Hemoglobin Bohr effects: Atomic origin of the histidine residue contributions

Biochemistry

Volumn 52, Issue 47, 2013, Pages 8539-8555

  Zheng, Guishan ^a   Schaefer, Michael ^b   Karplus, Martin ^a,c  

^a HARVARD UNIVERSITY   (United States)

^b NOVARTIS PHARMA AG   (Switzerland)

^c UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DOMINANT CONTRIBUTIONS; EXPERIMENTAL VALUES; HIGH-RESOLUTION STRUCTURES; HISTIDINE RESIDUES; LINEAR RESPONSE APPROXIMATION; MONTE CARLO SAMPLING; PHYSIOLOGICAL FUNCTIONS; POISSON-BOLTZMANN EQUATIONS;

ALKALINITY; AMINO ACIDS; MONTE CARLO METHODS;

HEMOGLOBIN;

DEOXYHEMOGLOBIN; HEMOGLOBIN; HEMOGLOBIN A; HISTIDINE; OXYHEMOGLOBIN;

ARTICLE; BOHR EFFECT; CALCULATION; CHEMICAL INTERACTION; CRYSTAL STRUCTURE; MONTE CARLO METHOD; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OXYGEN AFFINITY; PH; PKA; POISSON BOLTZMANN EQUATION; PRIORITY JOURNAL; PROTEIN STRUCTURE; PROTON TRANSPORT; STATIC ELECTRICITY;

CARBOXYHEMOGLOBIN; COMPUTATIONAL BIOLOGY; DATABASES, PROTEIN; HEMOGLOBIN A; HEMOGLOBIN SUBUNITS; HEMOGLOBINS; HISTIDINE; HUMANS; HYDROGEN-ION CONCENTRATION; KINETICS; MONTE CARLO METHOD; OXYHEMOGLOBINS; POISSON DISTRIBUTION; PROTEIN CONFORMATION;

EID: 84888614735     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi401126z     Document Type: Article

References (59)

