Protein dynamics explain the allosteric behaviors of hemoglobin

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1784, Issue 9, 2008, Pages 1146-1158

  Yonetani, Takashi ^a   Laberge, Monique ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Allostery; Cooperativity; Hemoglobin (Hb); Molecular dynamics; Oxygen binding; Quaternary structure

Indexed keywords

HEMOGLOBIN; OXYGEN;

ALLOSTERISM; ENTROPY; MOLECULAR DYNAMICS; OXYGEN AFFINITY; PRIORITY JOURNAL; PROTEIN STRUCTURE; REVIEW; STEREOCHEMISTRY; X RAY CRYSTALLOGRAPHY; BIOLOGICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; HUMAN; METABOLISM; THERMODYNAMICS;

ALLOSTERIC REGULATION; CRYSTALLOGRAPHY, X-RAY; HEMOGLOBINS; HUMANS; MODELS, BIOLOGICAL; MODELS, MOLECULAR; OXYGEN; THERMODYNAMICS;

EID: 53149126899     PISSN: 15709639     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbapap.2008.04.025     Document Type: Review

References (68)

1. C. Bohr, Theoretische Behandlung der quantitativen Verhaltnis bei der Sauerstoffaufnahme des Hamoglobin, Zentr. Physiol. 17 (1903) 682-689.
2. C. Bohr, K.A. Hasselbalch, A. Krogh, Ueber einen in biologischer Beziehung wichtigen Einfluss den die Kohlen-sauerspannung des Blutes aufdessen Sauerstoffbindung ubt, Skand. Arch. Physiol. 15 (1904) 401-412.
3. J. Monod, E.F. Jacob, General conclusion: teleonomic mechanism in cellular metabolism, growth, and differentiation, Cold Spring Harbor Sym. Quant. Biol. 26 (1961) 389-401.
4. J. Monod, J. Wyman, J.P. Changeux, On the nature of allosteric transitions: a plausible model, J. Mol. Biol. 12 (1965) 88-118.
5. G.S. Adair, A critical study of the direct method of measuring the osmotic pressure of haemoglobin, Proc. Roy. Soc. (London) Ser. A 108A (1925) 627-637.
6. G.S. Adair, The hemoglobin system. VI. The oxygen dissociation curve of hemoglobin, J. Biol. Chem. 63 (1925) 529-545.
7. D.E. Koshland, G. Nemethy, D. Filmer, Comparison of experimental binding data and theoretical models in proteins containing subunits, Biochemistry 5 (1966) 365-385.
8. H. Muirhead, M.F. Perutz, Structure of haemoglobin - a 3-dimensional Fourier synthesis of reduced human haemoglobin at 5.5 angstrom resolution, Nature 199 (1963) 633-638.
9. M.F. Perutz, Stereochemistry of cooperative effects in haemoglobin, Nature 228 (1970) 726-739.
10. M.F. Perutz, A.J. Wilkinson, M. Paoli, G.G. Dodson, The stereochemical mechanism of the cooperative effects in hemoglobin revisited, Annu. Rev. Biophys. Biomol. Struct. 27 (1998) 1-34.
11. 2-affinity, cooperativity, and Bohr effect by heterotropic allosteric effectors, J. Biol. Chem. 277 (2002) 34508-34520.
12. A. Chanutin, R.R. Curnish, Effects of organic and inorganic phosphates on the oxygen equilibrium of human erythrocytes, Arch. Biochem. Biophys. 121 (1967) 96-102.
13. R. Benesch, R.E. Benesch, The effect of organic phosphates from the human erythrocyte on the allosteric properties of hemoglobin, Biochem. Biophys. Res. Commun. 26 (1967) 162-174.
14. A. Arnone, X-ray diffraction study of binding of 2,3-diphosphoglycerate to human deoxyhaemoglobin, Nature 237 (1972) 146-149.
15. K. Imai, Allosteric Effects in Haemoglobin, Cambridge University Press, Cambridge, 1982.
16. A. Minton, K. Imai, Three-statemodel: aminimal allosteric description of homotropic and heterotropic effects in the binding of ligands to hemoglobin, Proc. Natl. Acad. Sci. U. S. A. 71 (1974) 1418-1421.
17. J. Kister, C. Poyart, S.J. Edelstein, Oxygen-organophosphate linkage in hemoglobin, Biophys. J. 52 (1987) 527-535.
18. M. Marden, B. Bohn, J. Kister, C. Poyart, Effectors of hemoglobin. Separation of allosteric and affinity factors, Biophys. J. 57 (1990) 397-403.
19. I. Lalezari, P. Lalezari, C. Poyart, M. Marden, J. Kister, B. Bohn, GG. Frmi, M.F. Perutz, New effectors of human hemoglobin: structure and function, Biochemistry 29 (1990) 1515-1523.
20. J. Kister, C. Poyart, S.J. Edelstein, An expanded two-state allosteric model for interactions of human hemoglobin A with non-saturating concentrations of 2,3-diphosphoglycerate, J. Biol. Chem. 262 (1987) 12085-12091.
