Filling up the heme pocket stabilizes apomyoglobin and speeds up its folding

Journal of Physical Chemistry B

Volumn 118, Issue 24, 2014, Pages 6511-6518

  Goodman, J S ^a   Chao, S H ^b   Pogorelov, T V ^a   Gruebele, M ^a,b,c  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b University of Illinois at Urbana Champaign   (United States)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAINS; MOLECULAR DYNAMICS; PROTEINS; TOPOLOGY;

CONTACT ORDERS; FOLDING MECHANISM; MOLECULAR DYNAMICS SIMULATIONS; PROTEIN STABILITY; REFOLDING KINETICS; SIMPLE TOPOLOGY; STOPPED-FLOW MEASUREMENTS; THERMAL DENATURATIONS;

PORPHYRINS;

APOMYOGLOBIN; APOPROTEIN; HEME; MYOGLOBIN; RECOMBINANT PROTEIN;

BIOSYNTHESIS; CHEMISTRY; CIRCULAR DICHROISM; GENETICS; KINETICS; METABOLISM; MOLECULAR DYNAMICS; MUTAGENESIS; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN REFOLDING; PROTEIN STABILITY; PROTEIN TERTIARY STRUCTURE; SPECTROFLUOROMETRY; THERMODYNAMICS;

APOPROTEINS; CIRCULAR DICHROISM; HEME; KINETICS; MOLECULAR DYNAMICS SIMULATION; MUTAGENESIS; MYOGLOBIN; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN REFOLDING; PROTEIN STABILITY; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; SPECTROMETRY, FLUORESCENCE; THERMODYNAMICS;

EID: 84902972809     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp412459z     Document Type: Article

References (38)

