Hydrophobic effect drives oxygen uptake in myoglobin via histidine E7

Journal of Biological Chemistry

Volumn 288, Issue 9, 2013, Pages 6754-6762

  Boechi, Leonardo ^a,d   Arrar, Mehrnoosh ^b,d   Martí, Marcelo A ^a   Olson, John S ^c   Roitberg, Adrián E ^b   Estrin, Darío A ^a  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^b UNIVERSITY OF FLORIDA   (United States)

^c RICE UNIVERSITY   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; CONCEPTUAL FRAMEWORKS; ENERGY PROFILE; HISTIDINE RESIDUES; HYDROPHOBIC EFFECT; HYDROPHOBIC SITES; MOLECULAR DYNAMICS SIMULATIONS; OPEN CONFORMATION; OXYGEN MIGRATION; OXYGEN UPTAKE; PROTONATION STATE; RATE ENHANCEMENT; SIDE-CHAINS; SIGNIFICANT DIFFERENCES;

AMINO ACIDS; HYDROPHOBICITY; LIGANDS; MOLECULAR DYNAMICS; OXYGEN; PROTONATION;

CONFORMATIONS;

ALANINE; HISTIDINE; HISTIDINE E7; MYOGLOBIN; OXYGEN; TRYPTOPHAN; UNCLASSIFIED DRUG;

ARTICLE; CHEMICAL STRUCTURE; ENERGY TRANSFER; HYDROPHOBICITY; MOLECULAR DYNAMICS; OXYGEN CONSUMPTION; OXYGEN TRANSPORT; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTON TRANSPORT;

ANIMALS; HISTIDINE; HUMANS; HYDROGEN-ION CONCENTRATION; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MYOGLOBIN; OXYGEN; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY;

EID: 84874770897     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.426056     Document Type: Article

References (62)

