Macromolecular crowding extended to a heptameric system: The Co-chaperonin protein 10

Biochemistry

Volumn 50, Issue 14, 2011, Pages 3034-3044

  Aguilar, Ximena ^a   F Weise, Christoph ^a   Sparrman, Tobias ^a   Wolf Watz, Magnus ^a   Wittung Stafshede, Pernilla ^a  

^a UMEÅ UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONIN; E. COLI; ERROR ESTIMATES; HEPTAMERS; MACROMOLECULAR CROWDING; MONOMER DISSOCIATION; MONOMERIC PROTEINS; MULTIPLE WAVELENGTHS; NEW APPROACHES; OLIGOMERIC PROTEINS; SPECTROSCOPIC DATA; THERMODYNAMIC CYCLE; THERMODYNAMIC PARAMETER; UV CIRCULAR DICHROISM;

AMINO ACIDS; CHEMICAL STABILITY; DICHROISM; DISSOCIATION; EQUILIBRIUM CONSTANTS; ESCHERICHIA COLI; EXPERIMENTS; GLUCOSE; MACROMOLECULES; MONOMERS; OLIGOMERS; PROTEINS; RESONANCE; THERMODYNAMIC STABILITY; THERMODYNAMICS;

NUCLEAR MAGNETIC RESONANCE;

BUFFER; CHAPERONIN; FICOLL; MONOMER; OLIGOMER; TYROSINE;

ARTICLE; BETA CHAIN; CIRCULAR DICHROISM; CROSS LINKING; DISSOCIATION; ESCHERICHIA COLI; FLUORESCENCE; MACROMOLECULE; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FOLDING; PROTEIN STABILITY; SPECTROSCOPY; THERMODYNAMICS; THERMOSTABILITY; ULTRAVIOLET RADIATION;

ALGORITHMS; CHAPERONIN 10; CIRCULAR DICHROISM; CROSS-LINKING REAGENTS; FICOLL; HUMANS; KINETICS; MACROMOLECULAR SUBSTANCES; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, CHEMICAL; PROTEIN DENATURATION; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; PROTEIN UNFOLDING; THERMODYNAMICS;

EID: 79953697415     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi2002086     Document Type: Article

References (82)