1. Kendrew, J. C.; Bodo, G.; Dintzis, H. M.; Parrish, R. G.; Wyckoff, H.; Phillips, D. C. A Three-Dimensional Model of the Myoglobin Molecule Obtained by X-Ray Analysis Nature 1958, 181, 662-666
2. Kirby, E. P.; Steiner, R. F. The Tryptophan Microenvironments in Apomyoglobin J. Biol. Chem. 1970, 245, 6300-6306
3. Cocco, M. J.; Lecomte, J. T. J. Characterization of Hydrophobic Cores in Apomyoglobin: A Proton NMR Spectroscopy Study Biochemistry 1990, 29, 11067-11072
4. Bashford, D.; Cohen, F. E.; Karplus, M.; Kuntz, I. D.; Weaver, D. L. Diffusion-Collision Model for the Folding Kinetics of Myoglobin Proteins 1988, 4, 211-227
5. Jennings, P. A.; Wright, P. E. Formation of a Molten Globule Intermediate Early in the Kinetic Folding Pathway of Apomyoglobin Science 1993, 262, 892-896
6. Ballew, R. M.; Sabelko, J.; Gruebele, M. Direct Observation of Fast Protein Folding: The Initial Collapse of Apomyoglobin Proc. Natl. Acad. Sci. U.S.A. 1996, 93, 5759-5764
7. Ballew, R. M.; Sabelko, J.; Gruebele, M. Observation of Distinct Nanosecond and Microsecond Protein Folding Events Nat. Struct. Biol. 1996, 3, 923-926
8. Rischel, C.; Thyberg, P.; Rigler, R.; Poulsen, F. M. Time-Resolved Fluorescence Studies of the Molten Globule State of Apomyoglobin J. Mol. Biol. 1996, 257, 877-885
9. Bieri, O.; Wirz, J.; Hellrung, B.; Schutkowski, M.; Drewello, M.; Kiefhaber, T. The Speed Limit of Protein Folding Measure by Triplet-Triplet Energy Transfer Proc. Natl. Acad. Sci. U.S.A. 1999, 96, 9597-9601
10. Gruebele, M. Protein Folding: The Free Energy Surface Curr. Opin. Struct. Biol. 2002, 12, 161-168
11. Gruebele, M. Downhill Protein Folding: Evolution Meets Physics C. R. Biol. 2005, 328, 701-712
12. Barrick, D.; Baldwin, R. Three-State Analysis of Sperm Whale Apomyoglobin Folding Biochemistry 1993, 32, 3790-3796
13. Spudich, G. M.; Miller, E. J.; Marqusee, S. Destabilization of the Escherichia Coli Rnase H Kinetic Intermediate: Switching between a Two-State and Three-State Folding Mechanism J. Mol. Biol. 2004, 335, 609-618
14. Sabelko, J.; Ervin, J.; Gruebele, M. The Cold Denatured Ensemble of Apomyoglobin: Implications for the Early Steps of Folding J. Phys. Chem. B 1998, 102, 1806-1819
15. Gilmanshin, R.; Dyer, R. B.; Callender, R. H. Structural Heterogeneity of the Various Forms of Apomyoglobin: Implications for Protein Folding Protein Sci. 1997, 6, 2134-2142
16. Yi, J.; Orville, A. M.; Skinner, J. M.; Skinner, M. J.; Richter-Addo, G. B. Synchrotron X-Ray-Induced Photoreduction of Ferric Myoglobin Nitrite Crystals Gives the Ferrous Derivative with Retention of the O-Bonded Nitrite Ligand Biochemistry 2010, 49, 5969-5971
17. Humphrey, W.; Dalke, A.; Schulten, K. VMD: Visual Molecular Dynamics J. Mol. Graphics 1996, 14 (33-38) 27-38
18. Phillips, J. C.; Braun, R.; Wang, W.; Gumbart, J.; Tajkhorshid, E.; Villa, E.; Chipot, C.; Skeel, R. D.; Kale, L.; Schulten, K. Scalable Molecular Dynamics with NAMD J. Comput. Chem. 2005, 26, 1781-1802
19. Vanommeslaeghe, K.; Hatcher, E.; Acharya, C.; Kundu, S.; Zhong, S.; Shim, J.; Darian, E.; Guvench, O.; Lopes, P.; Vorobyov, I.; Mackerell, A. D., Jr. Charmm General Force Field: A Force Field for Drug-Like Molecules Compatible with the Charmm All-Atom Additive Biological Force Fields J. Comput. Chem. 2010, 31, 671-690
20. Jorgensen, W. L.; Chandrasekhar, J.; Madura, J. D.; Impey, R. W.; Klein, M. L. Comparison of Simple Potential Functions for Simulating Liquid Water J. Chem. Phys. 1983, 79, 926-935
21. Mackerell, A. D., Jr.; Feig, M.; Brooks, C. L. Extending the Treatment of Backbone Energetics in Protein Force Fields: Limitations of Gas-Phase Quantum Mechanics in Reproducing Protein Conformational Distributions in Molecular Dynamics Simulations J. Comput. Chem. 2004, 25, 1400-1415
22. Martyna, G. J.; Tobias, D. J.; Klein, M. L. Constant Pressure Molecular Dynamics Algorithms J. Chem. Phys. 1994, 101, 4177-4189
23. Feller, S. E.; Zhang, Y.; Pastor, R. W.; Brooks, B. R. Constant Pressure Molecular Dynamics Simulation: The Langevin Piston Method J. Chem. Phys. 1995, 103, 4613-4621
24. Darden, T.; York, D.; Pedersen, L. Particle Mesh Ewald: An N Log(N) Method for Ewald Sums in Large Systems J. Chem. Phys. 1993, 98, 10089-10092
25. Till, M. S.; Ullmann, G. M. McVol-a Program for Calculating Protein Volumes and Identifying Cavities by a Monte Carlo Algorithm J. Mol. Model. 2010, 16, 419-429
26. Sethi, A.; Eargle, J.; Black, A. A.; Luthey-Schulten, Z. Dynamical Networks in Trna:Protein Complexes Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 6620-6625
27. Girvan, M.; Newman, M. E. Community Structure in Social and Biological Networks Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 7821-7826
28. Teale, F. W. Cleavage of the Haem-Protein Link by Acid Methylethylketone Biochim. Biophys. Acta 1959, 35, 543
29. Murray, J. W.; Delumeau, O.; Lewis, R. J. Structure of a Nonheme Globin in Environmental Stress Signaling Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 17320-17325
30. Nishii, I.; Kataoka, M.; Tokunaga, F.; Goto, Y. Cold Denaturation of the Molten Globule States of Apomyoglobin and a Profile for Protein Folding Biochemistry 1994, 33, 4903-4909
31. Tanford, C. Protein Denaturation Adv. Protein Chem. 1970, 24, 1-95
32. Picotti, P.; Marabotti, A.; Negro, A.; Musi, V.; Spolaore, B.; Zambonin, M.; Fontana, A. Modulation of the Structural Integrity of Helix F in Apomyoglobin by Single Amino Acid Replacements Protein Sci. 2004, 13, 1572-1585
33. Garcia, C.; Nishimura, C.; Cavagnero, S.; Dyson, H. J.; Wright, P. E. Changes in the Apomyoglobin Folding Pathway Caused by Mutation of the Distal Histidine Residue Biochemistry 2000, 39, 11227-11237
34. Chiba, K.; Ikai, A.; Kawamurakonishi, Y.; Kihara, H. Kinetic Study on Myoglobin Refolding Monitored by Five Optical Probe Stopped-Flow Methods Proteins 1994, 19, 110-119
35. Wan, L.; Twitchett, M. B.; Eltis, L. D.; Mauk, A. G.; Smith, M. In Vitro Evolution of Horse Heart Myoglobin to Increase Peroxidase Activity Proc. Natl. Acad. Sci. U.S.A. 1998, 95, 12825-12831
36. Ervin, J.; Larios, E.; Osvath, S.; Schulten, K.; Gruebele, M. What Causes Hyperfluorescence: Folding Intermediates or Conformationally Flexible Native States? Biophys. J. 2002, 83, 473-483
37. Yang, W. Y.; Gruebele, M. Folding at the Speed Limit Nature 2003, 423, 193-197
38. Chung, H. S.; McHale, K.; Louis, J. M.; Eaton, W. A. Single-Molecule Fluorescence Experiments Determine Protein Folding Transition Path Times Science 2012, 335, 981-984