Denatured state structural property determines protein stabilization by macromolecular crowding: A thermodynamic and structural approach

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Mittal, Shruti ^a   Singh, Laishram Rajendrakumar ^a  

^a UNIVERSITY OF DELHI   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA LACTALBUMIN; FICOLL; FICOLL 70; HOLO ALPHA LACTALBUMIN; LACTALBUMIN; LYSOZYME; RIBONUCLEASE A; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; FRACTIONATION; MACROMOLECULAR CROWDING; PH; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; PROTEIN TERTIARY STRUCTURE; THERMODYNAMICS; THERMOSTABILITY;

ANIMALS; CATTLE; HYDROGEN-ION CONCENTRATION; LACTALBUMIN; MACROMOLECULAR SUBSTANCES; MURAMIDASE; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN STABILITY; PROTEINS; RIBONUCLEASE, PANCREATIC; THERMODYNAMICS;

EID: 84893395763     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0078936     Document Type: Article

References (56)

1. Fulton AB (1982) How crowded is the cytoplasm? Cell 30: 345-347.
2. Goodsell DS (1991) Inside a living cell. Trends Biochem Sci 16: 203-206.
3. Ellis RJ (2001) Macromolecular crowding: an important but neglected aspect of the intracellular environment. Curr Opin Struct Biol 11: 114-119.
4. Zimmerman SB, Minton AP (1993) Macromolecular crowding: biochemical, biophysical, and physiological consequences. Annu Rev Biophys Biomol Struct 22: 27-65.
5. Hall D, Minton AP (2003) Macromolecular crowding: qualitative and semiquantitative successes, quantitative challenges. Biochim Biophys Acta 1649: 127-139.
6. Minton AP (2000) Implications of macromolecular crowding for protein assembly. Curr Opin Struct Biol 10: 34-39.
7. Luby-Phelps K (2000) Cytoarchitecture and physical properties of cytoplasm: volume, viscosity, diffusion, intracellular surface area. Int Rev Cytol 192: 189-221.
8. Benton LA, Smith AE, Young GB, Pielak GJ (2012) Unexpected Effects of Macromolecular Crowding on Protein Stability. Biochemistry 51: 9773-9775.
9. van den Berg B, Ellis RJ, Dobson CM (1999) Effects of macromolecular crowding on protein folding and aggregation. EMBO J 18: 6927-6933.
10. Stagg L, Zhang SQ, Cheung MS, Wittung-Stafshede P (2007) Molecular crowding enhances native structure and stability of alpha/beta protein flavodoxin. Proc Natl Acad Sci U S A 104: 18976-18981.
11. Batra J, Xu K, Zhou HX (2009) Nonadditive effects of mixed crowding on protein stability. Proteins 77: 133-138.
12. Chen E, Christiansen A, Wang Q, Cheung MS, Kliger DS, et al. (2012) Effects of Macromolecular Crowding on Burst Phase Kinetics of Cytochrome c Folding. Biochemistry 51: 9836-9845.
13. Dedmon MM, Patel CN, Young GB, Pielak GJ (2002) FlgM gains structure in living cells. Proc Natl Acad Sci U S A 99: 12681-12684.
14. 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.
15. Tokuriki N, Kinjo M, Negi S, Hoshino M, Goto Y, et al. (2004) Protein folding by the effects of macromolecular crowding. Protein Sci 13: 125-133.
16. Morar AS, Olteanu A, Young GB, Pielak GJ (2001) Solvent-induced collapse of alpha-synuclein and acid-denatured cytochrome c. Protein Sci 10: 2195-2199.
17. Engel R, Westphal AH, Huberts DH, Nabuurs SM, Lindhoud S, et al. (2008) Macromolecular crowding compacts unfolded apoflavodoxin and causes severe aggregation of the off-pathway intermediate during apoflavodoxin folding. J Biol Chem 283: 27383-27394.
18. Waegele MM, Gai F (2011) Power-law dependence of the melting temperature of ubiquitin on the volume fraction of macromolecular crowders. J Chem Phys 134: 095104.
19. McPhie P, Ni YS, Minton AP (2006) Macromolecular crowding stabilizes the molten globule form of apomyoglobin with respect to both cold and heat unfolding. J Mol Biol 361: 7-10.
20. Minton AP (2000) Effect of a concentrated ''inert'' macromolecular cosolute on the stability of a globular protein with respect to denaturation by heat and by chaotropes: a statistical-thermodynamic model. Biophys J 78: 101-109.
21. Cheung MS, Klimov D, Thirumalai D (2005) Molecular crowding enhances native state stability and refolding rates of globular proteins. Proc Natl Acad Sci U S A 102: 4753-4758.
22. 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.
23. Perham M, Stagg L, Wittung-Stafshede P (2007) Macromolecular crowding increases structural content of folded proteins. FEBS Lett 581: 5065-5069.
24. Miklos AC, Li C, Sharaf NG, Pielak GJ (2010) Volume exclusion and soft interaction effects on protein stability under crowded conditions. Biochemistry 49: 6984-6991.
25. Dhar A, Samiotakis A, Ebbinghaus S, Nienhaus L, Homouz D, et al. (2010) Structure, function, and folding of phosphoglycerate kinase are strongly perturbed by macromolecular crowding. Proc Natl Acad Sci U S A 107: 17586-17591.
