Spectroscopic and functional characterization of T state hemoglobin conformations encapsulated in silica gels

Biochemistry

Volumn 43, Issue 43, 2004, Pages 13674-13682

  Samuni, Uri ^a   Dantsker, David ^a   Juszczak, Laura J ^a   Bettati, Stefano ^b   Ronda, Luca ^b   Mozzarelli, Andrea ^b   Friedman, Joel M ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF PARMA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

APPROXIMATION THEORY; BINDING ENERGY; BIOCHEMISTRY; OXYGEN;

BINDING AFFINITY; BINDING CURVES; ENCAPSULATION PROTOCOLS; FUNCTIONAL CHARACTERIZATION;

SILICA GEL;

CARBON; OXYGEN DERIVATIVE; SILICA GEL;

ADDITION REACTION; ARTICLE; BINDING AFFINITY; CONFORMATIONAL TRANSITION; DERIVATIZATION; DISSOCIATION CONSTANT; ENCAPSULATION; HEMOGLOBIN DETERMINATION; LIGAND BINDING; MOLECULAR DYNAMICS; MOLECULAR EVOLUTION; MOLECULAR INTERACTION; MOLECULAR MECHANICS; PHASE TRANSITION; PHOTODEGRADATION; PRIORITY JOURNAL; RAMAN SPECTROMETRY; RATING SCALE; REACTION ANALYSIS; STRUCTURE ANALYSIS; ULTRAVIOLET SPECTROSCOPY;

ADULT; CARBON MONOXIDE; CARBOXYHEMOGLOBIN; GELS; HEMOGLOBIN A; HEMOGLOBINS; HUMANS; KINETICS; LIGANDS; OXYGEN; PHASE TRANSITION; PROTEIN BINDING; PROTEIN CONFORMATION; SILICON DIOXIDE; SOLUTIONS; SPECTRUM ANALYSIS, RAMAN; TIME FACTORS;

EID: 7244239027     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi048531d     Document Type: Article

References (63)