1. Rivas, G., Ferrone, F., and Herzfeld, J. (2004) Life in a crowded world EMBO Rep. 5, 23-27 (Pubitemid 38228522)
2. Ellis, R. J. and Minton, A. P. (2003) Cell biology: join the crowd Nature 425, 27-28
3. Minton, A. P. and Wilf, J. (1981) Effect of macromolecular crowding upon the structure and function of an enzyme: glyceraldehyde-3-phosphate dehydrogenase Biochemistry 20, 4821-4826
4. Laurent, T. C. and Ogston, A. G. (1963) The Interaction between Polysaccharides and Other Macromolecules. 4. the Osmotic Pressure of Mixtures of Serum Albumin and Hyaluronic Acid Biochem. J. 89, 249-253
5. Minton, A. P. (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 (Pubitemid 40975932)
6. Zhou, H. X. (2004) Loops, linkages, rings, catenanes, cages, and crowders: entropy based strategies for stabilizing proteins Acc. Chem. Res. 37, 123-130
7. Cheung, M. S., Klimov, D., and 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 (Pubitemid 40471526)
8. Cheung, M. S. and Thirumalai, D. (2007) Effects of crowding and confinement on the structures of the transition state ensemble in proteins J. Phys. Chem. B 111, 8250-8257 (Pubitemid 47184401)
9. Homouz, D., Sanabria, H., Waxham, M. N., and Cheung, M. S. (2009) Modulation of calmodulin plasticity by the effect of macromolecular crowding J. Mol. Biol. 391, 933-943
10. Zhang, S. Q. and Cheung, M. S. (2007) Manipulating biopolymer dynamics by anisotropic nanoconfinement Nano Lett. 7, 3438-3442 (Pubitemid 350216043)
11. Qin, S. and Zhou, H. X. (2009) Atomistic modeling of macromolecular crowding predicts modest increases in protein folding and binding stability Biophys. J. 97, 12-19
12. Mittal, J. and Best, R. B. (2008) Thermodynamics and kinetics of protein folding under confinement Proc. Natl. Acad. Sci. U.S.A. 105, 20233-20238
13. Wang, W., Xu, W. X., Levy, Y., Trizac, E., and Wolynes, P. G. (2009) Confinement effects on the kinetics and thermodynamics of protein dimerization Proc. Natl. Acad. Sci. U.S.A. 106, 5517-5522
14. Griffin, M. A., Friedel, M., and Shea, J. E. (2005) Effects of frustration, confinement, and surface interactions on the dimerization of an off-lattice beta-barrel protein J. Chem. Phys. 123, 174707
15. McGuffee, S. R. and Elcock, A. H. (2006) Atomically detailed simulations of concentrated protein solutions: the effects of salt, pH, point mutations, and protein concentration in simulations of 1000-molecule systems J. Am. Chem. Soc. 128, 12098-12110 (Pubitemid 44413841)
16. Dedmon, M. M., Patel, C. N., Young, G. B., and Pielak, G. J. (2002) FlgM gains structure in living cells Proc. Natl. Acad. Sci. U.S.A. 99, 12681-12684
17. Sasahara, K., McPhie, P., and Minton, A. P. (2003) Effect of dextran on protein stability and conformation attributed to macromolecular crowding J. Mol. Biol. 326, 1227-1237 (Pubitemid 36263394)
18. Jiao, M., Li, H. T., Chen, J., Minton, A. P., and Liang, Y. (2010) Attractive protein-polymer interactions markedly alter the effect of macromolecular crowding on protein association equilibria Biophys. J. 99, 914-923
19. Crowley, P. B., Brett, K., and Muldoon, J. (2008) NMR spectroscopy reveals cytochrome c-poly(ethylene glycol) interactions ChemBioChem 9, 685-688
20. Li, C. and Pielak, G. J. (2009) Using NMR to distinguish viscosity effects from nonspecific protein binding under crowded conditions J. Am. Chem. Soc. 131, 1368-1369
21. Minton, A. P. (1983) The effect of volume occupancy upon the thermodynamic activity of proteins: some biochemical consequences Mol. Cell. Biochem. 55, 119-140
22. Comper, W. D. and Laurent, T. C. (1978) An estimate of the enthalpic contribution to the interaction between dextran and albumin Biochem. J. 175, 703-708 (Pubitemid 9031641)
23. Perham, M., Stagg, L., and Wittung-Stafshede, P. (2007) Macromolecular crowding increases structural content of folded proteins FEBS Lett. 581, 5065-5069 (Pubitemid 47576087)