1. Perutz, M. F., Rossman, M. G., Cullis, A. F., Muirhead, H., Will, G., and North, A. C. (1960) Structure of haemoglobin: a three-dimensional Fourier synthesis at 5.5-A. resolution, obtained by x-ray analysis. Nature 185, 416-422
2. Kendrew, J. C., Dickerson, R. E., Strandberg, B. E., Hart, R. G., Davies, D. R., Phillips, D. C., and Shore, V. C. (1960) Structure of myoglobin: A threedimensional Fourier synthesis at 2 A2 resolution. Nature 185, 422-427
3. Perutz, M. F., and Mathews, F. S. (1966) An x-ray study of azide methaemoglobin. J. Mol. Biol. 21, 199-202
4. Frauenfelder, H., McMahon, B. H., and Fenimore, P. W. (2003) Myoglobin: the hydrogen atom of biology and a paradigm of complexity. Proc. Natl. Acad. Sci. U.S.A. 100, 8615-8617
5. Elber, R. (2010) Ligand diffusion in globins: Simulations versus Experiment. Curr. Opin. Struct. Biol. 20, 162-167
6. Yang, F., and Phillips, G. N. (1996) Crystal structures of CO-, deoxy- and met-myoglobins at various pH values. J. Mol. Biol. 256, 762-774
7. Rabenstein, B., and Knapp, E. W. (2001) Calculated pH-dependent population and protonation of carbon-monoxy-myoglobin conformers. Biophys. J. 80, 1141-1150
8. Scott, E. E., Gibson, Q. H., and Olson, J. S. (2001) Mapping the pathways for O2 entry into and exit from myoglobin. J. Biol. Chem. 276, 5177-5188
9. Milani, M., Pesce, A., Nardini, M., Ouellet, H., Ouellet, Y., Dewilde, S., Bocedi, A., Ascenzi, P., Guertin, M., Moens, L., Friedman, J. M., Wittenberg, J. B., and Bolognesi, M. (2005) Structural bases for heme binding and diatomic ligand recognition in truncated hemoglobins. J. Inorg. Biochem. 99, 97-109
10. Ouellet, H., Milani, M., LaBarre, M., Bolognesi, M., Couture, M., and Guertin, M. (2007) The roles of Tyr(CD1) and Trp(G8) in Mycobacterium tuberculosis truncated hemoglobin O in ligand binding and on the heme distal site architecture. Biochemistry 46, 11440-11450
11. Olson, J. S., Soman, J., and Phillips, G. N. (2007) Ligand pathways in myoglobin: a review of Trp cavity mutations. IUBMB Life 59, 552-562
12. Birukou, I., Soman, J., and Olson, J. S. (2011) Blocking the gate to ligand entry in human hemoglobin. J. Biol. Chem. 286, 10515-10529
13. Tian, W. D., Sage, J. T., and Champion, P. M. (1993) Investigations of ligand association and dissociation rates in the "open" and "closed" states of myoglobin. J. Mol. Biol. 233, 155-166
14. Esquerra, R. M., Jensen, R. A., Bhaskaran, S., Pillsbury, M. L., Mendoza, J. L., Lintner, B. W., Kliger, D. S., and Goldbeck, R. A. (2008) The pH dependence of heme pocket hydration and ligand rebinding kinetics in photodissociated carbonmonoxymyoglobin. J. Biol. Chem. 283, 14165-14175
15. Coletta, M., Ascenzi, P., Traylor, T. G., and Brunori, M. (1985) Kinetics of carbon monoxide binding to monomeric hemoproteins. Role of the proximal histidine. J. Biol. Chem. 260, 4151-4155
16. Smith, R. D., Blouin, G. C., Johnson, K. A., Phillips, G. N., Jr., and Olson, J. S. (2010) Straight-chain alkyl isocyanides open the distal histidine gate in crystal structures of myoglobin. Biochemistry 49, 4977-4986
17. Blouin, G. C., Schweers, R. L., and Olson, J. S. (2010) Alkyl isocyanides serve as transition state analogues for ligand entry and exit in myoglobin. Biochemistry 49, 4987-4997
18. Salter, M. D., Blouin, G. C., Soman, J., Singleton, E. W., Dewilde, S., Moens, L., Pesce, A., Nardini, M., Bolognesi, M., and Olson, J. S. (2012) Determination of ligand pathways in globins: apolar tunnels versus polar gates. J. Biol. Chem. 287, 33163-33178
19. Schmidt, M., Nienhaus, K., Pahl, R., Krasselt, A., Anderson, S., Parak, F., Nienhaus, G. U., and Srajer, V. (2005) Ligand migration pathway and protein dynamics in myoglobin:Atime-resolved crystallographic study on L29W MbCO. Proc. Natl. Acad. Sci. U.S.A. 102, 11704-11709
20. Elber, R., and Karplus, M. (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
21. Brunori, M., and Gibson, Q. H. (2001) Cavities and packing defects in the structural dynamics of myoglobin. EMBO Rep. 2, 674-679
