Evolution of allosteric models for hemoglobin

IUBMB Life

Volumn 59, Issue 8-9, 2007, Pages 586-599

  Eaton, William A ^a   Henry, Eric R ^a   Hofrichter, James ^a   Bettati, Stefano ^b   Viappiani, Cristiano ^b   Mozzarelli, Andrea ^b  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^b UNIVERSITY OF PARMA   (Italy)

Author keywords

Hemeproteins; Hemoglobin; Protein function; Protein structure; Structural biology

Indexed keywords

CARBON MONOXIDE; HEMOGLOBIN; HEMOPROTEIN;

ALLOSTERISM; CHEMICAL STRUCTURE; OXYGEN AFFINITY; OXYGENATION; PH MEASUREMENT; PROTEIN CONFORMATION; REVIEW; THERMODYNAMICS;

ALLOSTERIC REGULATION; EVOLUTION, MOLECULAR; HEMOGLOBINS; MODELS, MOLECULAR;

EID: 34547963038     PISSN: 15216543     EISSN: 15216551     Source Type: Journal    
DOI: 10.1080/15216540701272380     Document Type: Review

References (75)

1. Brunori, M. (1991) The fascination of hemoglobin - a roman perspective - a citation-classic commentary on hemoglobin and myoglobin in their reactions with ligands. Frontiers of Biology, Volume 21. Edited by Antonini, E., and Brunori, M. Current Contents/Life Sciences, 8-8.
2. Antonini, E., Rossi Fanelli, A., Wyman, J., Brunori, M., Bucci, E., and Fronticelli, C. (1963) Studies on relations between molecular and functional properties of hemoglobin .4. Bohr effect in human hemoglobin measured by proton binding. J. Biol. Chem. 238, 2950-2957.
3. Edsall, J. T., and Wyman, J. (1958) Biophysical Chemistry, Academic Press Inc., New York.
4. Monod, J., Wyman, J., and Changeux, J.-P. (1965) On the nature of allosteric transitions: a plausible model. J. Mol. Biol. 12, 88-118.
5. Brunori, M. (1999) Hemoglobin is an honorary enzyme. Trends Biochem. Sci. 24, 158-161.
6. Antonini, E., and Brunori, M. (1971) Hemoglobin and Myoglobin in their Reaction with Ligands, North Holland, Amsterdam.
7. Edelstein, S. J. (1975) Cooperative interactions of hemoglobin. Ann. Rev. Biochem. 44, 209-232.
8. Shulman, R. G., Hopfield, J. J., and Ogawa, S. (1975) Allosteric interpretation of haemoglobin properties. Quart. Rev. Biophys. 8, 325-420.
9. Imai, K. (1982) Allosteric Effects in Haemoglobin, Cambridge University Press, Cambridge.
10. Bunn, H. F., and Forget, B. G. (1986) Hemoglobin: Molecular, Genetic and Clinical Aspects, W. B. Saunders, Co., Philadelphia.
11. Eaton, W. A., and Hofrichter, J. (1987) Hemoglobin-S gelation and sickle-cell disease. Blood 70, 1245-1266.
12. Perutz, M. F. (1989) Mechanisms of cooperativity and allosteric regulation in proteins. Quart. Rev. Biophys. 22, 138-236.
13. Eaton, W. A., and Hofrichter, J. (1990) Sickle cell hemoglobin polymerization. Adv. Prot. Chem. 40, 263-279.
14. Ackers, G. K. (1998) Deciphering the molecular code of hemoglobin allostery. Adv. Prot. Chem. 51, 185-253.
15. Perutz, M. F., Wilkinson, A. J., Paoli, M., and Dodson, G. G. (1998) The stereochemistry of the cooperative effects in hemoglobin revisited. Annu. Rev. Biophys. Biomol. Struct. 27, 1-34.
16. Shulman, R. G. (2001) Spectroscopic contributions to the understanding of hemoglobin function: implications for structural biology. IUBMB Life 51, 351-357.
17. Lukin, J. A., and Ho, C. (2004) The structure-function relationship of hemoglobin in solution at atomic resolution. Chem. Rev. 104, 1219-1230.
18. Bellelli, A., Brunori, M., Miele, A. E., Panetta, G., and Vallone, B. (2006) The allosteric properties of hemoglobin: insights from natural and site directed mutants. Curr. Prot. Peptide Sci. 7, 17-45.
