Thermodynamics of formation of the insulin hexamer: Metal-stabilized proton-coupled assembly of quaternary structure

Biochemistry

Volumn 53, Issue 8, 2014, Pages 1296-1301

  Carpenter, Margaret C ^a   Wilcox, Dean E ^a  

^a Lamont Doherty Earth Observatory   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DESOLVATION; HEXAMERS; INSULIN HEXAMER; INSULIN MONOMERS; ISOTHERMAL TITRATION CALORIMETRY; QUATERNARY STRUCTURE; THERMODYNAMICS OF FORMATIONS;

CHELATION; GERMANIUM ALLOYS; INSULIN; METAL IONS; THERMODYNAMICS;

ZINC;

EDETIC ACID; INSULIN; METAL; METAL ION; MONOMER; PROTON; ZINC;

ARTICLE; CHELATION; ENTHALPY; ENTROPY; ISOTHERMAL TITRATION CALORIMETRY; MEASUREMENT; PH; PRIORITY JOURNAL; PROTON TRANSPORT; QUANTITATIVE ANALYSIS; THERMODYNAMICS;

HUMANS; INSULIN; MODELS, MOLECULAR; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; PROTEIN STRUCTURE, QUATERNARY; PROTONS; THERMODYNAMICS; ZINC;

EID: 84896761223     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi4016567     Document Type: Article

References (37)