22. Bourgeois, D., Vallone, B., Schotte, F., Arcovito, A., Miele, A. E., Sciara, G., Wulff, M., Anfinrud, P., and Brunori, M. (2003) Complex landscape of protein structural dynamics unveiled by nanosecond Laue crystallography. Proc. Natl. Acad. Sci. U.S.A. 100, 8704-8709
23. Tomita, A., Sato, T., Ichiyanagi, K., Nozawa, S., Ichikawa, H., Chollet, M., Kawai, F., Park, S. Y., Tsuduki, T., Yamato, T., Koshihara, S. Y., and Adachi, S. (2009) Visualizing breathing motion of internal cavities in concert with ligand migration in myoglobin. Proc. Natl. Acad. Sci. U.S.A. 106, 2612-2616
24. Hummer, G., Schotte, F., and Anfinrud, P. A. (2004) Unveiling functional protein motions with picosecond x-ray crystallography and molecular dynamics simulations. Proc. Natl. Acad. Sci. U.S.A. 101, 15330-15334
25. Lim, M., Jackson, T. A., and Anfinrud, P. A. (1997) Ultrafast rotation and trapping of carbon monoxide dissociated from myoglobin. Nat. Struct. Biol. 4, 209-214
26. Bossa, C., Amadei, A., Daidone, I., Anselmi, M., Vallone, B., Brunori, M., and Di Nola, A. (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
27. Ceccarelli, M., Anedda, R., Casu, M., and Ruggerone, P. (2008) CO escape from myoglobin with metadynamics simulations. Proteins 71, 1231-1236
28. Ostermann, A., Waschipky, R., Parak, F. G., and Nienhaus, G. U. (2000) Ligand binding and conformational motions in myoglobin. Nature 404, 205-208
29. Maragliano, L., Cottone, G., Ciccotti, G., and Vanden-Eijnden, E. (2010) Mapping the network of pathways of CO diffusion in myoglobin. J. Am. Chem. Soc. 132, 1010-1017
30. Cohen, J., Arkhipov, A., Braun, R., and Schulten, K. (2006) Imaging the migration pathways for O2, CO, NO, and Xe inside myoglobin. Biophys. J. 91, 1844-1857
31. Cohen, J., Olsen, K. W., and Schulten, K. (2008) Finding gas migration pathways in proteins using implicit ligand sampling. Methods Enzymol. 437, 439-457
32. Shadrina, M. S., English, A. M., and Peslherbe, G. H. (2012) Effective simulations of gas diffusion through kinetically accessible tunnels in multisubunit proteins: O2 pathways and escape routes in T-state deoxyhemoglobin. J. Am. Chem. Soc. 134, 11177-11184
33. Scott, E. E., and Gibson, Q. H. (1997) Ligand migration in sperm whale myoglobin. Biochemistry 36, 11909-11917
34. Ruscio, J. Z., Kumar, D., Shukla, M., Prisant, M. G., Murali, T. M., and Onufriev, A. V. (2008) Atomic level computational identification of ligand migration pathways between solvent and binding site in myoglobin. Proc. Natl. Acad. Sci. U.S.A. 105, 9204-9209
35. Gordon, J. C., Myers, J. B., Folta, T., Shoja, V., Heath, L. S., and Onufriev, A. (2005) H++: a server for estimating pKas and adding missing hydrogens to macromolecules. Nucleic Acids Res. 33, W368-371
36. Hornak, V., Abel, R., Okur, A., Strockbine, B., Roitberg, A., and Simmerling, C. (2006) Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins 65, 712-725
37. Bayly, C. I., Cieplak, P., Cornell, W., and Kollman, P. A. (1993) A wellbehaved electrostatic potential based method using charge restraints for deriving atomic charges: the RESP model. J. Phys. Chem. 97, 10269-10280
38. Boechi, L., Martì, M. A., Vergara, A., Sica, F., Mazzarella, L., Estrin, D. A., and Merlino, A. (2011) Protonation of histidine 55 affects the oxygen access to heme in the alpha chain of the hemoglobin from the Antarctic fish Trematomus bernacchii. IUBMB Life 63, 175-182
39. Martí, M. A., González Lebrero, M. C., Roitberg, A. E., and Estrin, D. A. (2008) Bond or cage effect: how nitrophorins transport and release nitric oxide. J. Am. Chem. Soc. 130, 1611-1618
40. Martí, M. A., Bidon-Chanal, A., Crespo, A., Yeh, S. R., Guallar, V., Luque, F. J., and Estrin, D. A. (2008) Mechanism of product release in NO detoxification from Mycobacterium tuberculosis truncated hemoglobin N. J. Am. Chem. Soc. 130, 1688-1693
41. Capece, L., Marti, M. A., Crespo, A., Doctorovich, F., and Estrin, D. A. (2006) Heme protein oxygen affinity regulation exerted by proximal effects. J. Am. Chem. Soc. 128, 12455-12461
