Insulin allosteric behavior: Detection, identification, and quantification of allosteric states via 19F NMR

Biochemistry

Volumn 44, Issue 21, 2005, Pages 7656-7668

  Bonaccio, Maria ^a   Ghaderi, Nima ^b   Borchardt, Dan ^b   Dunn, Michael F ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOSTERIC PROTEINS; DIABETES; INSULIN HEXAMER; LIGANDS;

CONFORMATIONS; DISEASES; FLUORINE; NEGATIVE IONS; NUCLEAR MAGNETIC RESONANCE; POSITIVE IONS; PROTEINS; ZINC;

INSULIN;

2 TRIFLUOROMETHYLCINNAMATE; 3 TRIFLUOROMETHYLBENZOATE; 4 TRIFLUOROMETHYLBENZOIC ACID; 4 TRIFLUOROMETHYLCINNAMATE; BENZOIC ACID DERIVATIVE; CARBOXYLIC ACID; CINNAMIC ACID DERIVATIVE; INSULIN; NITRIC OXIDE; PHENOL; UNCLASSIFIED DRUG; ZINC;

ALLOSTERISM; ANION TRANSPORT; ARTICLE; BINDING AFFINITY; BINDING SITE; CHEMICAL STRUCTURE; CONFORMATIONAL TRANSITION; DENATURATION; DIFFUSION; FLUORINATION; LIGAND BINDING; MATHEMATICAL ANALYSIS; MATHEMATICAL COMPUTING; MICROENVIRONMENT; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTON NUCLEAR MAGNETIC RESONANCE;

ALLOSTERIC REGULATION; ALLOSTERIC SITE; ANILIDES; BENZOATES; BINDING, COMPETITIVE; CARBOXYLIC ACIDS; CINNAMATES; COBALT; FLUORINE; HISTIDINE; HUMANS; HYDROXYBENZOIC ACIDS; INSULIN; LIGANDS; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, CHEMICAL; NAPHTHOLS; PHENOL; PROTEIN SUBUNITS; THERMODYNAMICS; ZINC;

EID: 19644362270     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi050392s     Document Type: Article

References (39)