1. 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.
2. 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.
3. Monod, J., Wyman, J., and Changeux, J. P. (1965) On the nature of allosteric transitions', a plausible model, J. Mol. Biol. 12, 88-118.
4. Mueser, T. C., Rogers, P. H., and Arnone, A. (2000) Interface sliding as illustrated by the multiple quaternary structures of liganded hemoglobin, Biochemistry 39, 15353-15364.
5. 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. U.S.A. 100, 517-520.
6. Ackers, G. K., Dalessio, P. M., Lew, G. H., Daugherty, M. A., and Holt, J. M. (2002) Single residue modification of only one dimer within the hemoglobin tetramer reveals autonomous dimer function, Proc. Natl. Acad. Sci. U.S.A. 99, 9777-9782.
7. Ackers, G. K., Holt, J. M., Burgie, E. S., and Yarian, C. S. (2004) Analyzing intermediate state cooperativity in hemoglobin, Methods Enzymol. 379, 3-28.
8. 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, Protein Sci. 10, 2401-2407.
9. Shibayama, N., and Saigo, S. (2001) Direct observation of two distinct affinity conformations in the T state human deoxyhemoglobin, FEBS Lett. 492, 50-53.
10. Samuni, U., Juszczak, L., Dantsker, D., Khan, I., Friedman, A. J., Perez-Gonzalez-de-Apodaca, J., Bruno, S., Hui, H. L., Colby, J. E., Karasik, E., Kwiatkowski, L. D., Mozzarelli, A., Noble, R. W., and Friedman, J. M. (2003) Functional and spectroscopic characterization of half-liganded iron-zinc hybrid hemoglobin: evidence for conformational plasticity within the T state, Biochemistry 42, 8272-8288.
11. Tsuneshige, A., Park, S., and Yonetani, T. (2002) Heterotropic effectors control the hemoglobin function by interacting with its T and R states - a new view on the principle of allostery, Biophys. Chem. 98, 49-63.
12. Yonetani, T., Park, S., Tsuneshige, A., Imai, K., and Kanaori, K. (2002) Global allostery model of hemoglobin: Modulation of O2-affinity, cooperativity, and Bohr effect by heterotropic allosteric effectors, J. Biol. Chem. 277, 34508-34520.
13. 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.
14. Hofrichter, J., Henry, E. R., Sommer, J. H., Deutsch, R., Ikeda-Saito, M., Yonetani, T., and Eaton, W. A. (1985) Nanosecond optical spectra of iron-cobalt hybrid hemoglobins: geminate recombination, conformational changes, and intersubunit communication, Biochemistry 24, 2667-2679.
15. Ghelichkhani, E., Goldbeck, R. A., Lewis, J. W., and Kliger, D. S. (1996) Nanosecond time-resolved absorption studies of human oxyhemoglobin photolysis intermediates, Biophys. J. 71, 1596-1604.
16. Goldbeck, R. A., Paquette, S. J., Bjorling, S. C., and Kliger, D. S. (1996) Allosteric intermediates in hemoglobin. 2. Kinetic modeling of HbCO photolysis, Biochemistry 35, 8628-8639.
17. Esquerra, R. M., Goldbeck, R. A., Reaney, S. H., Batchelder, A. M., Wen, Y., Lewis, J. W., and Kliger, D. S. (2000) Multiple geminate ligand recombinations in human hemoglobin, Biophys. J. 78, 3227-3239.
18. Sassaroli, M., and Rousseau, D. L. (1987) Time dependence of near-infrared spectra of photodissociated hemoglobin and myoglobin, Biochemistry 26, 3092-3098.
19. Bjorling, S. C., Goldbeck, R. A., Paquette, S. J., Milder, S. J., and Kliger, D. S. (1996) Allosteric intermediates in hemoglobin. 1. Nanosecond time-resolved circular dichroism spectroscopy, Biochemistry 35, 8619-8627.
20. Scott, T. W., and Friedman, J. M. (1984) Tertiary-structure relaxation in hemoglobin: a transient raman study, J. Am. Chem. Soc. 106, 5677-5687.
21. Hu, X., Rodgers, K. R., Mukerji, I., and Spiro, T. G. (1999) New light on allostery: dynamic resonance Raman spectroscopy of hemoglobin kempsey, Biochemistry 38, 3462-3467.
22. Friedman, J. M. (1994) Time-resolved resonance Raman spectroscopy as probe of structure, dynamics, and reactivity in hemoglobin, Methods Enzymol. 232, 205-231.
23. Su, C., Park, Y. D., Liu, G., and Spiro, T. G. (1989) Hemoglobin T-R structure dynamics from simltaneous monitoring of tyrosine and tryptophan time resolved UV resonance Raman signals, J. Am. Chem. Soc. 111, 3457-3459.
24. Rodgers, K. R., and Spiro, T. G. (1994) Nanosecond dynamics of the R→T transition in hemoglobin: ultraviolet Raman studies, Science 265, 1697-1699.