21. A. Tsuneshige, K. Kanaori, U. Samuni, D. Danker, J.M. Friedman, S. Neya, L. Giangiacomo, T. Yonetani, Semihemoglobin, high oxygen affinity dimeric forms of human hemoglobin respond efficiently to allosteric effectors without forming tetramers, J. Biol. Chem. 279 (2004) 48959-48967.
22. R.G. Shulman, S. Ogawa, J.J. Hopfield, Allosteric interpretation of haemoglobin properties, Quart. Rev. Biophys. 8 (1983) 325-420.
23. R.G. Shulman, Spectroscopic contributions to the understanding of hemoglobin function: Implications for structural biology, IUBMB Life 51 (2001) 351-357.
24. W.A. Eaton, E.R. Henry, J. Hofrichter, A. Mozzarelli, Is cooperative oxygen binding by hemoglobin really understood? Nature Struct. Biol. 6 (1999) 351-356.
25. W.A. Eaton, E.R. Henry, J. Hofrichter, S. Bettati, C. Viappiani, A. Mozzarelli, Evolution of allosteric models for hemoglobin, IUBMB Life 59 (2007) 586-599.
26. A. Szabo, M. Karplus, A mathematical model for structure-function relationship in hemoglobin, J. Mol. Biol. 72 (1972) 163-197.
27. 2 carriers, Biophys. Chem. 23 (1986) 215-222.
28. G.K. Ackers, Deciphering the molecular code of hemoglobin allostery, Adv. Protein Chem. 51 (1998) 185-253.
29. T. Yokoyama, S. Neya, A. Tsuneshige, T. Yonetani, S.-Y. Park, J.R.H. Tame, R-state haemoglobin with low affinity: crystal structures of deoxy human and carbonmonoxy horse haemoglobin bound to the effector molecule L35, J. Mol. Biol. 356 (2006) 790-801.
30. J. Baldwin, C. Chothia, Haemoglobin: the structural changes related to ligand binding and its allosteric mechanism, J. Mol. Biol. 129 (1979) 175-220.
31. B.R. Gelin, M. Karplus, Mechanism of tertiary structural-change in hemoglobin, Proc. Natl. Acad. Sci. U. S. A. 74 (1977) 801-805.
32. M.M. Silva, P.H. Rogers, A. Arnone, A third quaternary structure of human hemoglobin A at 1.7-Å resolution, J. Biol. Chem. 267 (1992) 17248-17256.
33. M.K. Safo, D.J. Abraham, The enigma of the liganded hemoglobin end state: a novel quaternary structure of human carbonmonoxy hemoglobin, Biochemistry 44 (2005) 8347-8359.
34. J.R.H. Tame, What is the true structure of liganded haemoglobin? Trends Biochem. Sci. 24 (1999) 372-277.
35. J.A. Lukin, G. Kontaxis, V. Simplaceanu, Y. Yuan, A. Bax, C. Ho, Quaternary structure of hemoglobin in solution, Proc. Natl. Scad. Sci. U. S. A. 100 (2003) 517-520.
36. T.C. Mueser, PH. Rogers, A. Arnone, Interface sliding as illustrated by the multiple quaternary structures of liganded hemoglobin, Biochemistry 39 (2000) 15353-15364.
37. high quaternary transitions, Biochemistry 44 (2005) 6101-6121.
38. E.S. Peterson, J.M. Friedman, Possible allosteric communication pathway identified through a resonance Raman study of four β37 mutants of human hemoglobin A, Biochemistry 37 (1998) 4346-4357.
39. M. Laberge, T. Yonetani, Molecular dynamics simulations of hemoglobin A in different quaternary states and bound to DPG: perturbation of tertiary conformations and HbA dynamics in the absence of homotropic effects, Biophys. J. 94 (2008) 1-15.
40. M. Laberge, T. Yonetani, J. Fidy, Normal coordinate structural decomposition of the heme distortions of hemoglobin in various quaternary states and bound to allosteric effectors, Mol. Diversity 7 (2003) 15-23.
41. T. Yonetani, A. Tsuneshige, Y. Zhou, X. Chen, Electron paramagnetic resonance and oxygen binding studies of α-nitrosyl hemoglobin, J. Biol. Chem. 273 (1998) 20323-20333.
42. T. Yonetani, H. Yamamoto, T. Iizuka, Studies on cobalt-myoglobin and hemoglobin III. Electron paramagnetic resonance studies of the reversible oxygen binding to cobalt myoglobins and cobalt hemoglobins, J. Biol. Chem. 249 (1974) 2168-2174.
43. B. Shaanan, Structure of human oxyhaemoglobin at 2.1 Å rsolution, J. Mol. Biol. 171 (1983) 31-59.
44. H. Frauenfelder, F. Parak, R.D. Young, Conformational substates in proteins, Annu. Rev. Biophys. Biophys. Chem. 17 (1988) 451-479.
45. M. Brunori, Q.H. Gibson, Cavities and packing defects in the structural dynamics of myoglobin, EMBO Reports 2 (2001) 674-679.
46. B.A. Springer, S.G. Sligar, J.S. Olson, G.N. Phillips, Mechanism of ligand recognition in myoglobin, Chem. Rev. 94 (1994) 699-714.
