Minimal effects of macromolecular crowding on an intrinsically disordered protein: A small-angle neutron scattering study

Biophysical Journal

Volumn 106, Issue 4, 2014, Pages 905-914

  Goldenberg, David P ^a   Argyle, Brian ^a  

^a UNIVERSITY OF UTAH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APROTININ; INTRINSICALLY DISORDERED PROTEIN; METMYOGLOBIN; N PROTEIN, BACTERIOPHAGE LAMBDA; VIRUS PROTEIN;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CATTLE; CHEMISTRY; HORSE; MOLECULAR GENETICS; NEUTRON DIFFRACTION; SMALL ANGLE SCATTERING;

AMINO ACID SEQUENCE; ANIMALS; APROTININ; CATTLE; HORSES; INTRINSICALLY DISORDERED PROTEINS; METMYOGLOBIN; MOLECULAR SEQUENCE DATA; NEUTRON DIFFRACTION; SCATTERING, SMALL ANGLE; VIRAL REGULATORY AND ACCESSORY PROTEINS;

EID: 84894427113     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2013.12.003     Document Type: Article

References (91)

1. A.B. Fulton How crowded is the cytoplasm? Cell 30 1982 345 347
2. S.B. Zimmerman, and S.O. Trach Estimation of macromolecule concentrations and excluded volume effects for the cytoplasm of Escherichia coli J. Mol. Biol. 222 1991 599 620
3. J. Spitzer, and B. Poolman How crowded is the prokaryotic cytoplasm? FEBS Lett. 587 2013 2094 2098
4. R.J. Ellis Macromolecular crowding: obvious but underappreciated Trends Biochem. Sci. 26 2001 597 604
5. D. Hall, and A.P. Minton Macromolecular crowding: qualitative and semiquantitative successes, quantitative challenges Biochim. Biophys. Acta 1649 2003 127 139
6. H.-X. Zhou, G. Rivas, and A.P. Minton Macromolecular crowding and confinement: biochemical, biophysical, and potential physiological consequences Annu. Rev. Biophys 37 2008 375 397
7. A.H. Elcock Models of macromolecular crowding effects and the need for quantitative comparisons with experiment Curr. Opin. Struct. Biol. 20 2010 196 206
8. A. Gershenson, and L.M. Gierasch Protein folding in the cell: challenges and progress Curr. Opin. Struct. Biol. 21 2011 32 41
9. H.-X. Zhou Influence of crowded cellular environments on protein folding, binding, and oligomerization: biological consequences and potentials of atomistic modeling FEBS Lett. 587 2013 1053 1061
10. M.S. Cheung, D.K. Klimov, and D. Thirumalai Molecular crowding enhances native state stability and refolding rates of globular proteins Proc. Natl. Acad. Sci. USA 102 2005 4753 4758
11. A.P. Minton Models for excluded volume interaction between an unfolded protein and rigid macromolecular cosolutes: macromolecular crowding and protein stability revisited Biophys. J. 88 2005 971 985
12. D.D.L. Minh, and C.E. Chang J.A. McCammon The influence of macromolecular crowding on HIV-1 protease internal dynamics J. Am. Chem. Soc. 128 2006 6006 6007
13. L. Stagg, and S.-Q. Zhang P. Wittung-Stafshede Molecular crowding enhances native structure and stability of α/β protein flavodoxin Proc. Natl. Acad. Sci. USA 104 2007 18976 18981
14. D. Homouz, and H. Sanabria M.S. Cheung Modulation of calmodulin plasticity by the effect of macromolecular crowding J. Mol. Biol. 391 2009 933 943
15. A. Dhar, and A. Samiotakis M.S. Cheung Structure, function, and folding of phosphoglycerate kinase are strongly perturbed by macromolecular crowding Proc. Natl. Acad. Sci. USA 107 2010 17586 17591
16. H. Dong, S. Qin, and H.-X. Zhou Effects of macromolecular crowding on protein conformational changes PLOS Comput. Biol. 6 2010 e1000833
17. J. Hong, and L.M. Gierasch Macromolecular crowding remodels the energy landscape of a protein by favoring a more compact unfolded state J. Am. Chem. Soc. 132 2010 10445 10452
18. A.C. Miklos, and C. Li G.J. Pielak Volume exclusion and soft interaction effects on protein stability under crowded conditions Biochemistry 49 2010 6984 6991