25. Jayaraman, V., Rodgers, K. R., Mukerji, I., and Spiro, T. G. (1995) Hemoglobin allostery: resonance Raman spectroscopy of kinetic intermediates, Science 269, 1843-1848.
26. Avnir, D., Braun, S., Lev, O., and Ottolenghi, M. (1994) Enzymes and other proteins entrapped in sol-gel materials, Chem. Mater. 6, 1605-1614.
27. Ellerby, L. M., Nishida, C. R., Nishida, F., Yamanaka, S. A., Dunn, B., Valentine, J. S., and Zink, J. I. (1992) Encapsulation of proteins in transparent porous silicate glasses prepared by the sol-gel method, Science 255, 1113-1115.
28. Abbruzzetti, S., Viappiani, C., Bruno, S., Mozzarelli, A. (2001) Enhanced geminate ligand rebinding upon photo-dissociation of silica gel-embedded myoglobin-CO, Chem. Phys. Lett. 346, 430-436.
29. Samuni, U., Navati, M. S., Juszczak, L. J., Dantsker, D., Yang, M., and Friedman, J. M. (2000) Unfolding and refolding of sol-gel encapsulated carbonmonoxymyoglobin: An orchestrated spectroscopic study of intermediates and kinetics? J. Phys. Chem. B 104, 10802-10813.
30. Samuni, U., Dantsker, D., Khan, I., Friedman, A. J., Peterson, E., and Friedman, J. M. (2002) Spectroscopically and kinetically distinct conformational populations of sol-gel-encapsulated carbonmonoxy myoglobin. A comparison with hemoglobin, J. Biol. Chem. 277, 25783-25790.
31. Shibayama, N., and Saigo, S. (2003) Oxygen equilibrium properties of myoglobin locked in the liganded and unliganded conformations, J. Am. Chem. Soc. 125, 3780-3783.
32. Sottini, S., Viappiani, C., Ronda, L., Bettati, S., and Mozzarelli, A. (2004) CO rebinding kinetics to myoglobin- and R state hemoglobin- doped silica gels in the presence of glycerol, J. Phys. Chem. B 108, 8478-8484.
33. 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.
34. Das, T. K., Khan, I., Rousseau, D. L., and Friedman, J. M. (1999) Temperature-dependent quaternary state relaxation in sol-gel encapsulated hemoglobin, Biospectroscopy 5 (Suppl.), 64-70.
35. Juszczak, L. J., and Friedman, J. M. (1999) UV resonance raman spectra of ligand binding intermediates of sol-gel encapsulated hemoglobin, J. Biol. Chem. 274, 30357-30360.
36. Khan, I., Shannon, C. F., Dantsker, D., Friedman, A. J., Perez-Gonzalez-de-Apodaca, J., and Friedman, J. M. (2000) Sol-gel trapping of functional intermediates of hemoglobin: geminate and bimolecular recombination studies, Biochemistry 39, 16099-16109.
37. 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.
38. Shibayama, N. (1999) Functional analysis of hemoglobin molecules locked in doubly liganded conformations, J. Mol. Biol. 285, 1383-1388.
39. Shibayama, N., and Saigo, S. (1999) Kinetics of the allosteric transition in hemoglobin within silicate sol-gels, J. Am. Chem. Soc. 121, 444-445.
40. Pioselli, B., Bettati, S., Demidkina, T. V., Zakomirdina, L. N., Phillips, R. S., and Mozzarelli, A. (2004) Tyrosine phenol lyase and tryptophan indole-lyase encapsulated in wet nanoporous silica gels: selective stabilization of tertiary conformations, Protein Sci. 13, 913-924.
41. Khan, I., Dantsker, D., Samuni, U., Friedman, A. J., Bonaventura, C., Manjula, B., Acharya, S. A., and Friedman, J. M. (2001) Beta 93 modified hemoglobin: kinetic and conformational consequences, Biochemistry 40, 7581-7592.
42. Abbruzzetti, S., Viappiani, C., Bruno, S., Bettati, S., Bonaccio., M., Mozzarelli, A. (2001) Functional characterization of heme proteins encapsulted in wet nanoporous silica gels, J. Nanosci. Nanotechnol. 1, 407-413.
43. 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.
44. 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, Protein Sci. 6, 484-489.
45. Rousseau, D. L., and Friedman, J. M. (1988) in Biological Applications of Raman Spectroscopy (Spiro, T. G., Ed.) pp 133-215, John Wiley & Sons, New York.
46. Zhao, X., Chen, R., Raj, V., and Spiro, T. G. (2001) Assignment of the 1511 cm(-1) UV resonance Raman marker band of hemoglobin to tryptophan, Biopolymers 62, 158-162.
47. Nagai, M., Wajcman, H., Lahary, A., Nakatsukasa, T., Nagatomo, S., and Kitagawa, T. (1999) Quaternary structure sensitive tyrosine residues in human hemoglobin: UV resonance raman studies of mutants at alpha140, beta35, and beta145 tyrosine, Biochemistry 38, 1243-1251.