19. Szabo, A., and Karplus, M. (1972) A mathematical model for structure-function relations in hemoglobin. J. Mol. Biol. 72, 163-197.
20. Perutz, M. F. (1970) Stereochemistry of cooperative effects in haemoglobin. Nature 228, 726-733.
21. Lee, A. W-M., and Karplus, M. (1983) Structure-specific model of hemoglobin cooperativity. Proc. Natl. Acad. Sci. USA 80, 7055-7059.
22. Lee, A. W.-M., Karplus, M., Poyart, C., and Bursaux, E. (1988) Analysis of proton release in oxygen binding by hemoglobin - implications for the cooperative mechanism. Biochemistry 27, 1285-1301.
23. Henry, E. R., Bettati, S., Hofrichter, J., and Eaton, W. A. (2002) A tertiary two-state allosteric model for hemoglobin. Biophys. Chem. 98, 149-164.
24. Herzfeld, J., and Stanley, H. E. (1974) A general approach to cooperativity and its application to the oxygen equilibrium of hemoglobin and its effectors. J. Mol. Biol. 82, 231-265.
25. Changeux, J. P., and Edelstein, S. J. (2005) Allosteric mechanisms of signal transduction. Science 308, 1424-1428.
26. Buc, H. (2006) In Allosteric Proteins. 40 Years with Monod-Wyman-Changeux (Brunori, M., Careri, G., Changeux, J.-P., and Schachman, H. K., eds.), Vol. 17, pp. 31-49, Accadaemia Nazionale dei Lincei, Rome.
27. Muirhead, H., and Perutz, M. F. (1963) Structure of haemoglobin - a 3-Dimensional Fourier synthesis of reduced human haemoglobin at 5.5 angstrom resolution. Nature 199, 633-638.
28. Perutz, M. F., Watson, H. C., Muirhead, H., Diamond, R., and Bolton, W. (1964) Structure of haemoglobin - X-Ray examination of reduced horse haemoglobin. Nature 203, 687-690.
29. Wyman, J. (1964) Linked functions and reciprocal effects in hemoglobin - a second look. Adv. Prot. Chem. 19, 223-286.
30. Perutz, M. F., Rossmann, M. G., Cullis, A. F., Muirhead, H., Will, G., and North, A. C. T. (1960) Structure of haemoglobin - 3-dimensional fourier synthesis at 5.5-angstrom resolution, obtained by X-ray analysis. Nature 185, 416-422.
31. Pauling, L. (1935) The oxygen equilibrium of hemoglobin and its structural interpretation. Proc. Natl. Acad. Sci. USA 21, 186-191.
32. Koshland, D. E., Nemethy, G., and Filmer, D. (1966) Comparison of experimental binding data and theoretical models in proteins containing subunits. Biochemistry 5, 365-385.
33. Eaton, W. A., Henry, E. R., Hofrichter, J., and Mozzarelli, A. (1999) Is cooperative oxygen binding by hemoglobin really understood? Nat. Struct. Biol. 6, 351-358.
34. Hopfield, J. J., Shulman, R. G., and Ogawa, S. (1971) Allosteric model of hemoglobin.1. Kinetics. J. Mol. Biol. 61, 425-443.
35. Gibson, Q. H. (1959) Photochemical formation of a quickly reacting form of haemoglobin. Biochem. J. 71, 293-303.
36. Antonini, E., and Brunori, M. (1970) Hemoglobin. Ann. Rev. Biochem. 39, 977-1042.
37. Sawicki, C. A., and Gibson, Q. H. (1976) Quaternary conformational- changes in human hemoglobin studied by laser photolysis of carboxyhemoglobin. J. Biol. Chem. 251, 1533-1542.
38. Mozzarelli, A., Rivetti, C., Rossi, G. L., Henry, E. R., and Eaton, W. A. (1991) Crystals of haemoglobin with the T quaternary structure bind oxygen non-cooperatively with no Bohr effect. Nature 351, 416-418.
39. Rivetti, C., Mozzarelli, A., Rossi, G. L., Henry, E. R., and Eaton, W. A. (1993) Oxygen binding by single crystals of hemoglobin. Biochemistry 32, 2888-2906.