19. J. Mittal, and R.B. Best Dependence of protein folding stability and dynamics on the density and composition of macromolecular crowders Biophys. J. 98 2010 315 320
20. D. Tsao, A.P. Minton, and N.V. Dokholyan A didactic model of macromolecular crowding effects on protein folding PLoS ONE 5 2010 e11936
21. A.C. Miklos, and M. Sarkar G.J. Pielak Protein crowding tunes protein stability J. Am. Chem. Soc. 133 2011 7116 7120
22. S. Nagarajan, and D. Amir E. Haas Modulation of functionally significant conformational equilibria in adenylate kinase by high concentrations of trimethylamine oxide attributed to volume exclusion Biophys. J. 100 2011 2991 2999
23. M.P. Latham, and L.E. Kay Is buffer a good proxy for a crowded cell-like environment? A comparative NMR study of calmodulin side-chain dynamics in buffer and E. coli lysate PLoS ONE 7 2012 e48226
24. L.A. Benton, and A.E. Smith G.J. Pielak Unexpected effects of macromolecular crowding on protein stability Biochemistry 51 2012 9773 9775
25. Y. Wang, and M. Sarkar G.J. Pielak Macromolecular crowding and protein stability J. Am. Chem. Soc. 134 2012 16614 16618
26. R. Harada, and N. Tochio M. Feig Reduced native state stability in crowded cellular environment due to protein-protein interactions J. Am. Chem. Soc. 135 2013 3696 3701
27. A.P. Minton 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 2000 101 109
28. B.E. Bowler Residual structure in unfolded proteins Curr. Opin. Struct. Biol. 22 2012 4 13
29. G. Haran How, when and why proteins collapse: the relation to folding Curr. Opin. Struct. Biol. 22 2012 14 20
30. T.Y. Yoo, and S.P. Meisburger K.W. Plaxco Small-angle x-ray scattering and single-molecule FRET spectroscopy produce highly divergent views of the low-denaturant unfolded state J. Mol. Biol. 418 2012 226 236
31. W. Meng, and N. Lyle R.V. Pappu Experiments and simulations show how long-range contacts can form in expanded unfolded proteins with negligible secondary structure Proc. Natl. Acad. Sci. USA 110 2013 2123 2128
32. H.-X. Zhou Effect of mixed macromolecular crowding agents on protein folding Proteins 72 2008 1109 1113
33. S. Qin, and H.-X. Zhou Atomistic modeling of macromolecular crowding predicts modest increases in protein folding and binding stability Biophys. J. 97 2009 12 19
34. S. Qin, and H.-X. Zhou Generalized fundamental measure theory for atomistic modeling of macromolecular crowding Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 81 2010 031919
35. D. Johansen, and C.M.J. Jeffries D.P. Goldenberg Effects of macromolecular crowding on an intrinsically disordered protein characterized by small-angle neutron scattering with contrast matching Biophys. J. 100 2011 1120 1128
36. S. Qin, and H.-X. Zhou An FFT-based method for modeling protein folding and binding under crowding: benchmarking on ellipsoidal and all-atom crowders J. Chem. Theory Comput. 9 2013 4633 4643
37. D.A. Jacques, and J. Trewhella Small-angle scattering for structural biology - expanding the frontier while avoiding the pitfalls Protein Sci. 19 2010 642 657
38. P. Bernadó, and D.I. Svergun Structural analysis of intrinsically disordered proteins by small-angle x-ray scattering Mol. Biosyst. 8 2012 151 167
39. R.P. Rambo, and J.A. Tainer Accurate assessment of mass, models and resolution by small-angle scattering Nature 496 2013 477 481
40. D.M. Engelman, and P.B. Moore A new method for the determination of biological quarternary structure by neutron scattering Proc. Natl. Acad. Sci. USA 69 1972 1997 1999
41. H.B. Stuhrmann Unique aspects of neutron scattering for the study of biological systems Rep. Prog. Phys. 67 2004 1073 1115