26. Homouz D, Perham M, Samiotakis A, Cheung MS, Wittung-Stafshede P (2008) Crowded, cell-like environment induces shape changes in aspherical protein. Proc Natl Acad Sci U S A 105: 11754-11759.
27. Miklos AC, Sarkar M, Wang Y, Pielak GJ (2011) Protein crowding tunes protein stability. J Am Chem Soc 133: 7116-7120.
28. Harada R, Tochio N, Kigawa T, Sugita Y, Feig M (2013) Reduced Native State Stability in Crowded Cellular Environment Due to Protein2Protein Interactions. JACS 135: 3696-3701.
29. Malik A, Kundu J, Mukherjee SK, Chowdhury PK (2012) Myoglobin unfolding in crowding and confinement. J Phys Chem B 116: 12895-12904.
30. Bigelow CC (1960) Difference spectra of ribonuclease and two ribonuclease derivatives. C R Trav Lab Carlsberg 31: 305-324.
31. Hamaguchi K, Kurono A (1968) Structure of muramidase (lysozyme). I. The effect of guanidine hydrochloride on muramidase. J Biochem 54: 111-122.
32. Sugai S, Yashiro H, Nitta K (1973) Equilibrium and kinetics of the unfolding of alpha-lactalbumin by guanidine hydrochloride. Biochim Biophys Acta 328: 35-41.
33. Pace CN (1986) Determination and analysis of urea and guanidine hydrochloride denaturation curves. Methods Enzymol 131: 266-280.
34. Sinha A, Yadav S, Ahmad R, Ahmad F (2000) A possible origin of differences between calorimetric and equilibrium estimates of stability parameters of proteins. Biochem J 345 Pt 3: 711-717.
35. 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 U S A 84: 4910-4913.
36. 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 Renal Physiol 288: F605-613.
37. Wenner JR, Bloomfield VA (1999) Crowding effects on EcoRV kinetics and binding. Biophys J 77: 3234-3241.
38. Privalov PL (1979) Stability of proteins: small globular proteins. Adv Protein Chem 33: 167-241.
39. Griko YV, Freire E, Privalov PL (1994) Energetics of the alpha-lactalbumin states: a calorimetric and statistical thermodynamic study. Biochemistry 33: 1889-1899.
40. Greene LH, Grobler JA, Malinovskii VA, Tian J, Acharya KR, et al. (1999) Stability, activity and flexibility in alpha-lactalbumin. Protein Eng 12: 581-587.
41. Becktel WJ, Schellman JA (1987) Protein stability curves. Biopolymers 26: 1859-1877.
42. Wang Y, Sarkar M, Smith AE, Krois AS, Pielak GJ (2012) Macromolecular crowding and protein stability. J Am Chem Soc 134: 16614-16618.
43. Mikaelsson T, Aden J, Johansson LB, Wittung-Stafshede P (2013) Direct observation of protein unfolded state compaction in the presence of macromolecular crowding. Biophys J 104: 694-704.
44. Schlesinger AP, Wang Y, Tadeo X, Millet O, Pielak GJ (2011) Macromolecular crowding fails to fold a globular protein in cells. J Am Chem Soc 133: 8082-8085.
45. Johansen D, Jeffries CM, Hammouda B, Trewhella J, Goldenberg DP (2011) Effects of macromolecular crowding on an intrinsically disordered protein characterized by small-angle neutron scattering with contrast matching. Biophys J 100: 1120-1128.
46. Szasz CS, Alexa A, Toth K, Rakacs M, Langowski J, et al. (2011) Protein disorder prevails under crowded conditions. Biochemistry 50: 5834-5844.
47. McNulty BC, Young GB, Pielak GJ (2006) Macromolecular crowding in the Escherichia coli periplasm maintains alpha-synuclein disorder. J Mol Biol 355: 893-897.
48. Flaugh SL, Lumb KJ (2001) Effects of macromolecular crowding on the intrinsically disordered proteins c-Fos and p27(Kip1). Biomacromolecules 2: 538-540.
49. Myers JK, Oas TG (2001) Preorganized secondary structure as an important determinant of fast protein folding. Nat Struct Biol 8: 552-558.
50. Koepf EK, Petrassi HM, Sudol M, Kelly JW (1999) WW: An isolated threestranded antiparallel beta-sheet domain that unfolds and refolds reversibly; evidence for a structured hydrophobic cluster in urea and GdnHCl and a disordered thermal unfolded state. Protein Sci 8: 841-853.
51. Anfinsen CB (1973) Principles that govern the folding of protein chains. Science 181: 223-230.
52. Baldwin RL, Rose GD (1999) Is protein folding hierarchic? I. Local structure and peptide folding. Trends Biochem Sci 24: 26-33.
53. Jackson SE (1998) How do small single-domain proteins fold? Fold Des 3: R81-91.
54. Huang L, Jin R, Li J, Luo K, Huang T, et al. (2010) Macromolecular crowding converts the human recombinant PrPC to the soluble neurotoxic beta-oligomers. FASEB J 24: 3536-3543.
55. Inomata K, Ohno A, Tochio H, Isogai S, Tenno T, et al. (2009) High-resolution multi-dimensional NMR spectroscopy of proteins in human cells. Nature 458: 106-109.
56. Takaoka Y, Kioi Y, Morito A, Otani J, Arita K, et al. (2013) Quantitative comparison of protein dynamics in live cells and in vitro by in-cell (19)F-NMR. Chem Commun (Camb) 49: 2801-2803.