24. Stagg, L., Zhang, S. Q., Cheung, M. S., and 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
25. Homouz, D., Perham, M., Samiotakis, A., Cheung, M. S., and Wittung-Stafshede, P. (2008) Crowded, cell-like environment induces shape changes in aspherical protein Proc. Natl. Acad. Sci. U.S.A. 105, 11754-11759
26. Martin, J., Geromanos, S., Tempst, P., and Hartl, F. U. (1993) Identification of nucleotide-binding regions in the chaperonin proteins GroEL and GroES Nature 366, 279-282 (Pubitemid 23359713)
27. Todd, M. J., Boudkin, O., Freire, E., and Lorimer, G. H. (1995) GroES and the chaperonin-assisted protein folding cycle: GroES has no affinity for nucleotides FEBS Lett. 359, 123-125
28. Burston, S. G., Weissman, J. S., Farr, G. W., Fenton, W. A., and Horwich, A. L. (1996) Release of both native and non-native proteins from a cis-only GroEL ternary complex Nature 383, 96-99 (Pubitemid 26296469)
29. Shtilerman, M., Lorimer, G. H., and Englander, S. W. (1999) Chaperonin function: folding by forced unfolding Science 284, 822-825 (Pubitemid 29291351)
30. Braig, K., Otwinowski, Z., Hegde, R., Boisvert, D. C., Joachimiak, A., Horwich, A. L., and Sigler, P. B. (1994) The crystal structure of the bacterial chaperonin GroEL at 2.8 A [see comments] Nature 371, 578-586
31. Athanasas-Platsis, S., Somodevilla-Torres, M. J., Morton, H., and Cavanagh, A. C. (2004) Investigation of the immunocompetent cells that bind early pregnancy factor and preliminary studies of the early pregnancy factor target molecule Immunol. Cell Biol. 82, 361-369 (Pubitemid 39141758)
32. Cappello, F., Bellafiore, M., David, S., Anzalone, R., and Zummo, G. (2003) Ten kilodalton heat shock protein (HSP10) is overexpressed during carcinogenesis of large bowel and uterine exocervix Cancer Lett. 196, 35-41 (Pubitemid 36830908)
33. Slavotinek, A. M. and Biesecker, L. G. (2001) Unfolding the role of chaperones and chaperonins in human disease Trends Genet. 17, 528-535 (Pubitemid 32763051)
34. Hunt, J. F., Weaver, A. J., Landry, S. J., Gierasch, L., and Deisenhofer, J. (1996) The crystal structure of the GroES co-chaperonin at 2.8 A resolution Nature 379, 37-45
35. Mande, S. C., Mehra, V., Bloom, B. R., and Hol, W. G. (1996) Structure of the heat shock protein chaperonin-10 of Mycobacterium leprae Science 271, 203-207 (Pubitemid 26033300)
36. Roberts, M. M., Coker, A. R., Fossati, G., Mascagni, P., Coates, A. R., and Wood, S. P. (1999) Crystallization, x-ray diffraction and preliminary structure analysis of Mycobacterium tuberculosis chaperonin 10 AActa Crystallogr., Sect. D: Biol. Crystallogr. 55, 910-914 (Pubitemid 29194549)
37. Hunt, J. F., van der Vies, S. M., Henry, L., and Deisenhofer, J. (1997) Structural adaptations in the specialized bacteriophage T4 co-chaperonin Gp31 expand the size of the Anfinsen cage Cell 90, 361-371 (Pubitemid 27329720)
38. Numoto, N., Kita, A., and Miki, K. (2005) Crystal structure of the Co-chaperonin Cpn10 from Thermus thermophilus HB8 Proteins 58, 498-500 (Pubitemid 40076063)
39. Guidry, J. J., Shewmaker, F., Maskos, K., Landry, S., and Wittung-Stafshede, P. (2003) Probing the Interface in a Human Co-Chaperonin Heptamer: Residues Disrupting Oligomeric Unfolded State Identified BMC Biochem. 4, 14
40. Guidry, J. J. and Wittung-Stafshede, P. (2002) Low stability for monomeric human chaperonin protein 10: interprotein interactions contribute majority of oligomer stability Arch. Biochem. Biophys. 405, 280-282 (Pubitemid 35191743)
41. Guidry, J. J., Moczygemba, C. K., Steede, N. K., Landry, S. J., and Wittung-Stafshede, P. (2000) Reversible denaturation of oligomeric human chaperonin 10: denatured state depends on chemical denaturant Protein Sci. 9, 2109-2117 (Pubitemid 32104147)
42. Boudker, O., Todd, M. J., and Freire, E. (1997) The structural stability of the co-chaperonin GroES J. Mol. Biol. 272, 770-779 (Pubitemid 27448192)
