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X-ray crystallographic studies on hexameric insulins in the presence of helix-stabilizing agents, thiocyanate, methylparaben, and phenol.

Whittingham JL, Chaudhuri S, Dodson EJ, Moody PC, Dodson GG
Biochemistry 34 15553-63 (1995)
Related entries: 1mpj, 3mth

Cited: 35 times
EuropePMC logo PMID: 7492558

Abstract

Three X-ray crystallographic studies have been carried out on pig insulin in the presence of three ligands, thiocyanate, methylparaben (methyl p-hydroxybenzoate), and phenol. In each case, rhombohedral crystals were obtained, which diffracted to 1.8, 1.9, and 2.3 A, respectively. Each crystal structure was very similar to that of 4-zinc pig insulin, which was used as a starting model for PROLSQ refinement (Collaborative Computational Project, Number 4, 1994). The R factors for the refined structures of thiocyanate insulin, methylparaben insulin, and phenol insulin were 19.6, 18.4, and 19.1, respectively. Each crystal structure consists of T3R3f insulin hexamers with two zinc ions per hexamer. In the R3f trimer of the thiocyanate insulin hexamer, one thiocyanate ion is coordinated to the zinc on the hexamer 3-fold axis, but there is no evidence of zinc ion binding in the off-axis zinc ion sites seen in the 4-zinc pig insulin structure. In the methylparaben insulin and phenol insulin hexamers, the phenolic ligands are bound at the dimer-dimer interfaces in the R3f trimers in a manner similar to that of phenol in R6 phenol insulin. The binding of methylparaben appears to make the hexamer more compact by drawing the A and the B chains closer together in the binding site. In all three structures presented herein, the conformations of the first three residues of the B chain in the R3f trimer are extended rather than alpha-helical, as is seen in R6 phenol insulin. The energetics of ligand binding in the insulin hexamer are discussed.

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  1. Zinc-ligand interactions modulate assembly and stability of the insulin hexamer -- a review. Dunn MF. Biometals 18 295-303 (2005)
  2. The metal site as a template for the metalloprotein structure formation. Liu C, Xu H. J. Inorg. Biochem. 88 77-86 (2002)
  3. Solid-state protein formulations. Angkawinitwong U, Sharma G, Khaw PT, Brocchini S, Williams GR. Ther Deliv 6 59-82 (2015)
  4. In Quest for Improved Drugs against Diabetes: The Added Value of X-ray Powder Diffraction Methods. Karavassili F, Valmas A, Fili S, Georgiou CD, Margiolaki I. Biomolecules 7 (2017)

