Crowded, cell-like environment induces shape changes in aspherical protein

Proceedings of the National Academy of Sciences of the United States of America

Volumn 105, Issue 33, 2008, Pages 11754-11759

  Homouz, Dirar ^a   Perham, Michael ^b   Samiotakis, Antonios ^a   Cheung, Margaret S ^a   Wittung Stafshede, Pernilla ^b,c  

^a University of Houston   (United States)

^b RICE UNIVERSITY   (United States)

^c UMEÅ UNIVERSITY   (Sweden)

Author keywords

Energy landscape theory; Excluded volume effect; Lyme disease; Macromolecular crowding; Off lattice model

Indexed keywords

BACTERIAL PROTEIN; PROTEIN VISE;

ARTICLE; BORRELIA BURGDORFERI; CONTROLLED STUDY; IN VITRO STUDY; LYME DISEASE; MATHEMATICAL COMPUTING; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE;

ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; BORRELIA BURGDORFERI; CIRCULAR DICHROISM; COMPUTER SIMULATION; LIPOPROTEINS; MODELS, MOLECULAR; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; THERMODYNAMICS;

BORRELIA BURGDORFERI;

EID: 50149092143     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0803672105     Document Type: Article

References (48)

1. van den Berg B, Ellis RJ, Dobson CM (1999) Effects of macromolecular crowding on protein folding and aggregation. EMBO J 18:6927-6933.
2. Rivas G, Ferrone F, Herzfeld J (2004) Life in a crowded world. EMBO Rep 5:23-27.
3. Ellis RJ, Minton AP (2003) Cell biology: Join the crowd. Nature 425:27-28.
4. Zimmerman SB, Minton AP (1993) Macromolecular crowding: Biochemical, biophysical, and physiological consequences. Annu Rev Biophys Biomol Struct 22:27-65.
5. Minton AP (2005) Models for excluded volume interaction between an unfolded protein and rigid macromolecular cosolutes: Macromolecular crowding and protein stability revisited. Biophys J 88:971-985.
6. Uversky VN, EMC, Bower KS, Li J, Fink AL (2002) Accelerated alpha-synuclein fibrillation in crowded milieu. FEBS Lett 515:99-103.
7. Cheung MS, Klimov D, Thirumalai D (2005) Molecular crowding enhances native state stability and refolding rates of globular proteins. Proc Natl Acad Sci USA 102:4753-4758.
8. Bokvist M, Grobner G (2007) Misfolding of amyloidogenic proteins at membrane surfaces: The impact of macromolecular crowding. J Am Chem Soc 129:14848-14849.
9. Hall D, Minton AP (2003) Macromolecular crowding: qualitative and semiquantitative successes, quantitative challenges. Biochim Biophys Acta 1649:127-139.
10. Zhou HX, Dill KA (2001) Stabilization of proteins in confined spaces. Biochemistry 40:11289-11293.
11. Eicken C, et al. (2002) Crystal structure of Lyme disease variable surface antigen VlsE of Borrelia burgdorferi. J Biol Chem 28:28.
12. Jones K, Wittung-Stafshede P (2003) The largest protein observed to fold by two-state kinetic mechanism does not obey contact-order correlation. J Am Chem Soc 125:9606-9607.
13. Jones K, Guidry J, Wittung-Stafshede P (2001) Characterization of surface antigen from Lyme disease spirochete Borrelia burgdorferi. Biochem Biophys Res Commun 289:389-394.
14. Liang FT, et al. (1999) Sensitive and specific serodiagnosis of Lyme disease by enzyme-linked immunosorbent assay with a peptide based on an immunodominant conserved region of Borrelia burgdorferi vlsE. J Clin Microbiol 37:3990-3996.
15. Venturoli D, Rippe B (2005) Ficoll and dextran vs. globular proteins as probes for testing glomerular permselectivity: Effects of molecular size, shape, charge, and deformability. Am J Physiol 288:F605-F613.
16. Luby-Phelps K, Castle PE, Taylor DL, Lanni F (1987) Hindered diffusion of inert tracer particles in the cytoplasm of mouse 3T3 cells. Proc Natl Acad Sci USA 84:4910-4913.
17. Monterroso B, Minton AP (2007) Effect of high concentration of inert cosolutes on the refolding of an enzyme: Carbonic anhydrase B in sucrose and Ficoll 70. J Biol Chem 282:33452-33458.
18. van den Berg B, Wain R, Dobson CM, Ellis RJ (2000) Macromolecular crowding perturbs protein refolding kinetics: Implications for folding inside the cell. EMBO J 19:3870-3875.
19. Zhou BR, Liang Y, Du F, Zhou Z, Chen J (2004) Mixed macromolecular crowding accelerates the oxidative refolding of reduced, denatured lysozyme: Implications for protein folding in intracellular environments. J Biol Chem 279:55109-55116.
20. Du F, et al. (2006) Mixed macromolecular crowding accelerates the refolding of rabbit muscle creatine kinase: Implications for protein folding in physiological environments. J Mol Biol 364:469-482.