43. Higurashi, T., Nosaka, K., Mizobata, T., Nagai, J., and Kawata, Y. (1999) Unfolding and refolding of Escherichia coli chaperonin GroES is expressed by a three-state model J. Mol. Biol. 291, 703-713 (Pubitemid 29392645)
44. Seale, J. W., Gorovits, B. M., Ybarra, J., and Horowitz, P. M. (1996) Reversible oligomerization and denaturation of the chaperonin GroES Biochemistry 35, 4079-4083 (Pubitemid 26113464)
45. Bascos, N., Guidry, J., and Wittung-Stafshede, P. (2004) Monomer topology defines folding speed of heptamer Protein Sci. 13, 1317-1321 (Pubitemid 38526096)
46. Steede, N., Guidry, J., and Landry, S. (2000) Preparation of recombinant human cpn10 Methods Mol. Biol. 140, 145-151
47. Landry, S. J., Steede, N. K., and Maskos, K. (1997) Temperature dependence of backbone dynamics in loops of human mitochondrial heat shock protein 10 Biochemistry 36, 10975-10986 (Pubitemid 27396254)
48. Ramsay, G. and Eftink, M. (1994) Analysis of multidimensional spectroscopic data to monitor unfolding of proteins Methods Enzymol. 240, 615-645
49. Greenfield, N. (2006) Using circular dichroism collected as a function of temperature to determine the thermodynamics of protein unfolding and binding interactions Nature Protocols 1, 2527-2535
50. Schellman, J. A. (1987) Selective binding and solvent denaturation Biopolymers 26, 549-559
51. Hall, D. and Minton, A. P. (2003) Macromolecular crowding: qualitative and semiquantitative successes, quantitative challenges Biochim. Biophys. Acta 1649, 127-139 (Pubitemid 38234581)
52. Record, M. T., Jr., Courtenay, E. S., Cayley, S., and Guttman, H. J. (1998) Biophysical compensation mechanisms buffering E. coli protein-nucleic acid interactions against changing environments Trends Biochem. Sci. 23, 190-194 (Pubitemid 28261038)
53. Cayley, S., Lewis, B. A., Guttman, H. J., and Record, M. T. (1991) Characterization of the cytoplasm of Escherichia coli K-12 as a function of external osmolarity: Implications for protein-DNA interactions in vivo J. Mol. Biol. 222, 281-300 (Pubitemid 121004007)
54. Luke, K., Apiyo, D., and Wittung-Stafshede, P. (2005) Dissecting homo-heptamer thermodynamics by isothermal titration calorimetry: entropy-driven assembly of co-chaperonin protein 10 Biophys. J. 89, 3332-3336 (Pubitemid 41636088)
55. Luke, K., Perham, M., and Wittung-Stafshede, P. (2006) Kinetic folding and assembly mechanisms differ for two homologous heptamers J. Mol. Biol. 363, 729-742 (Pubitemid 44486221)
56. Luke, K. and Wittung-Stafshede, P. (2006) Folding and assembly pathways of co-chaperonin proteins 10: Origin of bacterial thermostability Arch. Biochem. Biophys. 456, 8-18 (Pubitemid 44820027)
57. Perham, M., Chen, M., Ma, J., and 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 (Pubitemid 41740384)
58. Bohrer, M. P., GD, and Carroll, P. J. (1984) Hindered diffusion of dextran and Ficoll in microporous membranes Macromolecules 17, 1170-1173
59. Davidson, M. D. and W. (1988) Hindered diffusion of water-soluble macromolecules in membranes Macromolecules 21, 3474-3481
60. Ohlson, M., Sorensson, J., Lindstrom, K., Blom, A. M., Fries, E., and Haraldsson, B. (2001) Effects of filtration rate on the glomerular barrier and clearance of four differently shaped molecules Am. J. Physiol. Renal Physiol. 281, F103-113
61. Oliver, J. D., 3rd, Anderson, S., Troy, J. L., Brenner, B. M., and Deen, W. H. (1992) Determination of glomerular size-selectivity in the normal rat with Ficoll J. Am. Soc. Nephrol. 3, 214-228
62. Lavrenko, P. N., Mikriukova, O. I., and Okatova, O. V. (1987) On the separation ability of various Ficoll gradient solutions in zonal centrifugation Anal. Biochem. 166, 287-297
63. Wilkins, D. K., Grimshaw, S. B., Receveur, V., Dobson, C. M., Jones, J. A., and Smith, L. J. (1999) Hydrodynamic radii of native and denatured proteins measured by pulse field gradient NMR techniques Biochemistry 38, 16424-16431