42. W.T. Heller Small-angle neutron scattering and contrast variation: a powerful combination for studying biological structures Acta Crystallogr. D Biol. Crystallogr. 66 2010 1213 1217
43. C. Le Coeur, B. Demé, and S. Longeville Compression of random coils due to macromolecular crowding Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 79 2009 031910
44. C. Le Coeur, and J. Teixeira S. Longeville Compression of random coils due to macromolecular crowding: scaling effects Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 81 2010 061914
45. D.P. Goldenberg, and B. Argyle Self-crowding of globular proteins studied by small-angle x-ray scattering Biophys. J. 106 2013 895 904
46. E. Antonini, and M. Brunori Hemoglobin and Myoglobin in Their Reactions with Ligands 1971 North-Holland Publishing Dordrecht, The Netherlands 40 54
47. T.E. Creighton Renaturation of the reduced bovine pancreatic trypsin inhibitor J. Mol. Biol. 87 1974 563 577
48. W.A. Rees, and S.E. Weitzel P.H. von Hippel Bacteriophage λ N protein alone can induce transcription antitermination in vitro Proc. Natl. Acad. Sci. USA 93 1996 342 346
49. F.W. Studier Protein production by auto-induction in high density shaking cultures Protein Expr. Purif. 41 2005 207 234
50. M.R. van Gilst, and W.A. Rees P.H. von Hippel Complexes of N antitermination protein of phage λ with specific and nonspecific RNA target sites on the nascent transcript Biochemistry 36 1997 1514 1524
51. D. Johansen, J. Trewhella, and D.P. Goldenberg Fractal dimension of an intrinsically disordered protein: small-angle x-ray scattering and computational study of the bacteriophage λ-protein Protein Sci. 20 2011 1955 1970
52. P. Güntert, C. Mumenthaler, and K. Wüthrich Torsion angle dynamics for NMR structure calculation with the new program DYANA J. Mol. Biol. 273 1997 283 298
53. D.P. Goldenberg Computational simulation of the statistical properties of unfolded proteins J. Mol. Biol. 326 2003 1615 1633
54. Y. Wang, J. Trewhella, and D.P. Goldenberg Small-angle x-ray scattering of reduced ribonuclease A: effects of solution conditions and comparisons with a computational model of unfolded proteins J. Mol. Biol. 377 2008 1576 1592
55. C. Chothia Structural invariants in protein folding Nature 254 1975 304 308
56. B. Lee, and F.M. Richards The interpretation of protein structures: estimation of static accessibility J. Mol. Biol. 55 1971 379 400
57. D.I. Svergun, and S. Richard G. Zaccai Protein hydration in solution: experimental observation by x-ray and neutron scattering Proc. Natl. Acad. Sci. USA 95 1998 2267 2272
58. J.L. Lebowitz, E. Helfand, and E. Praestgaard Scaled particle theory of fluid mixtures J. Chem. Phys. 43 1965 774 779
59. G.I. Makhatadze, G.M. Clore, and A.M. Gronenborn Solvent isotope effect and protein stability Nat. Struct. Biol. 2 1995 852 855
60. p and evaluation of solvent isotope effects Protein Sci. 7 1998 2405 2412
61. 2O Biopolymers 85 2007 264 273
62. 2O J. Phys. Chem. 69 1965 3132 3144
63. T.G. Oas, and E.J. Toone Thermodynamic solvent isotope effects and molecular hydrophobicity Adv. Biophys. Chem. 6 1997 1 52
64. J.P. Vincent, R. Chicheportiche, and M. Lazdunski The conformational properties of the basic pancreatic trypsin-inhibitor Eur. J. Biochem. 23 1971 401 411
65. T.E. Creighton Electrophoretic analysis of the unfolding of proteins by urea J. Mol. Biol. 129 1979 235 264
66. F. Ahmad, and C.C. Bigelow Estimation of the free energy of stabilization of ribonuclease A, lysozyme, α-lactalbumin, and myoglobin J. Biol. Chem. 257 1982 12935 12938
67. J.E. Kohn, and I.S. Millett K.W. Plaxco Random-coil behavior and the dimensions of chemically unfolded proteins Proc. Natl. Acad. Sci. USA 101 2004 12491 12496
