The role of higher CO-multipole moments in understanding the dynamics of photodissociated carbonmonoxide in myoglobin

Biophysical Journal

Volumn 94, Issue 7, 2008, Pages 2505-2515

  Plattner, Nuria ^a   Meuwly, Markus ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON MONOXIDE; MYOGLOBIN;

ARTICLE; BINDING SITE; CHEMICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER SIMULATION; KINETICS; LIGHT; METHODOLOGY; PHOTOCHEMISTRY; PROTEIN BINDING; PROTEIN CONFORMATION; RADIATION EXPOSURE; ULTRASTRUCTURE;

BINDING SITES; CARBON MONOXIDE; COMPUTER SIMULATION; KINETICS; LIGHT; MODELS, CHEMICAL; MODELS, MOLECULAR; MYOGLOBIN; PHOTOCHEMISTRY; PROTEIN BINDING; PROTEIN CONFORMATION;

EID: 41649119610     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1529/biophysj.107.120519     Document Type: Article

References (59)

1. Williams, P., J. Cosme, and A. Ward. 2003. Crystal structure of human cytochrome P4502C9 with bound warfarin. Nature. 242:464-468.
2. Reibarkh, M., T. Malia, and G. Wagner. 2006. NMR distinction of single- and multiple-mode binding of small-molecule protein ligands. J. Am. Chem. Soc. 128:2160-2161.
3. Kraut, J., P. Sigala, B. Pybus, C. Liu, D. Ringe, G. Petsko, and D. Herschlag. 2006. Testing electrostatic complementarity in enzyme catalysis: hydrogen bonding in the ketosteroid isomerase oxyanion hole. PLoS Biol. 4:501-519.
4. Campbell, S., N. Gold, R. Jackson, and D. Westhead. 2003. Ligand binding: functional site location, similarity and docking. Curr. Opin. Struct. Biol. 13:389-395.
5. Kraut, J. 1988. How do enzymes work? Science. 242:533-540.
6. Wolfenden, R. 2003. Thermodynamic and extrathermodynamic requirements of enzyme catalysis. Biophys. Chem. 105:559-572.
7. Warshel, A., P. K. Sharma, M. Kato, Y. Xiang, H. B. Liu, and M. H. M. Olsson. 2006. Electrostatic basis for enzyme catalysis. Chem. Rev. 106:3210-3235.
8. Schlichting, I., J. Berendzen, G. Phillips, and R. Sweet. 1994. Crystal structure of photolyzed carbonmonoxy-myoglobin. Nature. 371:808-812.
9. Teng, T., V. Srajer, and K. Moffat. 1994. Photolysis-induced changes. Nat. Struct. Biol. 1:701-705.
10. Ostermann, A., R. Waschipky, F. Parak, and G. Nienhaus. 2000. Ligand binding and conformational motions in myoglobin. Nature. 404:205-208.
11. Schotte, F., M. Lim, A. Jackson, V. Smirnov, J. Soman, J. Olson, G. Phillips, M. Wulff, and P. A. Anfinrud. 2003. Watching a protein as it functions with 150-ps time-resolved x-ray crystallography. Science. 300:1944-1947.
12. Srajer, V., Z. Ren, T. Teng, M. Schmidt, T. Ursby, D. Bourgeois, C. Pradervand, W. Schildkamp, M. Wulff, and K. Moffat. 2001. Protein conformational relaxation and ligand migration in myoglobin: a nanosecond to millisecond molecular movie from time-resolved Laue x-ray diffraction. Biochemistry. 40:13802-13815.
13. Straub, J. E., and M. Karplus. 1991. Molecular dynamics study of the photodissociation of carbon monoxide from myoglobin: ligand dynamics in the first 10 ps. Chem. Phys. 158:221-248.
14. Ma, J., S. Huo, and J. Straub. 1997. Molecular dynamics simulation study of the B-states of solvated carbon monoxymyoglobin. J. Am. Chem. Soc. 119:2541-2551.
15. Meller, J., and R. Elber. 1998. Computer simulations of carbon monoxide photodissociation in myoglobin: Structural interpretation of the B states. Biophys. J. 74:789-802.
16. Nutt, D. R., and M. Meuwly. 2003. Theoretical investigation of infrared spectra and pocket dynamics of photodissociated carbonmonoxy myoglobin. Biophys. J. 85:3612-3623.
17. Nutt, D. R., and M. Meuwly. 2004. CO migration in native and mutant myoglobin: atomistic simulations for the understanding of protein function. Proc. Natl. Acad. Sci. USA. 101:5998-6002.
18. Bossa, C., M. Anselmi, D. Roccatano, A. Amadei, B. Vallone, M. Brunori, and A. Di Nola. 2004. Extended molecular dynamics simulation of the carbon monoxide migration in sperm whale myoglobin. Biophys. J. 86:3855-3862.
19. Danielsson, J., P. Banushkina, D. Nutt, and M. Meuwly. 2006. Computer simulations of structures, energetics and dynamics of myoglobin⋯ligand complexes. Int. Rev. Phys. Chem. 25:407-425.