1. 2+-dependent double-stranded DNA binding activity J. Biol. Chem. 286, 30759-30768
2. 2 heterotetramer, calprotectin, illustrates how conformational changes of interacting α-helices can determine specific association of two EF-hand proteins J. Mol. Biol. 370, 887-898
3. Raman, C. S., Li, H., Martasek, P., Kral, V., Masters, B. S. S., and Poulos, T. L. (1998) Crystal structure of constitutive endothelial nitric oxide synthase: a paradigm for pterin function involving a novel metal center Cell 95, 939-950
4. Hopfner, K.-P., Craig, L., Moncalian, G., Zinkel, R. A., Usui, T., Owen, B. A. L., Karcher, A., Henderson, B., Bodmer, J.-L., McMurray, C. T., Carney, J. P., Petrini, J. H. J., and Tainer, J. A. (2002) The Rad50 zinc-hook is a structure joining Mre11 complexes in DNA recombination and repair Nature 418, 562-565
5. Callaghan, A. J., Marcida, M. J., Stead, J. A., McDowell, K. J., Scott, W. G., and Luisi, B. F. (2005) "Zn-link": A metal-sharing interface that organizes the quarternary structure and catalytic site of the endoribonuclease, RNase E Nature 437, 1187-1191
6. Brodin, J. D., Ambroggio, X. I., Tang, C., Parent, K. N., Baker, T. S., and Tezcan, F. A. (2012) Metal-directed, chemically tunable assembly of one-, two- and three-dimensional crystalline protein arrays Nat. Chem. 4, 375-382 and references therein
7. Dodson, G. and Steiner, D. (1998) The role of assembly in insulin's biosynthesis Curr. Opin. Struct. Biol. 8, 189-194
8. Waugh, D. F. (1946) A fibrous modification of insulin: The heat precipitate of insulin J. Am. Chem. Soc. 68, 247-250
9. Brange, J., Andersen, L., Laursen, E. D., Meyn, G., and Rasmussen, E. (1997) Towards understanding insulin fibrillation J. Pharm. Sci. 86, 517-525
10. Baker, E. N., Blundell, T. L., Cutfield, J. F., Cutfield, S. M., Dodson, E. J., Dodson, G. R., Hodgkin, D. M., Hubbard, R. E., Isaacs, N. W., Reynolds, C. D., Sakabe, K., Sakabe, N., and Vijayan, N. M. (1988) The structure of 2-zinc pig insulin crystals at 1.5 Å resolution Philos. Trans. R. Soc., B 319, 369-456
11. 6 human insulin at 1.0 Å resolution Acta Crystallogr., Sect. D 59, 474-482
12. Storm, M. C. and Dunn, M. F. (1985) The Glu(B13) carboxylates of the insulin hexamer form a cage for cadmium and calcium ions Biochemistry 24, 1749-1756
13. Summerell, J. M., Osmond, A., and Smith, G. H. (1965) An equilibrium-dialysis study of the binding of zinc to insulin Biochem. J. 95, 31
14. Grant, P. T., Coombs, T. L., and Frank, B. H. (1972) Differences in the nature of the interaction of insulin and proinsulin with zinc Biochem. J. 126, 433-440
15. Goldman, J. and Carpenter, F. H. (1974) Zinc binding, circular dichroism, and equilibrium sedimentation studies on insulin (bovine) and several of its derivatives Biochemistry 13, 4566-4574
16. Dunn, M. F. (2005) Zinc-ligand interactions modulate assembly and stability of the insulin hexamer-a review BioMetals 18, 295-303 and references therein
17. Brader, M. L. (1997) Zinc coordination, asymmetry, and allostery of the human insulin hexamer J. Am. Chem. Soc. 119, 7603-7604
18. Huus, K., Havelund, S., Olsen, H. B., van de Weert, M., and Frokjaer, S. (2005) Thermal dissociation and unfolding of insulin Biochemistry 44, 11171-11177
19. Huus, S., Havelund, K., Olsen, H. B., Sigurskjold, B. W., van de Weert, M., and Frokjaer, S. (2006) Ligand binding and thermostability of different allosteric states of the insulin zinc hexamer Biochemistry 45, 4014-4024
20. Lisi, G. P., Png, C. Y. M., and Wilcox, D. E. Thermodynamic contributions to the stability of the insulin hexamer, Biochemistry. Submitted for publication.
21. Birnbaum, D. T., Dodd, S. W., Saxberg, B. E. H., Varshavsky, A. D., and Beals, J. M. (1996) Hierarchical modeling of phenolic ligands binding to 2Zn-insulin hexamers Biochemistry 35, 5366-5378
22. McGraw, S. E. and Lindenbaum, S. (1990) The use of microcalorimetry to measure thermodynamic parameters of the binding of ligands to insulin Pharm. Res. 7, 606-611
23. Brange, J., Ribel, U., Hansen, J. F., Dodson, G. G., Hansen, M. T., Havelund, S., Melberg, S. G., Norris, F., Norris, K., Snel, L., Sørenson, A. R., and Voight, H. O. (1988) Monomeric insulins obtained by protein engineering and their medical implications Nature 333, 679-682
24. Coffman, F. and Dunn, M. F. (1988) Insulin-metal ion interactions: The binding of divalent cations to insulin hexamers and tetramers and the assembly of insulin hexamers Biochemistry 27, 6179-6187
25. Nielsen, L., Khurana, R., Coats, A., Frokjaer, S., Brange, J., Vyas, S., Uversky, V. N., and Fink, A. L. (2001) Effect of environmental factors on the kinetics of insulin fibril formation: Elucidation of the molecular mechanism Biochemistry 40, 6036-6046
26. Bouchard, M., Zurdo, J., Nettlenton, E. J., Dobson, C. M., and Robinson, C. V. (2000) Formation of insulin amyloid fibrils followed by FTIR simultaneously with CD and electron microscopy Protein Sci. 9, 1960-1967
27. Ahmad, A., Uversky, V. N., Hong, D., and Fink, A. L. (2005) Early events in the fibrillation of monomeric insulin J. Biol. Chem. 280, 42669-42675
28. Critically Selected Stability Constants of Metal Complexes, Version 8.0, NIST, Gaithersburg, MD.
29. Grossoehme, N. E., Spuches, A. M., and Wilcox, D. E. (2012) Application of isothermal titration calorimetry in bioinorganic chemistry J. Biol. Inorg. Chem. 15, 1183-1191
30. Sigurskjold, B. W. (2000) Exact analysis of competition ligand binding by displacement isothermal titration calorimetry Anal. Biochem. 277, 260-266
31. Yang, Y., Petkova, A., Huang, K., Xu, B., Hua, Q.-X., Ye, I.-J., Chu, Y.-C., Hu, S.-Q., Phillips, N. B., Whittaker, J., Ismail-Beigi, F., Mackin, R. B., Katsoyannis, P. G., Tycko, R., and Weiss, M. A. (2010) An Achilles' heel in an amyloidogenic protein and its repair: insulin fibrillation and therapeutic design J. Biol. Chem. 285, 10806-10821 and references therein
32. Zhang, Y. (2001) Ph.D. Thesis, Dartmouth College, Hanover, NH.
33. 4 transcription factor site J. Am. Chem. Soc. 134, 10405-10418
34. Masouka, J., Hegenauer, J., Van Dyke, B. R., and Saltman, P. (1993) Intrinsic stoichiometric equilibrium constants for the binding of zinc(II) and copper(II) to the high affinity site of serum albumin J. Biol. Chem. 268, 21533-21537
35. Chu, A. H. and Ackers, G. K. (1981) Mutual effects of protons, NaCl, and oxygen on the dimer-tetramer assembly of human hemoglobin J. Biol. Chem. 256, 1199-1205
36. Antonini, E., Wyman, J., Brunori, M., Fronticelli, C., Bucci, E., and Rossi-Fanelli, A. (1965) Studies on the relations between molecular and functional properties of hemoglobin: V. The influence of temperature on the Bohr effect in human and horse hemoglobin J. Biol. Chem. 240, 1096-1103
37. Rollema, H. S., de Bruin, S. H., Janssen, L. H., and van Os, G. A. (1975) The effect of potassium chloride on the Bohr effect of human hemoglobin J. Biol. Chem. 250, 1333-1339