1. Antonini, E. and Brunori, M. (1970) Hemoglobin Annu. Rev. Biochem. 39, 977-1042
2. Bohr, C. (1903) Theoretische Behandlung der quantitativen Verhältnisse der Kohlensäurebindung des Hämoglobins Zentralblatt Für Physiologie XVII, 713-716
3. Bohr, C., Hasselbalch, K., and Krogh, A. (1904) About a new biological relation of high importance that the blood carbonic acid tension exercises on its oxygen binding Skandinavisches Archiv Fur Physiologie 16, 404-412
4. Edsall, J. T. (1980) Hemoglobin and the origins of the concept of allosterism Federation Proceedings 39, 226-235
5. Christiansen, J., Douglas, C., and Haldane, J. (1914) The absorption and discussion of carbon dioxide by human blood Journal of Physiology-London 48, 244-271
6. Brunori, M. (2012) The Bohr effect before Perutz Biochem. Mol. Biol. Educ. 40, 297-299
7. Rossifanelli, A., Antonini, E., and Caputo, A. (1964) Hemoglobin and Myoglobin Adv. Protein Chem. 19, 73-222
8. Kilmartin, J. and Rossi-Bernardi, L. (1973) Interaction of hemoglobin with hydrogen ions, carbon dioxide, and organic phosphates Physiol. Rev. 53, 836-890
9. Riggs, A. F. (1988) The Bohr effect Annu. Rev. Physiol. 50, 181-204
10. Perutz, M. F. (1970) Stereochemistry of cooperative effects in hemoglobin Nature 228, 726-734
11. Perutz, M. F. and Ten Eyck, L. F. (1970) Stereochemistry of cooperative effects in hemoglobin Cold Spring Harbor Symp. Quantum Biol. 36, 295-310
12. Szabo, A. and Karplus, M. (1972) Mathematical model for structure-function relations in hemoglobin J. Mol. Biol. 72, 163-197
13. Szabo, A. and Karplus, M. (1972) Mathematical model for structure-function relationships in hemoglobin Biochem. Biophys. Res. Commun. 46, 855-860
14. Monod, J., Wyman, J., and Changeux, J. P. (1965) On the nature of allosteric transitions: a plausible model J. Mol. Biol. 12, 88-118
15. Roughton, F. J. W. and Lyster, R. L. J. (1965) Hvalradets Skrifter 48, 185-198
16. Lee, A. W. M. and Karplus, M. (1983) Structure-specific model of hemoglobin cooperativity Proc. Natl. Acad. Sci. U.S.A. 80, 7055-7059
17. Henry, E. R., Bettati, S., Hofrichter, J., and Eaton, W. A. (2002) A tertiary two-state allosteric model for hemoglobin. Biophys. Chem. 98.
18. Eaton, W. A., Henry, E., Hofrichter, J., Bettati, S., Viappiani, C., and Mozzarelli, A. (2007) Evolution of allosteric models for hemoglobin IUBMB Life 59, 586-599
19. Ho, C. and Yuan, Y. Haemoglobin: Cooperativity in Protein-Ligand Interactions; Encyclopedia of Life Sciences ed.; John Wiley Sons, Ltd, 2010; pp 1-6.
20. Fang, T.-Y., Zou, M., Simplaceanu, V., Ho, N. T., and Ho, C. (1999) Assessment of roles of surface histidyl residues in the molecular basis of the bohr effect and of beta 143 histidine in the binding of 2,3-bisphosphoglycerate in human normal adult hemoglobin Biochemistry 38, 13423-13432
21. Bashford, D. and Karplus, M. (1990) pKas of ionizable groups in proteins-atomic detail from a continuum electrostatic model Biochemistry 29, 10219-10225
22. Lim, C., Bashford, D., and Karplus, M. (1991) Absolute pKa calculations with continuum dielectric methods J. Phys. Chem. 95, 5610-5620
23. Bashford, D., Case, D. A., Dalvit, C., Tennant, L., and Wright, P. E. (1993) Electrostatic calculations of side-chain pKa values in myoglobin and comparison with NMR data for histidines Biochemistry 32, 8045-8056
24. Antosiewicz, J., Mccammon, J., and Gilson, M. K. (1994) Prediction of pH-dependent properties of proteins J. Mol. Biol. 238, 415-436
25. Yang, A. S., Gunner, M. R., Sampogna, R., Sharp, K., and Honig, B. (1993) On the calculation of pKas in proteins Proteins 15, 252-65
26. Schaefer, M., Sommer, M., and Karplus, M. (1997) pH-dependence of protein stability: Absolute electrostatic free energy differences between conformations J. Phys. Chem. B 101, 1663-1683
27. Simonson, T., Carlsson, J., and Case, D. A. (2004) Proton binding to proteins: pKa calculations with explicit and implicit solvent models J. Am. Chem. Soc. 126, 4167-4180
28. Riccardi, D., Schaefer, P., and Cui, Q. (2005) pKa calculations in solution and proteins with QM/MM free energy perturbation simulations: a quantitative test of QM/MM protocols J. Phys. Chem. B 109, 17715-17733
29. Zheng, L., Chen, M., and Yang, W. (2008) Random walk in orthogonal space to achieve efficient free-energy simulation of complex systems Proc. Natl. Acad. Sci. U.S.A. 105, 20227-20232
30. Khandogin, J. and Brooks, C. L. (2005) Constant pH molecular dynamics with proton tautomerism Biophys. J. 89, 141-157
31. Arthur, E. J., Yesselman, J. D., and Brooks, C. L. (2011) Predicting extreme pKa shifts in staphylococcal nuclease mutants with constant pH molecular dynamics Proteins 79, 3276-3286
32. Zhang, B. W., Brunetti, L., and Brooks, C. L., III (2011) Probing pH-dependent dissociation of HdeA dimers J. Am. Chem. Soc. 133, 19393-19398