1. Roy, M., Brader, M. L., Lee, R. W.-K., Kaarsholm, N. C., Hansen, J., and Dunn, M. F. (1989) Spectroscopic signatures of the T to R conformational transition in the insulin hexamer, J. Biol. Chem. 264, 19081-19085.
2. Rahuel-Clermont, S., French, C. A., Chou, C. I., Kaarsholm, N. C., and Dunn, M. F. (1997) Mechanisms of stabilization of the insulin hexamer through allosteric ligand interactions, Biochemistry 36, 5837-5845.
3. Steiner, D. F., Peterson, J. D., Tager, H. S., Emdin, S., Ostberg, Y., and Falkmer, S. (1973) Comparative aspects of proinsulin and insulin structure and biosynthesis, Am. Zool. 13, 591-604.
4. Blundell, T., Dodson, G., Hodgkin, D., and Mercola, D. (1972) Insulin: the structure in the crystal and its reflection in chemistry and biology, Adv. Protein Chem. 26, 279-402.
5. Bailyes, E. M., Guest, P. C., and Hutton, J. C. (1992) Insulin Synthesis, in Insulin: Molecular Biology to Pathology (Ashcroft, F. M., and Ashcroft, S. J. H., Eds) pp 64-92, Oxford University Press, New York.
6. Kaarsholm, N. C., Ko, H. C., and Dunn, M. F. (1989) Comparison of solution structural flexibility and zinc binding domains for insulin, proinsulin, and mini-proinsulin, Biochemistry 28, 4427-4435.
7. Brader, M. L., and Dunn, M. F. (1991) Insulin hexamers: new conformations and applications, Trends Biochem. Sci., 16, 341-345,
8. Choi, W. E., Brader, M. L., Aguilar, V., Kaarsholm, N. C., and Dunn, M. F. (1993) The allosteric transition of the insulin hexamer is modulated by homotropic and heterotropic interactions, Biochemistry 32, 11638-11645,
9. Brzovic, P. S., Choi, W. E., Borchardt, D, Kaarsholm, N. C., and Dunn, M. F. (1994) Structural asymmetry and half-site reactivity in the T to R allosteric transition of the insulin hexamer, Biochemistry 33, 13057-13069.
10. Bloom, C. R., Choi, W. E., Brzovic, P. S., Ha, J. J., Huang, S. T., Kaarsholm, N. C., and Dunn, M. F. (1995) Ligand binding to wild-type and E-B13Q mutant insulins; a three-state allosteric model system showing half-site reactivity, J. Mol. Biol. 245, 324-330.
11. Bloom, C. R., Heymann, R., Kaarsholm, N. C., and Dunn, M. F. (1997) Binding of 2,6- and 2,7-dihydroxynaphthalene to wild-type and E-B13Q insulins: dynamic, equilibrium, and molecular modeling investigations, Biochemistry 36, 12746-12758.
12. Bloom, C. R., Kaarsholm, N. C., Ha, J. J., and Dunn, M. F. (1997) Half-site reactivity, negative cooperativity, and positive cooperativity: quantitative considerations of a plausible model, Biochemistry 36, 12759-12765.
13. Bloom, C. R., Wu, N., Dunn, A., Kaarsholm, N. C., and Dunn, M. F. (1998) Comparison of the allosteric properties of the Co(II)- and Zn(II)-substituted insulin hexamers, Biochemistry 37, 10937-10944.
14. Derewenda, U., Derewenda, Z., Dodson, E. J., Dodson, G. G., Reynolds, C., D., Smith, G., D., Sparks, C., and Swensen, D. (1989) Phenol stabilizes more helix in a new symmetrical zinc insulin hexamer, Nature 338, 594-596.
15. Smith, G. D., Swenson, D. C., Dodson, E. J., Dodson, G. G., and Reynolds, C. D. (1984) Structural stability in the 4-zinc human insulin hexamer, Proc. Natl. Acad. Sci. U.S.A. 81, 7093-7097.
16. 3 human insulin hexamer, Biochemistry 33, 1512-1517.
17. Brader, M. L., Kaarsholm, N. C., Lee, R. W.-K., and Dunn, M. F. (1991) Characterization of the R-state insulin hexamer and its derivatives. The hexamer is stabilized by heterotropic ligand binding interactions, Biochemistry 30, 6636-6645.
18. Whittingham, J. L., Chaudhuri, S., Dodson, E. J., Moody, P. C. E., and Dodson, G. G. (1995) X-ray crystallographic studies on hexameric insulins in the presence of helix-stabilizing agents, thiocyanate, methylparaben, and phenol, Biochemistry 34, 15553-15563.