20. Meuwly, M. 2007. Using small molecules to probe protein cavities: the myoglobin-XO (X = C, N) family of systems. Eur. Phys. J. 141:209-216.
21. Nienhaus, K., J. S. Olson, S. Franzen, and G. U. Nienhaus. 2005. The origin of stark splitting in the initial photoproduct state of MbCO. J. Am. Chem. Soc. 127:40-41.
22. Meuwly, M. 2006. On the influence of the local environment on the CO stretching frequencies in native myoglobin: assignment of the B-states in MbCO. ChemPhysChem. 10:2061-2063.
23. Anselmi, M., M. Aschi, A. Di Nola, and A. Amadei. 2007. Theoretical characterization of carbon monoxide vibrational spectrum in sperm whale myoglobin distal pocket. Biophys. J. 92:3442-3447.
24. Lim, M., T. A. Jackson, and P. A. Anfinrud. 1995. Mid-infrared vibrational spectrum of CO after photodissociation from heme: evidence of a docking site in the heme pocket of hemoglobin and myoglobin. J. Chem. Phys. 102:4355-4366.
25. Lim, M., T. A. Jackson, and P. A. Anfinrud. 1997. Ultrafast rotation and trapping of carbon monoxide dissociated from myoglobin. Nat. Struct. Biol. 4:209-214.
26. Nutt, D., P. Banushkina, and M. Meuwly. 2005. Computational chemistry for elucidating protein function: Energetics and dynamics of myoglobin-ligand systems. Chimia (Aarau). 59:517-521.
27. MacKerell, A. D., Jr., D. Bashford, M. Bellott, R. L. Dunbrack, Jr., J. D. Evanseck, M. J. Field, S. Fischer, J. Gao, H. Guo, S. Ha, D. Joseph-McCarthy, L. Kuchnir, K. Kuczera, F. T. K. Lau, C. Mattos, S. Michnick, T. Ngo, D. T. Nguyen, B. Prodhom, W. E. Reiher III, B. Roux, M. Schlenkrich, J. C. Smith, R. Stote, J. E. Straub, M. Watanabe, J. Wiorkiewicz-Kuczera, D. Yin, and M. Karplus. 1998. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B. 102:3586-3616.
28. Weiner, S. J., P. A. Kollman, D. A. Case, U. Singh, C. Ghio, G. Alagona, S. Profeta, Jr., and P. Weiner. 1984. A new force-field for molecular mechanical simulation of nucleic-acids and proteins. J. Am. Chem. Soc. 106:765-784.
29. Mulliken, R. 1955. Electronic population analysis on LCAO-MO molecular wave functions. J. Chem. Phys. 23:1833-1840.
30. Singh, U. C., and P. A. Kollman. 1984. An approach to computing electrostatic charges for molecules. J. Comput. Chem. 5:129-145.
31. Besler, B. H., K. M. Merz, and P. A. Kollman. 1990. Atomic charges derived from semiempirical methods. J. Comput. Chem. 11:431-439.
32. Stone, A. J., and M. Alderton. 1985. Distributed multipole analysis - methods and applications. Mol. Phys. 56:1047-1064.
33. Sokalski, W., and R. Poirier. 1983. Cumulative atomic multipole representations of the molecular charge distribution and its basis set dependence. Chem. Phys. Lett. 98:86-92.
34. Mankoo, P. K., and T. Keyes. 2006. Induction model for molecular electrostatics: application to the infrared spectroscopy of CO liquid. J. Chem. Phys. 124:204503.
35. Stoll, J., J. Vrabec, and H. Hasse. 2003. A set of molecular models for carbon monoxide and halogenated hydrocarbons. J. Chem. Phys. 119:11396-11407.
36. Kuriyan, J., S. Wilz, M. Karplus, and G. Petsko. 1986. X-ray structure and refinement of carbon-monoxy (Fe-II)-myoglobin at 1.5-Å resolution. J. Mol. Biol. 192:133-154.
37. Meuwly, M., O. Becker, R. Stote, and M. Karplus. 2002. NO rebinding to myoglobin: a reactive molecular dynamics study. Biophys. Chem. 89:183-207.
38. Huffaker, J. N. 1976. Diatomic molecules as perturbed Morse oscillators. I. Energy levels. J. Chem. Phys. 64:3175-3181.
39. Johnson, J., D. Lamb, H. Frauenfelder, J. Muller, B. McMahon, G. Nienhaus, and R. D. Young. 1996. Ligand binding to heme proteins. 6. Interconversion of taxonomic substates in carbonmonoxymyoglobin. Biophys. J. 71:1563-1573.
40. Rovira, C., B. Schulze, M. Eichinger, J. D. Evanseck, and M. Parrinello. 2001. Influence of the heme pocket conformation on the structure and vibrations of the Fe-CO bond in myoglobin: a QM/MM density functional study. Biophys. J. 81:435-445.