47. J.J. Hopfield, Relation between structure, cooperativity and spectra in a model of hemoglobin action, J. Mol. Biol. 77 (1973) 207-222.
48. I. Messana, M. Angeletti, M. Castagnola, G. De Sanctis, E. Di Stasio, B. Giardina, S. Puccinrelli, M. Coletta, Thermodynamics of inositol hexakisphosphate interaction with human oxyhemoglobin, J. Biol.Chem. 273 (1966) 15329-15334.
49. M. Fujii, H. Hori, G. Miyazaki, H. Morimoto, T. Yonetani, The porphyrin-iron hybrid hemoglobins. Absence of the Fe-His bonds in one type of subunits favors a deoxylike structure with low oxygen affinity, J. Biol. Chem. 268 (1993) 15386-15393.
50. N. Shibayama, H. Morimoto, G. Miyazaki, Oxygen equilibrium study and light absorption spectra of Ni(II)-Fe(II) hybrid hemoglobins, J.Mol. Biol.192 (1986) 323-329.
51. N. Shibayama, T. Inubushi, H. Morimoto, T. Yonetani, Proton nuclear magnetic resonance and spectrophotometric studies of nickel(II)-iron(II) hybrid hemoglobins, Biochemistry 26 (1987) 2194-2101.
52. G. Miyazaki, H. Morimoto, K.-M. Yun, S.-Y. Park, A. Nakagawa, H. Minagawa, N. Shibayama, Magnesium (II) and Zn (II)-protoporphyrin IX's stabilize the lowest oxygen affinity state of human hemoglobin evenmore than deoxyheme, J. Mol. Biol. 292 (1999) 1121-1136.
53. S.-Y. Park, A. Nakagawa, H. Morimoto, High-resolution crystal structure of magnesium (MgII)-iron(FeII) hybrid hemoglobin with liganded beta subunits, J. Mol. Biol. 255 (1996) 726-734.
54. S.W. Englander, N. Kallenbach, Hydrogen exchange and structural dynamics of proteins, Annu. Rev. Biophys. Biomol. Struct. 25 (1996) 213-258.
55. J.R. Labowicz, G. Weber, Quenching of protein fluorescence by oxygen. Detection of structural fluctuations in proteins on the nanosecond time scale, Biochemistry 12 (1983) 4171-4179.
56. H. Frauenfelder, McMahon, R.H. Austin, K. Chu, J.T. Groves, The role of structure, energy landscape, dynamics, and allostery in the enzymic function of myoglobin, Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 2370-2374.
57. T. Liu, S.T. Witten, V.J. Hilser, Functional residues serve a dominant role in mediating the cooperativity of protein ensemble, Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 4347-4352.
58. V.A. Jarymowycz, M.J. Stone, Fast time scale dynamics of protein backbones: NMR relaxation methods, applications, and functional consequences, Chem. Rev. 106 (2006) 1624-1671.
59. I. Igumenova, K.K. Frederick, A.J. Wand, Characterization of the fast dynamics of protein amino acid side chains using NMR relaxation in solution, Chem. Rev. 106 (2006) 1672-1699.
60. K.K. Frederick, M. Marlow, K.G. Valentine, A.J. Wand, Conformational entropy in molecular recognition by proteins, Nature 448 (2007) 325-329.
61. J. Wyman, Heme proteins, Adv. Protein Chem. 4 (1948) 407-531.
62. M. Kotani, Fluctuation in quaternary structure of proteins and cooperative ligand binding. I, Prog. Theor. Phys. Suppl. (1968) 233-241 Extra No.
63. L. Mouaward, D. Perahia, C.H. Robert, C. Guilbert, New insights into the allosteric mechanism of human hemoglobin from molecular dynamics simulations, Biophys. J. 82 (2002) 3224-3245.
64. J. Gao, K. Kuczera, B. Tider, M. Karplus, Hidden thermodynamics of mutant proteins: a molecular dynamics analysis, Science 244 (1989) 1069-1072.
65. M. Saito, I. Okazaki, A 45-ns molecular dynamics simulation of hemoglobin in water by vectorizing and parallelizing COSMOS90 on the earth simulator: dynamics of tertiary and quaternary structures, J. Comp. Chem. 28 (2007) 1129-1136.
66. I. Koevesi, G. Schay, T. Yonetani, M. Laberge, J. Fidy, High pressure reveals that the stability of interdimeric contacts in the R- and T-state of HbA is influenced by allosteric effectors: insights from computational simulations, Biochim. Biophys. Acta-Proteins & Proteomics 1764 (2006) 516-521.
67. N. Ramadas, J.M. Rifkind, Molecular dynamics of human methemoglobin: the transmission of conformational information between subunits in an ab dimmer, Biophys. J. 76 (1999) 1796-1811.
68. R.E. Alcantra, C. Xu, T.G. Spiro, V. Guallar, A quantum-chemical picture of hemoglobin affinity, Proc. Natl. Acad. Sci. U. S. A. 194 (2007) 18451-18455.