64. Wallgren, M., Aden, J., Pylypenko, O., Mikaelsson, T., Johansson, L. B., Rak, A., and Wolf-Watz, M. (2008) Extreme temperature tolerance of a hyperthermophilic protein coupled to residual structure in the unfolded state J. Mol. Biol. 379, 845-858
65. Galan, A., Sot, B., Llorca, O., Carrascosa, J. L., Valpuesta, J. M., and Muga, A. (2001) Excluded volume effects on the refolding and assembly of an oligomeric protein. GroEL, a case study J. Biol. Chem. 276, 957-964 (Pubitemid 32096515)
66. Minton, A. P. (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 (Pubitemid 30207122)
67. Christiansen, A., Wang, Q., Samiotakis, A., Cheung, M. S., and Wittung-Stafshede, P. (2010) Factors defining effects of macromolecular crowding on protein stability: an in vitro/in silico case study using cytochrome c Biochemistry 49, 6519-6530
68. Tellam, R. L., Sculley, M. J., Nichol, L. W., and Wills, P. R. (1983) The influence of poly(ethylene glycol) 6000 on the properties of skeletal-muscle actin Biochem. J. 213, 651-659
69. Harding, S. E., Horton, J. C., Jones, S., Thornton, J. M., and Winzor, D. J. (1999) COVOL: an interactive program for evaluating second virial coefficients from the triaxial shape or dimensions of rigid macromolecules Biophys. J. 76, 2432-2438 (Pubitemid 29264605)
70. Fissell, W. H., Hofmann, C. L., Smith, R., and Chen, M. H. (2010) Size and conformation of Ficoll as determined by size-exclusion chromatography followed by multiangle light scattering Am. J. Physiol. Renal Physiol. 298, F205-F208
71. Fodeke, A. A. and Minton, A. P. (2010) Quantitative characterization of polymer-polymer, protein-protein, and polymer-protein interaction via tracer sedimentation equilibrium J. Phys. Chem. B 114, 10876-10880
72. Guven, O. and Eltan, E. (2003) Molecular association in aqueous solutions of high molecular weight poly(N-vinyl-2-pyrrolidone) Makromol. Chem. 182, 3129-3134
73. Okamoto, D. N., Oliveira, L. C., Kondo, M. Y., Cezari, M. H., Szeltner, Z., Juhasz, T., Juliano, M. A., Polgar, L., Juliano, L., and Gouvea, I. E. (2010) Increase of SARS-CoV 3CL peptidase activity due to macromolecular crowding effects in the milieu composition Biol. Chem. 391, 1461-1468
74. Phillip, Y., Sherman, E., Haran, G., and Schreiber, G. (2009) Common crowding agents have only a small effect on protein-protein interactions Biophys. J. 97, 875-885
75. Wilf, J. and Minton, A. P. (1981) Evidence for protein self-association induced by excluded volume. Myoglobin in the presence of globular proteins Biochim. Biophys. Acta 670, 316-322
76. Kim, Y. C., Best, R. B., and Mittal, J. (2010) Macromolecular crowding effects on protein-protein binding affinity and specificity J. Chem. Phys. 133, 205101
77. Snoussi, K. and Halle, B. (2005) Protein self-association induced by macromolecular crowding: a quantitative analysis by magnetic relaxation dispersion Biophys. J. 88, 2855-2866 (Pubitemid 40983844)
78. McGuffee, S. R. and Elcock, A. H. (2010) Diffusion, crowding & protein stability in a dynamic molecular model of the bacterial cytoplasm PLoS Comput. Biol. 6, e1000694
79. Rivas, G., Fernandez, J. A., and Minton, A. P. (2001) Direct observation of the enhancement of noncooperative protein self-assembly by macromolecular crowding: indefinite linear self-association of bacterial cell division protein FtsZ Proc. Natl. Acad. Sci. U.S.A. 98, 3150-3155 (Pubitemid 32220814)
80. del Alamo, M., Rivas, G., and Mateu, M. G. (2005) Effect of macromolecular crowding agents on human immunodeficiency virus type 1 capsid protein assembly in vitro J. Virol. 79, 14271-14281 (Pubitemid 41552725)
81. Hong, J. and Gierasch, L. M. (2010) Macromolecular crowding remodels the energy landscape of a protein by favoring a more compact unfolded state J. Am. Chem. Soc. 132, 10445-10452
82. Ando, T. and Skolnick, J. (2010) Crowding and hydrodynamic interactions likely dominate in vivo macromolecular motion Proc. Natl. Acad. Sci. U.S.A. 107, 18457-18462