41. Merchant, K. A., W. G. Noid, D. E. Thompson, R. Akiyama, R. F. Loring, and M. D. Fayer. 2003. Structural assignments and dynamics of the A substates of MbCO: spectrally resolved vibrational echo experiments and molecular dynamics simulations. J. Phys. Chem. B. 107:4-7.
42. Allen, M. P., and D. J. Tildesley. 1987. Computer Simulation of Liquids. Clarendon Press, Oxford.
43. Berens, P. H., and K. R. Wilson. 1981. Molecular-dynamics and spectra. 1. Diatomic rotation and vibration. J. Chem. Phys. 74:4872-4882.
44. Stone, A. J. 2005. Distributed multipole analysis: stability for large basis sets. J. Chem. Theory Comput. 1:1128-1132.
45. th algebraic order of accuracy. Dokl. Math. 59:477-481.
46. Stone, A. J., A. Dullweber, O. Engkvist, E. Fraschini, M. P. Hodges, A. W. Meredith, D. R. Nutt, P. L. A. Popelier, and D. J. Wales. 2002. ORIENT: a program for studying interactions between molecules. Available at http://www.stone.ch.cam.ac.uk/programs.html#Orient.
47. Frisch, M. J., G. W. Trucks, H. B. Schlegel, G. E. Scuseria, M. A. Robb, J. R. Cheeseman, J. A. Montgomery, Jr., T. Vreven, K. N. Kudin, J. C. Burant, J. M. Millam, S. E. S. Iyengar, J. Tomasi, V. Barone, B. Mennucci, M. Cossi, G. Scalmani, N. Rega, G. A. Petersson, H. Nakatsuji, M. Hada, M. Ehara, K. Toyota, R. Fukuda, J. Hasegawa, M. Ishida, T. Nakajima, Y. Honda, O. Kitao, H. Nakai, M. Klene, X. Li, J. E. Knox, H. P. Hratchian, J. B. Cross, C. Adamo, J. Jaramillo, R. Gomperts, R. E. Stratmann, O. Yazyev, A. J. Austin, R. Cammi, C. Pomelli, J. W. Ochterski, P. Y. Ayala, K. Morokuma, G. A. Voth, P. Salvador, J. J. Dannenberg, V. G. Zakrzewski, S. Dapprich, A. D. Daniels, M. C. Strain, O. Farkas, D. K. Malick, A. D. Rabuck, and K. Raghavachari. J. B. F. Resman, J. V. Ortiz, Q. Cui, A. G. Baboul, S. Clifford, J. Cioslowski, B. B. Stefanov, G. Liu, A. Liashenko, P. Piskorz, I. Komaromi, R. L. Martin, D. J. Fox, T. Keith, M. A. A. Laham, C. Y. Peng, A. Nanayakkara, M. Challacombe, P. M. W. Gill, B. Johnson, W. Chen, M. W. Wong, C. Gonzalez, and J. A. Pople. 2004. Gaussian 03, Rev. C.01. Gaussian Incorporated, Wallingford, CT.
48. Becke, A. D. 1993. Density-functional thermochemistry. 3. The role of exact exchange. J. Chem. Phys. 98:5648-5652.
49. Dunning, T. H., Jr. 1989. Gaussian-basis sets for use in correlated molecular calculations. 1. The atoms boron through neon and hydrogen. J. Chem. Phys. 90:1007-1023.
50. Maroulis, G. 1996. Electric polarizability and hyperpolarizability of carbon monoxide. J. Phys. Chem. 100:13466-13473.
51. Maroulis, G. 2001. Accurate higher electric multipole moments for carbon monoxide. Chem. Phys. Lett. 334:214-219.
52. Stone, A. J. 1996. The Theory of Intermolecular Forces. Clarendon Press, Oxford, UK.
53. Vitkup, D., G. A. Petsko, and M. Karplus. 1997. A comparison between molecular dynamics and x-ray results for dissociated CO in myoglobin. Nat. Struct. Biol. 4:202-208.
54. Teng, T., V. Srajer, and K. Moffat. 1997. Initial trajectory of carbon monoxide after photodissociation from myoglobin at cryogenic temperatures. Biochemistry. 36:12087-12100.
55. Vojtechovsky, J., K. Chu, J. Berendzen, G. Phillips, R. Sweet, and I. Schlichting. 1999. Crystal structures of myoglobin-ligand complexes at near-atomic resolution. Biophys. J. 77:2153-2174.
56. Phillips, G., M. Teodoro, T. Li, B. Smith, and J. Olson. 1999. Bound CO is a molecular probe of electrostatic potential in the distal pocket of myoglobin. J. Phys. Chem. B. 103:8817-8829.
57. Kim, S., and M. Lim. 2005. Picosecond dynamics of ligand interconversion in the primary docking site of heme proteins. J. Am. Chem. Soc. 127:5786-5787.
58. Lin, M., T. A. Jackson, and P. Anfinrud. 2004. Orientational distribution of CO before and after photolysis of MbCO and HbCO: a determination using time-resolved polarized mid-IR spectroscopy. J. Am. Chem. Soc. 126:7946-7957.
59. Anfinrud, P., M. Lim, and T. Jackson. 1994. Femtosecond IR spectroscopy: methods and applications to protein dynamics. Proc. SPIE Int. Soc. Opt. Eng. 2138:107-115.