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  1. Mini-proinsulin and mini-IGF-I: homologous protein sequences encoding non-homologous structures. Hua QX, Hu SQ, Jia W, Chu YC, Burke GT, Wang SH, Wang RY, Katsoyannis PG, Weiss MA. J. Mol. Biol. 277 103-118 (1998)
  2. Ligand escape pathways and (un)binding free energy calculations for the hexameric insulin-phenol complex. Vashisth H, Abrams CF. Biophys. J. 95 4193-4204 (2008)
  3. Hybrid insulin cocrystals for controlled release delivery. Brader ML, Sukumar M, Pekar AH, McClellan DS, Chance RE, Flora DB, Cox AL, Irwin L, Myers SR. Nat. Biotechnol. 20 800-804 (2002)
  4. Binding of phenol to R6 insulin hexamers. Berchtold H, Hilgenfeld R. Biopolymers 51 165-172 (1999)
  5. Chemical and thermal stability of insulin: effects of zinc and ligand binding to the insulin zinc-hexamer. Huus K, Havelund S, Olsen HB, van de Weert M, Frokjaer S. Pharm. Res. 23 2611-2620 (2006)
  6. A novel complex of a phenolic derivative with insulin: structural features related to the T-->R transition. Smith GD, Ciszak E, Pangborn W. Protein Sci. 5 1502-1511 (1996)
  7. Spectroscopic and molecular dynamics simulation studies of the interaction of insulin with glucose. Falconi M, Bozzi M, Paci M, Raudino A, Purrello R, Cambria A, Sette M, Cambria MT. Int. J. Biol. Macromol. 29 161-168 (2001)
  8. Raman signatures of ligand binding and allosteric conformation change in hexameric insulin. Ferrari D, Diers JR, Bocian DF, Kaarsholm NC, Dunn MF. Biopolymers 62 249-260 (2001)
  9. Spectroscopic evidence for preexisting T- and R-state insulin hexamer conformations. Choi WE, Borchardt D, Kaarsholm NC, Brzovic PS, Dunn MF. Proteins 26 377-390 (1996)
  10. Stable Monomeric Insulin Formulations Enabled by Supramolecular PEGylation of Insulin Analogues. Maikawa CL, Smith AAA, Zou L, Meis CM, Mann JL, Webber MJ, Appel EA. Adv Ther (Weinh) 3 1900094 (2020)
  11. Crystal structure of ultralente--a microcrystalline insulin suspension. Wagner A, Diez J, Schulze-Briese C, Schluckebier G. Proteins 74 1018-1027 (2009)
  12. Ligand perturbation effects on a pseudotetrahedral Co(II)(His)3-ligand site. A magnetic circular dichroism study of the Co(II)-substituted insulin hexamer. Brader ML, Kaarsholm NC, Harnung SE, Dunn MF. J. Biol. Chem. 272 1088-1094 (1997)
  13. Analysis of insulin allostery in solution and solid state with FTIR. Maltesen MJ, Bjerregaard S, Hovgaard L, Havelund S, van de Weert M. J Pharm Sci 98 3265-3277 (2009)
  14. Crystallographic characterization of two novel crystal forms of human insulin induced by chaotropic agents and a shift in pH. Norrman M, Schluckebier G. BMC Struct. Biol. 7 83 (2007)
  15. Enhancing the T-->R transition of insulin by helix-promoting sequence modifications at the N-terminal B-chain. Shneine J, Voswinkel M, Federwisch M, Wollmer A. Biol. Chem. 381 127-133 (2000)
  16. High-resolution powder X-ray data reveal the T(6) hexameric form of bovine insulin. Margiolaki I, Giannopoulou AE, Wright JP, Knight L, Norrman M, Schluckebier G, Fitch AN, Von Dreele RB. Acta Crystallogr. D Biol. Crystallogr. 69 978-990 (2013)
  17. Structural signatures of the complex formed between 3-nitro-4-hydroxybenzoate and the Zn(II)-substituted R(6) insulin hexamer. Olsen HB, Leuenberger-Fisher MR, Kadima W, Borchardt D, Kaarsholm NC, Dunn MF. Protein Sci. 12 1902-1913 (2003)
  18. Structural interpretation of reduced insulin activity as seen in the crystal structure of human Arg-insulin. Sreekanth R, Pattabhi V, Rajan SS. Biochimie 90 467-473 (2008)
  19. Metal induced structural changes observed in hexameric insulin. Sreekanth R, Pattabhi V, Rajan SS. Int. J. Biol. Macromol. 44 29-36 (2009)
  20. The structures of T6, T3R3 and R6 bovine insulin: combining X-ray diffraction and absorption spectroscopy. Frankær CG, Knudsen MV, Norén K, Nazarenko E, Ståhl K, Harris P. Acta Crystallogr. D Biol. Crystallogr. 68 1259-1271 (2012)
  21. 1H[19F] NOE NMR structural signatures of the insulin R6 hexamer: evidence of a capped HisB10 site in aryl- and arylacryloyl-carboxylate complexes. Keidel D, Bonaccio M, Ghaderi N, Niks D, Borchardt D, Dunn MF. Chembiochem 10 450-453 (2009)
  22. Characterization of insulin crystalline form in isolated β-cell secretory granules. Asai S, Moravcová J, Žáková L, Selicharová I, Hadravová R, Brzozowski AM, Nováček J, Jiráček J. Open Biol 12 220322 (2022)
  23. Formulation Excipients and Their Role in Insulin Stability and Association State in Formulation. Maikawa CL, Nguyen LT, Mann JL, Appel EA. Pharm Res 39 2721-2728 (2022)
  24. Insulin Hexamer-Caged Gadolinium Ion as MRI Contrast-o-phore. Taylor SK, Tran TH, Liu MZ, Harris PE, Sun Y, Jambawalikar SR, Tong L, Stojanovic MN. Chemistry 24 10646-10652 (2018)
  25. Insulin and insulin mutants stimulate glucose uptake in rat adipocytes. Yao S, Zhang X, Xu Y, Zhang X, Zhu S. Sci. China, C, Life Sci. 42 63-67 (1999)
  26. SiteFerret: Beyond Simple Pocket Identification in Proteins. Gagliardi L, Rocchia W. J Chem Theory Comput 19 5242-5259 (2023)
  27. The T2 structure of polycrystalline cubic human insulin. Triandafillidis DP, Karavassili F, Spiliopoulou M, Valmas A, Athanasiadou M, Nikolaras G, Fili S, Kontou P, Bowler MW, Chasapis CT, Von Dreele RB, Fitch AN, Margiolaki I. Acta Crystallogr D Struct Biol 79 374-386 (2023)
  28. Vitamin E induces regular structure and stability of human insulin, more intense than vitamin D3. Soleymani H, Saboury AA, Moosavi-Movahedi AA, Rahmani F, Maleki J, Yousefinejad S, Maghami P. Int. J. Biol. Macromol. 93 868-878 (2016)


Related citations provided by authors (2)

  1. The structure of a rhombohedral R6 insulin hexamer that binds phenol.. Smith GD, Dodson GG Biopolymers 32 441-5 (1992)
  2. Phenol stabilizes more helix in a new symmetrical zinc insulin hexamer.. Derewenda U, Derewenda Z, Dodson EJ, Dodson GG, Reynolds CD, Smith GD, Sparks C, Swenson D Nature 338 594-6 (1989)

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