19. Bentley, G. A., Brange, J., Derewenda, Z., Dodson, E. J., Dodson, G. G., Markussen, J., Wilkinson, A. J., Wollmer, A., and Xiao, B. (1992) Role of B13 Glu in insulin assembly. The hexamer structure of recombinant mutant (B13 Glu → Gin) insulin, J. Mol. Biol. 228, 1163-1176.
20. Baker, E. N., Blundell, T. L., Cutfield, J. F., Cutfield, S. M., Dodson, E. J., Dodson, G. G., Hodgkin, D. C., Hubbard, R. E., Isaacs, N. W., Reynolds, C. D., Sakabe, K., Sakabe, N., and Vijayan, N. M. (1988) The structure of 2Zn pig insulin crystals at 1,5 Å resolution, Philos. Trans. R. Soc. London, Ser. B 319, 369-456.
21. 6 insulin hexamer, Protein Sci. 12, 1902-1913.
22. Seydoux, F., Malhotra, O. P., and Bernhard, S. A. (1974) Half-site reactivity, CRC Crit. Rev. Biochem. 2, 227-257.
23. Dugad, L. B., Cooley, C. R., and Gerig, J. T. (1989) NMR studies of carbonic anhydrase-fluorinated benzenesulfonamide complexes, Biochemistry 28, 3955-3960.
24. Gregory, D. H., and Gerig, J. T. (1991) Prediction of fluorine chemical shifts in proteins, Biopolymers 31, 845-858.
25. Sylvia, L. A., and Gerig, J. T. (1995) NMR studies of the alpha-chymotrypsin-(R)-1-acetamido-2-(4-fluorophenyl)ethane-1-boronic acid complex at pH 7, Biochim. Biophys. Acta 1252, 225-232.
26. Sylvia, L. A., and Gerig, J. T. (1993) NMR studies of the alpha-chymotrypsin-(R)-1-acetamido-2-(4-fluorophenyl)ethane-1-boronic acid complex, Biochim. Biophys. Acta 1163, 321-334.
27. Lau, E. Y., and Gerig, J. T. (1997) Effects of fluorine substitution on the structure and dynamics of complexes of dihydrofolate reductase (Escherichia coli), Biophys. J. 73, 1579-1592.
28. 2+ ions, Biochemistry 24, 1749-1756
29. Huang, S. T., Choi, W. E., Bloom, C. R, Leuenberger, M., and Dunn, M. F. (1997) Carboxylate ions are strong allosteric ligands for the HisB10 sites of the R-state insulin hexamer, Biochemistry 36, 9878-9888.
30. Brader, M. L., Kaarsholm, N. C., Harnung, S. E., and Dunn, M. F. (1997) Ligand perturbation on a pseudotetrahedral Co(II)(His)-3L site. A magnetic circular dichroism study of the Co(II)-substituted insulin hexamer, J. Biol. Chem. 272, 1088-1094.
31. Lian, L.-Y., and Roberts, G. C. K. (1996) Effects of chemical exchange on NMR spectra, in NMR of Macromolecules: A Practical Approach (Roberts, G. C. K., Rickwood, D., and Hames, B. D., Eds.), pp 152-182, Oxford University Press, Oxford, U.K.
32. Ando, M. E., Gerig, J. T., Luk, K. F., and Roe, D. C. (1980) Evidence for multiple forms of p-trifluoromethylbenzenesulfonyl-alpha-chymotrypsin, Can. J. Biochem. 58, 427-433.
33. Ando, M. E., and Gerig, J. T. (1982) Reactions of alpha-chymotrypsin with 4-(trifluoromethyl)-alpha-bromoacetanilide, Biochemistry 21, 2299-2304.
34. Kairi, M., Keder, N. L., and Gerig, J. T. (1990) Conformations of N-(2-fluorophenyl)-N-phenylcarbamoyl-alpha-chymotrypsin, Arch. Biochem. Biophys. 279, 305-314.
35. Kairi, M., and Gerig, J. T. (1990) Conformational dynamics in fluorophenylcarbamoyl-alpha-chymotrypsins, Biochim. Biophys. Acta 1039, 157-170.
36. Jacobson, A. R., and Gerig, J. T. (1991) Structure and dynamics of alpha-chymotrypsin-N-trifluoroacetyl-4-fluorophenylalanine complexes, J. Biomol. NMR 1, 131-144.
37. Ferrari, D., Diers, J. R., Bocian, D. F., Kaarsholm, N. C., and Dunn, M. F. (2001) Raman signatures of ligand binding and allosteric conformation change in hexameric insulin, Biopolym.: Biospectrosc. 58, 249-260.
38. 6 insulin hexamer that binds phenol, Biopolymers 32, 1749-1756.
39. Turkenberg, M. G. W., Whittingham, J. L., Turkenberg, J. P., Dodson, G. G., Derewenda, U., Smith, G. D., Dodson, E. J., Derewenda, A. S., and Xiao, B. (1967) Insulin, monoclinic crystal form, Protein Data Bank entry 1ZNJ.