42. Boechi, L., Mañez, P. A., Luque, F. J., Marti, M. A., and Estrin, D. A. (2010) Unraveling the molecular basis for ligand binding in truncated hemoglobins: the trHbO Bacillus subtilis case. Proteins 78, 962-970
43. Boechi, L., Martí, M. A., Milani, M., Bolognesi, M., Luque, F. J., and Estrin, D. A. (2008) Structural determinants of ligand migration in Mycobacterium tuberculosis truncated hemoglobin O. Proteins 73, 372-379
44. Pesce, A., Nardini, M., Dewilde, S., Capece, L., Martí, M. A., Congia, S., Salter, M. D., Blouin, G. C., Estrin, D. A., Ascenzi, P., Moens, L., Bolognesi, M., and Olson, J. S. (2011) Ligand migration in the apolar tunnel of Cerebratulus lacteus mini-hemoglobin. J. Biol. Chem. 286, 5347-5358
45. Bidon-Chanal, A., Martí, M. A., Crespo, A., Milani, M., Orozco, M., Bolognesi, M., Luque, F. J., and Estrin, D. A. (2006) Ligand-induced dynamical regulation of NO conversion in Mycobacterium tuberculosis truncated hemoglobin-N. Proteins 64, 457-464
46. Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., and Klein, M. L. (1983) Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79, 926-936
47. Ryckaert, J. P., Ciccotti, G., and Berendsen, H. (1977) Numerical integration of the cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J. Comput. Phys. 23, 327-341
48. Berendsen, H. J. C., Postma, J. P. M., Van Gunsteren, W. F., DiNola, A., and Haak, J. R. (1984) Molecular dynamics with coupling to an external bath. J. Chem. Phys. 81, 3684-3690
49. Jarzynski, C. (1997) Nonequilibrium Equality for Free Energy Differences. Phys. Rev. Lett. 78, 2690-2693
50. Xiong, H., Crespo, A., Marti, M., Estrin, D., and Roitberg, A. E. (2006) Free Energy Calculations with Non-Equilibrium Methods: Applications of the Jarzynski Relationship. Theor. Chem. Acc. 116, 338-346
51. Meuwly, M., Becker, O. M., Stote, R., and Karplus, M. (2002)NOrebinding to myoglobin: a reactive molecular dynamics study. Biophys. Chem. 98, 183-207
52. Gore, J., Ritort, F., and Bustamante, C. (2003) Bias and error in estimates of equilibrium free-energy differences from nonequilibrium measurements. Proc. Natl. Acad. Sci. U.S.A. 100, 12564-12569
53. Jewsbury, P., and Kitagawa, T. (1994) The distal residue-CO interaction in carbonmonoxy myoglobins: a molecular dynamics study of two distal histidine tautomers. Biophys. J. 67, 2236-2250
54. De Biase, P. M., Paggi, D. A., Doctorovich, F., Hildebrandt, P., Estrin, D. A., Murgida, D. H., and Marti, M. A. (2009) Molecular basis for the electric field modulation of cytochrome c structure and function. J. Am. Chem. Soc. 131, 16248-16256
55. Nadra, A. D., Martí, M. A., Pesce, A., Bolognesi, M., and Estrin, D. A. (2008) Exploring the molecular basis of heme coordination in human neuroglobin. Proteins 71, 695-705
56. Capece, L., Marti, M. A., Bidon-Chanal, A., Nadra, A., Luque, F. J., and Estrin, D. A. (2009) High pressure reveals structural determinants for globin hexacoordination: neuroglobin and myoglobin cases. Proteins 75, 885-894
57. Birukou, I., Maillett, D. H., Birukova, A., and Olson, J. S. (2011) Modulating distal cavities in the α and β subunits of human HbA reveals the primary ligand migration pathway. Biochemistry 50, 7361-7374
58. Wittenberg, J. B., Bolognesi, M., Wittenberg, B. A., and Guertin, M. (2002) Truncated hemoglobins: a new family of hemoglobins widely distributed in bacteria, unicellular eukaryotes, and plants. J. Biol. Chem. 277, 871-874
59. Milani, M., Pesce, A., Ouellet, Y., Ascenzi, P., Guertin, M., and Bolognesi, M. (2001) Mycobacterium tuberculosis hemoglobin N displays a protein tunnel suited for O2 diffusion to the heme. EMBO J. 20, 3902-3909
60. Cazade, P. A., and Meuwly, M. (2012) Oxygen migration pathways in NO-bound truncated hemoglobin. Chemphyschem 13, 4276-4286
61. Bossa, C., Anselmi, M., Roccatano, D., Amadei, A., Vallone, B., Brunori, M., and Di Nola, A. (2004) Extended molecular dynamics simulation of the carbon monoxide migration in sperm whale myoglobin. Biophys. J. 86, 3855-3862
62. Cohen, J., and Schulten, K. (2007) O2 migration pathways are not conserved across proteins of a similar fold. Biophys. J. 93, 3591-3600