O2 migration pathways are not conserved across proteins of a similar fold

Biophysical Journal

Volumn 93, Issue 10, 2007, Pages 3591-3600

  Cohen, Jordi ^a   Schulten, Klaus ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

AMINE OXIDASE (FLAVIN CONTAINING); COPPER; GLOBIN; OXYGEN; PROTEIN; VEGETABLE PROTEIN;

ARTICLE; CRYSTAL STRUCTURE; ENZYME ACTIVITY; MATHEMATICAL COMPUTING; MATHEMATICAL MODEL; MOLECULAR DYNAMICS; POINT MUTATION; PROTEIN FAMILY; PROTEIN INTERACTION; X RAY CRYSTALLOGRAPHY; ANIMAL; BIOPHYSICS; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER SIMULATION; CONFORMATION; HUMAN; METHODOLOGY; PROTEIN DATABASE; PROTEIN ENGINEERING; PROTEIN FOLDING; PROTEIN TERTIARY STRUCTURE; STATISTICAL MODEL;

ANIMALS; BIOPHYSICS; COMPUTER SIMULATION; DATABASES, PROTEIN; GLOBINS; HUMANS; MODELS, MOLECULAR; MODELS, STATISTICAL; MOLECULAR CONFORMATION; OXYGEN; PLANT PROTEINS; PROTEIN ENGINEERING; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; PROTEINS;

EID: 36549007107     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.107.108712     Document Type: Article

References (69)