40. Liddington, R., Derewenda, Z., Dodson, G., and Harris, D. (1988) Structure of the liganded T-state of hemoglobin identifies the origin of cooperative oxygen binding. Nature 331, 725-728.
41. Shibayama, N., and Saigo, S. (1995) Fixation of the quaternary structures of human adult haemoglobin by encapsulation in transparent porous silica gels. J. Mol. Biol. 251, 203-209.
42. Brunori, M., Coletta, M., and Di Cera, E. (1986) A cooperative model for ligand-binding to biological macromolecules as applied to O2 carriers. Biophys. Chem. 23, 215-222.
43. Gill, S. J., Robert, C. H., Coletta, M., DiCera, E., and Brunori, M. (1986) Cooperative free energies for nested allosteric models as applied to human hemoglobin. Biophys. J. 50, 747-752.
44. Smith, F. R., and Ackers, G. K. (1985) Experimental resolution of cooperative free-energies for the 10 ligation states of human-hemoglobin. Proc. Natl. Acad. Sci. USA 82, 5347-5351.
45. Speros, P. C., Licata, V. J., Yonetani, T., and Ackers, G. K. (1991) Experimental resolution of cooperative free-energies for the 10 ligation species of cobalt(II) iron(II)-CO hemoglobin. Biochemistry 30, 7254-7262.
46. Gelin, B. R., Lee, A. W. M., and Karplus, M. (1983) Hemoglobin tertiary structural-change on ligand-binding-it's role in the cooperative mechanism. J. Mol. Biol. 171, 489-559.
47. Yun, K. M., Morimoto, H., and Shibayama, N. (2002) The contribution of the asymmetric alpha 1 beta 1 half-oxygenated intermediate to human hemoglobin cooperativity. J. Biol. Chem. 277, 1878-1883.
48. Bettati, S., Mozzarelli, A., Rossi, G. L., Tsuneshige, A., Yonetani, T., Eaton, W. A., and Henry, E. R. (1996) Oxygen binding by single crystals of hemoglobin: the problem of cooperativity and inequivalence of alpha and beta subunits. Proteins-Struct. Funct.Gen. 25, 425-437.
49. Mozzarelli, A., Rivetti, C., Rossi, G. L., Eaton, W. A., and Henry, E. R. (1997) Allosteric effectors do not alter the oxygen affinity of hemoglobin crystals. Prot. Sci. 6, 484-489.
50. Perutz, M. F. (1970) The Bohr effect and combination with organic phosphates. Nature 228, 734-739.
51. Shulman, R. G., Ogawa, S., Wuthrich, K., Yamane, T., Peisach, J., and Blumberg, W. E. (1969) Absence of heme-heme interactions in hemoblobin. Science 165, 251-257.
52. Szabo, A., and Karplus, M. (1976) Analysis of interaction of organic phosphates with hemoglobin. Biochemistry 15, 2869-2877.
53. Gelin, B. R., and Karplus, M. (1977) Mechanism of tertiary structural-change in hemoglobin. Proc. Natl. Acad. Sci. USA 74, 801-805.
54. Gelin, B. R., Lee, A. W. M., and Karplus, M. (1983) Hemoglobin tertiary structural-change on ligand-binding - its role in the cooperative mechanism. J. Mol. Biol. 171, 489-559.
55. Bettati, S., and Mozzarelli, A. (1997) T state hemoglobin binds oxygen noncooperatively with allosteric effects of protons, inositol hexaphosphate, and chloride. J. Biol. Chem. 272, 32050-32055.
56. Bruno, S., Bonaccio, M., Bettati, S., Rivetti, C., Viappiani, C., Abbruzzetti, S., and Mozzarelli, A. (2001) High and low oxygen affinity conformations of T state hemoglobin. Prot. Sci. 10, 2401-2407.
57. Lyons, K. B., Friedman, J. M., and Fleury, P. A. (1978) Nanosecond transient Raman-spectra of photolysed carboxyhemoglobin. Nature 275, 565-566.