68. G. Porod General theory O. Glatter, O. Kratky, Small-Angle X-Ray Scattering 1982 Academic Press London 17 51
69. P.J. Flory The configuration of real polymer chains J. Chem. Phys. 17 1949 303 310
70. P.J. Flory Principles of Polymer Chemistry 1953 Cornell University Press Ithaca, NY
71. P.-G. de Gennes Scaling Concepts in Polymer Physics 1979 Cornell University Press Ithaca, NY
72. M. Rubinstein, and R.H. Colby Polymer Physics 2003 Oxford University Press Oxford, UK
73. J. Teixeira Small-angle scattering by fractal systems J. Appl. Cryst. 21 1988 781 785
74. P.W. Schmidt Use of scattering to determine the fractal dimension D. Avnir, The Fractal Approach to Heterogeneous Chemistry 1989 John Wiley & Sons Chichester, UK 67 79
75. G. Beaucage Toward resolution of ambiguity for the unfolded state Biophys. J. 95 2008 503 509
76. D. Johansen, and C.M.J. Jeffries D.P. Goldenberg Correction."Effects of macromolecular crowding on an intrinsically disordered protein characterized by small-angle neutron scattering with contrast matching." Biophys. J. 105 2013 1285 1286
77. S. Qin, J. Mittal, and H.-X. Zhou Folding free energy surfaces of three small proteins under crowding: validation of the postprocessing method by direct simulation Phys. Biol. 10 2013 045001
78. S. Qin, and H.-X. Zhou Effects of macromolecular crowding on the conformational ensembles of disordered proteins J. Phys. Chem. Lett. 4 2013 3429 3434
79. K. Sasahara, P. McPhie, and A.P. Minton Effect of dextran on protein stability and conformation attributed to macromolecular crowding J. Mol. Biol. 326 2003 1227 1237
80. N. Tokuriki, and M. Kinjo T. Yomo Protein folding by the effects of macromolecular crowding Protein Sci. 13 2004 125 133
81. L.M. Charlton, and C.O. Barnes G.J. Pielak Residue-level interrogation of macromolecular crowding effects on protein stability J. Am. Chem. Soc. 130 2008 6826 6830
82. A. Christiansen, and Q. Wang P. Wittung-Stafshede Factors defining effects of macromolecular crowding on protein stability: an in vitro/in silico case study using cytochrome c Biochemistry 49 2010 6519 6530
83. R. Engel, and A.H. Westphal C.P.M. van Mierlo Macromolecular crowding compacts unfolded apoflavodoxin and causes severe aggregation of the off-pathway intermediate during apoflavodoxin folding J. Biol. Chem. 283 2008 27383 27394
84. C.S. Szasz, and A. Alexa P. Tompa Protein disorder prevails under crowded conditions Biochemistry 50 2011 5834 5844
85. T. Mikaelsson, and J. Adén P. Wittung-Stafshede Direct observation of protein unfolded state compaction in the presence of macromolecular crowding Biophys. J. 104 2013 694 704
86. H.-X. Zhou Polymer crowders and protein crowders act similarly on protein folding stability FEBS Lett. 587 2013 394 397
87. Y.C. Kim, and J. Mittal Crowding induced entropy-enthalpy compensation in protein association equilibria Phys. Rev. Lett. 110 2013 208102
88. J.A. Marsh, and J.D. Forman-Kay Sequence determinants of compaction in intrinsically disordered proteins Biophys. J. 98 2010 2383 2390
89. S. Müller-Späth, and A. Soranno B. Schuler Charge interactions can dominate the dimensions of intrinsically disordered proteins Proc. Natl. Acad. Sci. USA 107 2010 14609 14614
90. A.H. Mao, and S.L. Crick R.V. Pappu Net charge per residue modulates conformational ensembles of intrinsically disordered proteins Proc. Natl. Acad. Sci. USA 107 2010 8183 8188
91. R.K. Das, and R.V. Pappu Conformations of intrinsically disordered proteins are influenced by linear sequence distributions of oppositely charged residues Proc. Natl. Acad. Sci. USA 110 2013 13392 13397