21. Asakura S, Oosawa F (1954) On interaction between two bodies immersed in a solution of macromolecules. J Chem Phys 22:1255-1256.
22. Perham M, Stagg L, Wittung-Stafshede P (2007) Macromolecular crowding increases structural content of folded proteins. FEBS Lett 581:5065-5069.
23. Manning MC, Illangasekare M, Woody RW (1988) Circular dichroism studies of distorted alpha-helices, twisted beta-sheets, and beta turns. Biophys Chem 31: 77-86.
24. Onuchic JN, Luthey-Schulten Z, Wolynes PG (1997) Theory of protein folding: The energy landscape perspective. Annu Rev Phys Chem 48:545-600.
25. Brooks CL, III, Gruebele M, Onuchic JN, Wolynes PG (1998) Chemical physics of protein folding. Proc Natl Acad Sci USA 95:11037-11038.
26. Cheung MS, Finke JM, Callahan B, Onuchic JN (2003) Exploring the interplay of topology and secondary structural formation in the protein folding problem. J Phys Chem B 107:11193-11200.
27. Klimov DK, Newfield D, Thirumalai D (2002) Simulations of beta-hairpin folding confined to spherical pores using distributed computing. Proc Natl Acad Sci USA 99:8019-8024.
28. Stagg L, Zhang S-Q, Cheung MS, Wittung-Stafshede P (2007) Molecular crowding enhances native structure and stability of alpha/beta protein flavodoxin. Proc Natl Acad Sci USA 104:18976-18981.
29. Perham M, Chen M, Ma J, Wittung-Stafshede P (2005) Unfolding of heptameric co-chaperonin protein follows "fly casting" mechanism: Observation of transient nonnative heptamer. J Am Chem Soc 127:16402-16403.
30. Zong C, Wilson CJ, Shen T, Wolynes PG, Wittung-Stafshede P (2006) Phi-value analysis of apo-azurin folding: Comparison between experiment and theory. Biochemistry 45:6458-6466.
31. Snir Y, Kamien RD (2005) Entropically driven helix formation. Science 307:1067.
32. Philipp MT, et al. (2001) Antibody response to IR6, a conserved immunodominant region of the VlsE lipoprotein, wanes rapidly after antibiotic treatment of Borrelia burgdorferi infection in experimental animals and in humans. J Infect Dis 184:870-878.
33. Sasahara K, McPhie P, Minton AP (2003) Effect of dextran on protein stability and conformation attributed to macromolecular crowding. J Mol Biol 326:1227-1237.
34. Spencer DS, Xu K, Logan TM, Zhou HX (2005) Effects of pH, salt, and macromolecular crowding on the stability of FK506-binding protein: An integrated experimental and theoretical study. J Mol Biol 351:219-232.
35. Qu Y, Bolen D (2002) Efficacy of macromolecular crowding in forcing proteins to fold. Biophys Chem 101-102:155-165.
36. Tokuriki N, et al. (2004) Protein folding by the effects of macromolecular crowding. Protein Sci 13:125-133.
37. Veitshans T, Klimov D, Thirumalai D (1997) Protein folding kinetics: Timescales, pathways and energy landscapes in terms of sequence-dependent properties. Fold Des 2:1-22.
38. Sanbonmatsu KY, Garcia AE (2002) Structure of Met-Enkephalin in explicit aqueous solution using replica exchange molecular dynamics. Proteins 46:225-234.
39. Sugita Y, Okamoto Y (1999) Replica-exchange molecular dynamics methods for protein folding. Chem Phys Lett 314:141-151.
40. Kumar S, Bouzida D, Swendsen RH, Kollman PA, Rosenberg JM (1992) The weighted histogram analysis method for free-energy calculations on biomolecules I. The method. J Comput Chem 13:1011-1021.
41. Chodera JD, Swope WC, Pitera JW, Seok C, Dill KA (2007) Use of the weighted histogram analysis method for the analysis of simulated and parallel tempering simulations. J Chem Theory Comput 3:26-41.
42. Brooks BR, et al. (1983) CHARMM: A program for macromolecular energy, minimization, and dynamics calculations. J Comput Chem 4:187-217.
43. MacKerel AD, Jr, et al. (1998) CHARMM: The energy function and its parameterization with an overview of the program. The Encyclopedia of Computational Chemistry, ed von Ragué Schleyer P (Wiley, Chichester, NY), Vol 1, pp 271-277.
44. Cheung MS, Thirumalai D (2006) Nanopore-protein interactions dramatically alter stability and yield of the native state in restricted spaces. J Mol Biol 357:632-643.
45. Betancourt MR, Thirumalai D (1999) Exploring the kinetic requirements for enhancement of protein folding rates in the GroEL cavity. J Mol Biol 287:627-644.
46. Dima RI, Thirumalai D (2004) Asymmetry in the shapes of folded and denatured states of proteins. J Phys Chem B 108:6564-6570.
47. Phillips JC, et al. (2005) Scalable molecular dynamics with NAMD. J Comput Chem 26:1781-1802.
48. Fraczkiewicz R, Braun W (1998) Exact and efficient analytical calculation of the accessible surface areas and their gradients for macromolecules. J Comput Chem 19:319-333.