1. Carlson, M. L., R. M. Regan, and Q. H. Gibson. 1996. Distal cavity fluctuations in myoglobin: protein motion and ligand diffusion. Biochemistry. 35:1125-1136.
2. 2 transport in CpI [FeFe]-hydrogenase and the role of packing defects. Structure. 13:1321-1329.
3. 2, CO, NO, and Xe inside myoglobin. Biophys. J. 91:1844-1857.
4. Boichenko, V. A., E. Greenbaum, and M. Seibert. 2004. Hydrogen production by photosynthetic microorganisms. In Photoconversion of Solar Energy: Molecular to Global Photosynthesis. M. D. Archer and J. Barber, editors. Imperial College Press, London. 397-452.
5. Mertens, R., and A. Liese. 2004. Biotechnological applications of hydrogenases. Curr. Opin. Biotechnol. 15:343-348.
6. 2. Trends Biotechnol. 18:506-511.
7. Wang, Y., J. Cohen, W. F. Boron, K. Schulten, and E. Tajkhorshid. 2007. Exploring gas permeability of cellular membranes and membrane channels with molecular dynamics. J. Struct. Biol. 157:534-544.
8. Johnson, B. J., J. Cohen, R. W. Welford, A. R. Pearson, K. Schulten, J. P. Klinman, and C. M. Wilmot. 2007. Exploring molecular oxygen pathways in Hanseluna polymorpha copper-containing amine oxidase. J. Biol. Chem. 282:17767-17776.
9. Appleby, C. A. 1984. Leghemoglobin and rhizobium respiration. Ann. Rev. Plant Physiol. 35:443-478.
10. Frauenfelder, H., B. H. McMahon, R. H. Austin, K. Chu, and J. T. Groves. 2001. The role of structure, energy landscape, dynamics, and allostery in the enzymatic function of myoglobin. Proc. Natl. Acad. Sci. USA. 98:2370-2374.
11. Brunori, M., D. Bourgeois, and B. Vallone. 2004. The structural dynamics of myoglobin. J. Struct. Biol. 147:223-234.
12. Wittenberg, J. B., and B. A. Wittenberg. 2003. Myoglobin function reassessed. J. Exp. Biol. 206:2011-2020.
13. Garry, D. J., S. B. Kanatous, and P. P. A. Mammen. 2003. Emerging roles for myoglobin in the heart. Trends Cardiovasc. Med. 13:111-116.
14. Flögel, U., M. W. Merx, A. Gödecke, U. K. M. Decking, and J. Schrader. 2001. Myoglobin: a scavenger of bioactive NO. Proc. Natl. Acad. Sci. USA. 98:735-740.
15. Wan, L., M. B. Twitchett, L. D. Eltis, A. G. Mauk, and M. Smith. 1998. In vitro evolution of horse heart myoglobin to increase peroxidase activity. Proc. Natl. Acad. Sci. USA. 95:12825-12831.
16. Weber, R. E., and S. N. Vinogradov. 2001. Non-vertebrate hemoglobins: functions and molecular adaptations. Physiol. Rev. 81:569-627.
17. Perutz, M. F. 1979. Regulation of oxygen affinity of hemoglobin: influence of structure of the globin on the heme iron. Annu. Rev. Biochem. 48:327-386.
18. Royer, W. E. Jr., H. Zhu, T. A. Gorr, J. F. Flores, and J. E. Knapp. 2005. Allosteric hemoglobin assembly: diversity and similarity. J. Biol. Chem. 39:27477-27480.
19. Tilton, R. F., I. D. Kuntz, and G. A. Petsko. 1984. Cavities in proteins: structure of a metmyoglobin-xenon complex solved to 1.9 Å. Biochemistry. 23:2849-2857.
20. Brunori, M., B. Vallone, F. Cutruzzola, C. Travaglini-Allocatelli, J. Berendzen, K. Chu, R. M. Sweeti, and I. Schlichting. 2000. The role of cavities in protein dynamics: crystal structure of a photolytic intermediate of a mutant myoglobin. Proc. Natl. Acad. Sci. USA. 97:2058-2063.
21. Schotte, F., M. Lim, T. A. Jackson, A. V. Smirnov, J. Soman, J. S. Olson, G. N. Phillips Jr., 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.
22. Schmidt, M., K. Nienhaus, R. Pahl, A. Krasselt, S. Anderson, F. Parak, G. U. Nienhaus, and V. Šrajer. 2005. Ligand migration pathway and protein dynamics in myoglobin: a time-resolved crystallographic study on L29W MbCO. Proc. Natl. Acad. Sci. USA. 102:11704-11709.
23. Šrajer, V., Z. Ren, T. Y. 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.
24. Bourgeois, D., B. Vallone, F. Schotte, A. Arcovito, A. E. Miele, G. Sciara, M. Wulff, P. Anfinrud, and M. Brunori. 2003. Complex landscape of protein structural dynamics unveiled by nanosecond Laue crystallography. Proc. Natl. Acad. Sci. USA. 100:8704-8709.
25. Šrajer, V., T. Y. Teng, T. Ursby, C. Pradervand, Z. Ren, S. Adachi, W. Schildkamp, D. Bourgeois, M. Wulff, and K. Moffat. 1996. Photolysis of the carbon monoxide complex of myoglobin: nanosecond time-resolved crystallography. Science. 274:1726-1729.
