.
45. Forrer P, Binz HK, Stumpp MT, Plückthun A, (2004) Consensus design of repeat proteins. ChemBioChem 5: 183-189.
46. Kajander T, Cortajarena AL, Regan L, (2006) Consensus design as a tool for engineering repeat proteins. Methods Mol Biol 340: 151-170.
47. Tripp KW, Barrick D, (2007) Enhancing the stability and folding rate of a repeat protein through the addition of consensus repeats. J Mol Biol 365: 1187-1200.
48. Javadi Y, Main ERG, (2009) Exploring the folding energy landscape of a series of designed consensus tetratricopeptide repeat proteins. Proc Natl Acad Sci USA 106: 17383-17388.
49. Hagai T, Azia A, Trizac E, Levy Y, (2012) Modulation of Folding Kinetics of Repeat Proteins: Interplay between Intra- and Interdomain Interactions. Biophys J 103: 1555-1565.
50. Street TO, Bradley CM, Barrick D, (2007) Predicting coupling limits from an experimentally determined energy landscape. Proc Natl Acad Sci USA 104: 4907-4912.
51. Gsponer J, Futschik ME, Teichmann SA, Babu MM, (2008) Tight regulation of unstructured proteins: from transcript synthesis to protein degradation. Science 322: 1365-1368.
52. Li P, Oliva FY, Naganathan AN, Muñoz V, (2009) Dynamics of one-state downhill protein folding. Proc Natl Acad Sci USA 106: 103-108.
53. Kaya H, Chan HS, (2003) Origins of Chevron Rollovers in Non-Two-State Protein Folding Kinetics. Phys Rev Lett 90: 258104.
54. Hagai T, Levy Y, (2008) Folding of Elongated Proteins: Conventional or Anomalous? J Am Chem Soc 130: 14253-14262.
55. Schafer NP, Hoffman RMB, Burger A, Craig PO, Komives EA, et al. (2012) Discrete Kinetic Models from Funneled Energy Landscape Simulations. Plos One 7: e50635.
56. Naganathan AN, Orozco M, (2011) The Native Ensemble and Folding of a Protein Molten-Globule: Functional Consequence of Downhill Folding. J Am Chem Soc 133: 12154-12161.
57. Cerminara M, Desai TM, Sadqi M, Muñoz V, (2012) Downhill protein folding modules as scaffolds for broad-range ultrafast biosensors. J Am Chem Soc 134: 8010-8013.
58. Motlagh HN, Hilser VJ, (2012) Agonism/antagonism switching in allosteric ensembles. Proc Natl Acad Sci USA 109: 4134-4139.
59. Löw C, Homeyer N, Weininger U, Sticht H, Balbach J, (2008) Conformational Switch upon Phosphorylation: Human CDK Inhibitor p19INK4d between the Native and Partially Folded State. ACS Chem Biol 4: 53-63.