33. Matthew, J. B., Gurd, F. R. N., Garcia-Moreno, B. E., Flanagan, M. A., March, K. L., and Shire, S. J. (1985) pH-dependent processes in protein Crit. Rev. Biochem. Mol. Biol. 18, 91-197
34. Sommers, M. Electrostatic modeling of biological macromolecules in solution; Ph.D. thesis; Harvard University, 1995.
35. Vriend, G. (1990) WHAT IF: A molecular modeling and drug design program J. Mol. Graphics Modell. 8, 52-56
36. Bashford, D. and Karplus, M. (1991) Multiple-site titration curves of proteins-an analysis of exact and approximate methods for their calculation J. Phys. Chem. 95, 9556-9561
37. Tanokura, M., Tasumi, M., and Miyazawa, T. (1976) 1H Nuclear magnetic resonance studies of histidine-containing di- and tripeptides. Estimation of the effects of charged groups on the pKa value of the imidazole ring Biopolymers 15, 393-401
38. Bash, P. A., Field, M. J., Davenport, R. C., Petsko, G. A., Ringe, D., and Karplus, M. (1991) Computer-simulation and analysis of the reaction pathway of triosephosphate isomerase Biochemistry 30, 5826-5832
39. Cui, Q. and Karplus, M. (2002) Quantum mechanics/molecular mechanics studies of triosephosphate isomerase-catalyzed reactions: Effect of geometry and tunneling on proton-transfer rate constants J. Am. Chem. Soc. 124, 3093-3124
40. Brooks, B. R., Bruccoleri, R. E., Olafson, B. D., States, D. J., Swaminathan, S., and Karplus, M. (1983) CHARMM- a program for macromolecular energy, minimization, and dynamics calculations J. Comput. Chem. 4, 187-217
41. Chu, J. W., Trout, B. L., and Brooks, B. R. (2003) A super-linear minimization scheme for the nudged elastic band method J. Chem. Phys. 119, 12708-12717
42. Brooks, B. R. 2009, CHARMM: the biomolecular simulation program J. Comput. Chem. 30, 1545-1614
43. Davis, M. E., Madura, J. D., Luty, B. A., and McCammon, J. A. (1991) UHBD 4.1 Comput. Phys. Commun. 62, 187
44. Beroza, P., Fredkin, D. R., Okamura, M. Y., and Feher, G. (1991) Protonation of interacting residues in a protein by a Monte Carlo method: application to lysozyme and the photosynthetic reaction center of Rhodobacter sphaeroides Proc. Natl. Acad. Sci. U.S.A. 88, 5804-5808
45. Park, S.-Y., Yokoyama, T., Shibayama, N., Shiro, Y., and Tame, J. R. (2006) 1.25 Å resolution crystal structures of human haemoglobin in the oxy, deoxy and carbonmonoxy forms J. Mol. Biol. 360, 690-701
46. Shaanan, B. (1983) Structure of human oxyhaemoglobin at 2.1 Å resolution resolution J. Mol. Biol. 171, 31-59
47. Silva, M., Rogers, P., and Arnone, A. (1992) A third quaternary structure of human hemoglobin a at 1.7Å resolution J. Biol. Chem. 267, 17248-17256
48. Safo, M. and Abraham, D. (2005) The enigma of the liganded hemoglobin end state: a novel quaternary structure of human carbonmonoxy hemoglobin Biochemistry 44, 8347-8359
49. Caves, L. S. D., Evanseck, J. D., and Karplus, M. (1998) Locally accessible conformations of proteins: Multiple molecular dynamics simulations of crambin Protein Sci. 7, 649-666
50. Kilmarti, J. V. and Rossi-Bernardi, L. (1973) Interaction of hemoglobin with hydrogen-ions, carbon-dioxide, and organic phosphates Physiol. Rev. 53, 836-890
51. Rao, M. J. and Acharya, A. S. (1992) Contribution of the gamma-carboxyl group of Glu43(beta) to the alkaline Bohr effect of hemoglobin A Biochemistry 31, 7231-7236
52. Simonson, T., Archontis, G., and Karplus, M. (2002) Free energy simulations come of age: Protein-ligand recognition Acc. Chem. Res. 35, 430-437
53. Baker, N., Sept, D., Joseph, S., and Holst, M. J. (2001) Electrostatics of nanosystems: application to microtubules and the ribosome Proc. Natl. Acad. Sci. U.S.A. 98, 10037-10041
54. Schaefer, M. and Karplus, M. (1996) A comprehensive analytical treatment of continuum electrostatics J. Phys. Chem. 100, 1578-1599
55. Schaefer, M., Bartels, C., and Karplus, M. (1998) Solution conformations and thermodynamics of structured peptides: Molecular dynamics simulation with an implicit solvation model J. Mol. Biol. 284, 835-848
56. Fermi, G., Perutz, M., Shaanan, B., and Fourme, R. (1984) The crystal structure of human deoxyhaemoglobin at 1.74 Å resolution J. Mol. Biol. 175, 159-174
57. Kavanaugh, J., Moo-Penn, W., and Arnone, A. (1993) Accommodation of insertions in helices: the mutation in hemoglobin Catonsville (Pro 37 alpha-Glu-Thr 38 alpha) generates a 3(10)->alpha bulge Biochemistry 32, 2509-2513
58. Chan, N., Kavanaugh, J., Rogers, P., and Arnone, A. (2004) Crystallographic analysis of the interaction of nitric oxide with quaternary-T human hemoglobin Biochemistry 43, 118-132
59. Kavanaugh, J., Rogers, P., and Arnone, A. (2005) Crystallographic evidence for a new ensemble of ligand-induced allosteric transitions in hemoglobin: the T-to-T(high) quaternary transitions Biochemistry 44, 6101-6121