26. Austin, R. H., K. W. Beeson, L. Eisenstein, H. Frauenfelder, and I. C. Gunsalus. 1975. Dynamics of ligand binding to myoglobin. Biochemistry. 14:5355-5373.
27. 2 entry into and exit from myoglobin. J. Biol. Chem. 276:5177-5188.
28. Ostermann, A., R. Waschipky, F. G. Parak, and G. U. Nienhaus. 2000. Ligand binding and conformational motions in myoglobin. Nature. 404:205-208.
29. Dantsker, D., C. Roche, U. Samuni, G. Blouin, J. S. Olson, and J. M. Friedman. 2005. The position 68(E11) side chain in myoglobin regulates ligand capture, bond formation with heme iron, and internal movement into the xenon cavities. J. Biol. Chem. 280:38740-38755.
30. Scott, E. E., and Q. H. Gibson. 1997. Ligand migration in sperm whale myoglobin. Biochemistry. 36:11909-11917.
31. Gibson, Q. H., R. Regan, R. Elber, J. S. Olson, and T. E. Carver. 1992. Distal pocket residues affect picosecond ligand recombination in myoglobin. J. Biol. Chem. 267:22022-22034.
32. Rohlfs, R. J., J. S. Olson, and Q. H. Gibson. 1988. A comparison of the geminate recombination kinetics of several monomeric heme proteins. J. Biol. Chem. 263:1803-1813.
33. Case, D. A., and M. Karplus. 1979. Ligands binding to heme proteins. J. Mol. Biol. 132:353-368.
34. Elber, R., and M. Karplus. 1990. Enhanced sampling in molecular dynamics: use of the time-dependent Hartree approximation for a simulation of carbon monoxide diffusion through myoglobin. J. Am. Chem. Soc. 112:9161-9175.
35. Bossa, C., M. Anselmi, D. Roccatano, A. Amadei, B. Vallone, M. Brunori, and A. D. Nola. 2004. Extended molecular dynamics simulation of the carbon monoxide migration in sperm whale myoglobin. Biophys. J. 86:3855-3862.
36. Hummer, G., F. Schotte, and P. A. Anfinrud. 2004. Unveiling functional protein motions with picosecond x-ray crystallography and molecular dynamics simulations. Proc. Natl. Acad. Sci. USA. 101:15330-15334.
37. 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.
38. Zhang, L., and J. Hermans. 1996. Hydrophilicity of cavities in proteins. Proteins. 24:433-438.
39. Humphrey, W., A. Dalke, and K. Schulten. 1996. VMD-Visual Molecular Dynamics. J. Mol. Graph. 14:33-38.
40. Phillips, J. C., R. Braun, W. Wang, J. Gumbart, E. Tajkhorshid, E. Villa, C. Chipot, R. D. Skeel, L. Kale, and K. Schulten. 2005. Scalable molecular dynamics with NAMD. J. Comput. Chem. 26:1781-1802.
41. Gower, M., J. Cohen, J. Phillips, R. Kufrin, and K. Schulten. 2006. Managing biomolecular simulations in a grid environment with NAMD-G. Proc. 2006 TeraGrid Conf. 7 pp.
42. MacKerell, A. Jr., D. Bashford, M. Bellott, R. L. Dunbrack Jr., J. Evanseck, M. J. Field, S. Fischer, J. Gao, H. Guo, S. Ha, D. Joseph, L. Kuchnir, K. Kuczera, F. T. K. Lau, C. Mattos, S. Michnick, T. Ngo, D. T. Nguyen, B. Prodhom, I. W. E. Reiher, B. Roux, M. Schlenkrich, J. Smith, R. Stote, J. 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.
43. Allocatelli, C. T., F. Cutruzzolà, A. Brancaccio, B. Vallone, and M. Brunori. 1994. Engineering Ascaris hemoglobin oxygen affinity in sperm whale myoglobin: role of tyrosine B10. FEBS Lett. 352:63-66.
44. Bossa, C., A. Amadei, I. Daidone, M. Anselmi, B. Vallone, M. Brunori, and A. D. Nola. 2005. Molecular dynamics simulation of sperm whale myoglobin: effects of mutations and trapped CO on the structure and dynamics of cavities. Biophys. J. 89:465-474.
45. Czerminski, R., and R. Elber. 1991. Computational studies of ligand diffusion in globins: I. Leghemoglobin. Proteins. 10:70-80.
46. Salomonsson, L., A. Lee, R. B. Gennis, and P. Brzezinski. 2004. A single-amino-acid lid renders a gas-tight compartmentwithin a membrane-bound transporter. Proc. Natl. Acad. Sci. USA. 101:11617-11621.
47. Buhrke, T., O. Lenz, N. Krauss, and B. Friedrich. 2005. Oxygen tolerance of the H2-sensing [NiFe] hydrogenase from Ralstonia eutropha H16 is based on limited access of oxygen to the active site. J. Biol. Chem. 280:23791-23796.
48. Ghirardi, M. L., J. Cohen, P. King, K. Schulten, K. Kim, and M. Seibert. 2006. [FeFe]-hydrogenases and photobiological hydrogen production. Proc. SPIE: Solar Hydrogen and Nanotechnology. L. Vayssieres, editor. 6340:253-258.