48. Nagai, M., Kaminaka, S., Ohba, Y., Nagai, Y., Mizutani, Y., and Kitagawa, T. (1995) Ultraviolet resonance Raman studies of quaternary structure of hemoglobin using a tryptophan beta 37 mutant, J. Biol. Chem. 270, 1636-1642.
49. Huang, S., Peterson, E. S., Ho, C., and Friedman, J. M. (1997) Quaternary structure sensitive tyrosine interactions in hemoglobin: a UV resonance Raman study of the double mutant rHb (beta99Asp→Asn, alpha42Tyr→Asp), Biochemistry 36, 6197-6206.
50. Lalezari, I., Lalezari, P., Poyart, C., Marden, M., Kister, J., Bohn, B., Fermi, G., and Perutz, M. F. (1990) New effectors of human hemoglobin: structure and function, Biochemistry 29, 1515-1523.
51. Samuni, U., Dantsker, D., Ray, A., Wittenberg, J. B., Wittenberg, B. A., Dewilde, S., Moens, L., Quellet, Y., Guertin, M., and Friedman, J. M. (2003) Kinetic modulation in carbonmonoxy derivatives of truncated hemoglobins: The role of distal heme pocket residues and extended apolar tunnel, J. Biol. Chem. 278, 27241-27250.
52. Dantsker, D., Samuni, U., Friedman, A. J., Yang, M., Ray, A., and Friedman, J. M. (2002) Geminate rebinding in trehalose-glass embedded myoglobins reveals residue specific control of intramolecular trajectories, J. Mol. Biol. 13, 239-251.
53. Hu, X., and Spiro, T. G. (1997) Tyrosine and tryptophan structure markers in hemoglobin ultraviolet resonance Raman spectra: mode assignments via subunit-specific isotope labeling of recombinant protein, Biochemistry 36, 15701-15712.
54. Juszczak, L. J., Fablet, C., Baudin-Creuza, V., Lesecq-Le Gall, S., Hirsch, R. E., Nagel, R. L., Friedman, J. M., and Pagnier, J. (2003) Conformational changes in hemoglobin S (betaE6V) imposed by mutation of the beta Glu7-beta Lys132 salt bridge and detected by UV resonance Raman spectroscopy, J. Biol. Chem. 278, 7257-7263.
55. Dave, B. C., Miller, J. M., Dunn, B., Valentine, J. S., and Zink, J. I. (1997) Encapsulation of proteins in bulk and thin film sol-gel matrices, J. Sol-Gel Sci. Technol. 8, 629-634.
56. Peterson, E. S., Shinder, R., Khan, I., Juczszak, L., Wang, J., Manjula, B., Acharya, S. A., Bonaventura, C., and Friedman, J. M. (2004) Domain-specific effector interactions within the central cavity of human adult hemoglobin in solution and in porous sol-gel matrices: evidence for long-range communication pathways, Biochemistry 43, 4832-4843.
57. Friedman, J. M., Scott, T. W., Stepnoski, R. A., Ikeda-Saito, M., and Yonetani, T. (1983) The iron-proximal histidine linkage and protein control of oxygen binding in hemoglobin. A transient Roman study, J. Biol. Chem. 258, 10564-10572.
58. Friedman, J. M. (1985) Structure, dynamics, and reactivity in hemoglobin, Science 228, 1273-1280.
59. Peterson, E. S., and Friedman, J. M. (1998) A possible allosteric communication pathway identified through a resonance Raman study of four β37 mutants of human hemoglobin A, Biochemistry 37, 4346-4357.
60. Huang, J., Juszczak, L. J., Peterson, E. S., Shannon, C. F., Yang, M., Huang, S., Vidugiris, G. V., and Friedman, J. M. (1999) The conformational and dynamic basis for ligand binding reactivity in hemoglobin Ypsilanti (beta 99 asp→Tyr): origin of the quaternary enhancement effect, Biochemistry 38, 4514-4525.
61. Kwiatkowski, L. D., Hui, H. L., Wierzba, A., Noble, R. W., Walder, R. Y., Peterson, E. S., Sligar, S. G., and Sanders, K. E. (1998) Preparation and kinetic characterization of a series of betaW37 variants of human hemoglobin A: evidence for high-affinity T quaternary structures, Biochemistry 37, 4325-4335.
62. Noble, R. W., Hui, H. L., Kwiatkowski, L. D., Paily, P., DeYoung, A., Wierzba, A., Colby, J. E., Bruno, S., and Mozzarelli, A. (2001) Mutational effects at the subunit interfaces of human hemoglobin: evidence for a unique sensitivity of the T quaternary state to changes in the hinge region of the alpha 1 beta 2 interface, Biochemistry 40, 12357-12368.
63. 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 conformation in silica gels, Proc. Natl. Acad. Sci. U.S.A. (in press).