58. Hofrichter, J., Sommer, J. H., Henry, E. R., and Eaton, W. A. (1983) Nanosecond absorption spectroscopy of hemoglobin, elementary processes in kinetic cooperativity. Proc. Natl. Acad. Sci. USA 80, 2235-2239.
59. Jones, C. M., Ansari, A., Henry, E. R., Christoph, G. W., Hofrichter, J., and Eaton, W. A. (1992) Speed of intersubunit communication in proteins. Biochemistry 31, 6692-6702.
60. Henry, E. R., Jones, C. M., Hofrichter, J., and Eaton, W. A. (1997) Can a two-state MWC allosteric model explain hemoglobin kinetics? Biochemistry 36, 6511-6528.
61. Jackson, T. A., Lim, M., and Anfinrud, P. A. (1994) Complex nonexponential relaxation in myoglobin after photodissociation of MbCO - Measurement and analysis from 2-ps to 56-mu-s. Chem. Phys. 180, 131-140.
62. Hagen, S. J., and Eaton, W. A. (1996) Nonexponential structural relaxations in proteins. J. Chem. Phys. 104, 3395-3398.
63. Hagen, S. J., Hofrichter, J., and Eaton, W. A. (1996) Geminate rebinding and conformational dynamics of myoglobin embedded in a glass at room temperature. J. Phys. Chem. 100, 12008-12021.
64. Perrella, M., Colosimo, A., Benazzi, L., Ripamonti, M., and Rossi Bernardi, L. (1990) What the intermediate compounds in ligand-binding to hemoglobin tell about the mechanism of cooperativity. Biophys. Chem. 37, 211-223.
65. Perrella, M., and Di Cera, E. (1999) CO ligation intermediates and the mechanism of hemoglobin cooperativity. J. Biol. Chem. 274, 2605-2608.
66. Yonetani, T., Park, S., Tsuneshige, A., Imai, K., and Kanaori, K. (2002) Global allostery model of hemoglobin - modulation of O-2 affinity, cooperativity, and Bohr effect by heterotropic allosteric effectors. J. Biol. Chem. 277, 34508-34520.
67. Viappiani, C., Bettati, S., Bruno, S., Ronda, L., Abbruzzetti, S., Mozzarelli, A., and Eaton, W. A. (2004) New insights into allosteric mechanisms from trapping unstable protein conformations in silica gels. Proc. Natl. Acad. Sci. USA 101, 14414-14419.
68. Szabo, A. (1978) Kinetics of hemoglobin and transition-state theory. Proc. Natl. Acad. Sci. USA 75, 2108-2111.
69. Lukin, J. A., Kontaxis, G., Simplaceanu, V., Yuan, Y., Bax, A., and Ho, C. (2003) Quaternary structure of hemoglobin in solution. Proc. Natl. Acad. Sci. USA 100, 517-520.
70. Hopfield, J. J. (1973) Relation between structure, cooperativity and spectra in a model of hemoglobin action. J. Mol. Biol. 77, 207-222.
71. Jayaraman, V., Rodgers, K. R., Mukerji, I., and Spiro, T. G. (1995) Hemoglobin allostery - resonance Raman-spectroscopy of kinetic intermediates. Science 269, 1843-1848.
72. Balakrishnan, G., Case, M. A., Pevsner, A., Zhao, X. J., Tengroth, C., McLendon, G. L., and Spiro, T. G. (2004) Time-resolved absorption and UV resonance Raman spectra reveal stepwise formation of T quaternary contacts in the allosteric pathway of hemoglobin. J. Mol. Biol. 340, 843-856.
73. Sahu, S. C., Simplaceanu, V., Gong, Q. G., Ho, N. T., Glushka, J. G., Prestegard, J. H., and Ho, C. (2006) Orientation of deoxyhemoglobin at high magnetic fields: structural insights from RDCs in solution. J. Am. Chem. Soc. 128, 6290-6291.
74. Gong, Q. G., Simplaceanu, V., Lukin, J. A., Giovannelli, J. L., Ho, N. T., and Ho, C. (2006) Quaternary structure of carbonmonoxyhemoglobins in solution: structural changes induced by the allosteric effector inositol hexaphosphate. Biochemistry 45, 5140-5148.
75. Dickerson, R. E., and Geis, I. (1983) Hemoglobins: Structure, Function, Evolution, and Pathology, Benjamin/Cummings, Menlo Park, CA.