49. Duff, A., A. E. Cohen, P. J. Ellis, J. A. Kuchar, D. B. Langley, E. M. Shepard, D. M. Dooley, H. C. Freeman, and J. M. Guss. 2003. The crystal structure of Pichia pastoris lysyl oxidase. Biochemistry. 42: 15148-15157.
50. Duff, A., D. Trambaiolo, A. Cohen, P. Ellis, G. Juda, E. Shepard, D. Langley, D. Dooley, H. Freeman, and J. Guss. 2004. Using xenon as a probe for dioxygen-binding sites in copper amine oxidases. J. Mol. Biol. 344:599-607.
51. Springer, B. A., S. G. Sligar, J. S. Olson, and G. N. Phillips Jr. 1994. Mechanisms of ligand recognition inmyoglobin. Chem. Rev. 94:699-714.
52. 2, NO, and CO by electrostatic interactions with the bound ligand. J. Biol. Inorg. Chem. 2:544-552.
53. Liong, E. C., Y. Dou, E. E. Scott, J. S. Olson, and G. N. Phillips. 2001. Waterproofing the heme pocket. J. Biol. Chem. 276:9093-9100.
54. Radding, W., and G. N. Phillips Jr. 2004. Kinetic proofreading by the cavity system of myoglobin: protection from poisoning. Bioessays. 26:422-433.
55. Brunori, M., and Q. H. Gibson. 2001. Cavities and packing defects in the structural dynamics of myoglobin. EMBO Rep. 2:676-679.
56. Perutz, M. F., and F. S. Mathews. 1966. An x-ray study of azide methaemoglobin. J. Mol. Biol. 21:199-202.
57. Huang, X., and S. G. Boxer. 1994. Discovery of new ligand binding pathways in myoglobin by random mutagenesis. Nat. Struct. Biol. 1:226-229.
58. Amara, P., P. Andreoletti, H. M. Jouve, and M. J. Field. 2001. Ligand diffusion in the catalase from Proteus mirabilis: a molecular dynamics study. Prot. Sci. 10:1927-1935.
59. Montet, Y., P. Amara, A. Volbeda, X. Vernede, E. C. Hatchikian, M. J. Field, M. Frey, and J. C. Fontecilla-Camps. 1997. Gas access to the active site of Ni-Fe hydrogenase probed by x-ray crystallography and molecular dynamics. Nat. Struct. Biol. 4:523-526.
60. Vojtechovsky, J., K. Chu, J. Berendzen, R. Sweet, and I. Schlichting. 1999. Crystal structures of myoglobin-ligand complexes at near-atomic resolution. Biophys. J. 77:2153-2164.
61. Maurus, R., C. Overall, R. Bogumil, Y. Luo, A. Mauk, M. Smith, and G. Brayer. 1997. A myoglobin variant with a polar substitution in a conserved hydrophobic cluster in the heme binding pocket. Biochim. Biophys. Acta. 1341:1-13.
62. Bolognesi, M., S. Onesti, G. Gatti, A. Coda, P. Ascenzi, and M. Brunori. 1989. Aplysia limacina myoglobin. Crystallographic analysis at 1.6 Å resolution. J. Mol. Biol. 205:529-544.
63. Yang, J., A. P. Kloek, D. E. Goldberg, and F. S. Mathews. 1995. The structure of Ascaris hemoglobin domain I at 2.2 Å resolution: molecular features of oxygen avidity. Proc. Natl. Acad. Sci. USA. 92:4224-4228.
64. Pesce, A., S. Dewilde, L. Kiger, M. Milani, P. Ascenzi, M. C. Marden, M. L. V. Hauwaert, J. Vanfleteren, L. Moens, and M. Bolognesi. 2001. Very high resolution structure of a trematode hemoglobin displaying a TyrB10-TyrE7 heme distal residue pair and high oxygen affinity. J. Mol. Biol. 309:1153-1164.
65. Park, H. J., C. Yang, N. Treff, J. D. Satterlee, and C. Kang. 2002. Crystal structures of unligated and CN-ligated Glycera dibranchiata monomer ferric hemoglobin components III and IV. Proteins. 49: 49-60.
66. Steigemann, W., and E. Weber. 1979. Structure of erythrocruorin in different ligand states refined at 1.4 Å resolution. J. Mol. Biol. 127:309-338.
67. Rizzi, M., J. B. Wittenberg, A. Coda, M. Fasano, P. Ascenzi, and M. Bolognesi. 1994. Structure of the sulfide-reactive hemoglobin from the clam Lucina pectinata. Crystallographic analysis at 1.5 Å resolution. J. Mol. Biol. 244:86-99.
68. Harutyunyan, H. E., T. N. Safonova, I. P. Kuranova, A. N. Popov, A. V. Teplyakov, G. V. Obmolova, A. A. Rusakov, B. K. Vainshtein, G. G. Dodson, J. C. Wilson, and M. F. Perutz. 1995. The structure of deoxy- and oxy-leghaemoglobin from lupin. J. Mol. Biol. 251:104-115.
69. Hargrove, M., J. Barry, E. Brucker, M. Berry, G. Phillips Jr., J. Olson, R. Arredondo-Peter, J. Dean, R. Klucas, and G. Sarath. 1997. Characterization of recombinant soybean leghemoglobin a and apolar distal histidine mutants. J. Mol. Biol. 266:1032-1042.