Ligand-controlled assembly of hexamers, dihexamers, and linear multihexamer structures by the engineered acylated insulin degludec

Biochemistry

Volumn 52, Issue 2, 2013, Pages 295-309

  Steensgaard, Dorte B ^a   Schluckebier, Gerd ^a   Strauss, Holger M ^a   Norrman, Mathias ^a   Thomsen, Jens K ^a   Friderichsen, Anders V ^a   Havelund, Svend ^a   Jonassen, Ib ^a  

^a NOVO NORDISK A S   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

AVERAGE MOLAR MASS; HEXAMERS; INSULIN HEXAMER; LIGAND BINDING PROPERTIES; LINEAR ARRAYS; NOVEL CONCEPT; PHARMACEUTICAL FORMULATION; PHENOLIC LIGANDS; PROTEIN FOLDS; QUATERNARY STRUCTURE; SLOW RELEASE; SOLVENT CONDITIONS; STRUCTURAL METHODS; SUPRAMOLECULAR STRUCTURE;

ACYLATION; BINDING ENERGY; GLUCOSE; LIGANDS; PHENOLS; PROTEIN FOLDING; ZINC;

INSULIN;

INSULIN DEGLUDEC; PHENOL; RESORCINOL; ZINC;

ARTICLE; CHEMICAL INTERACTION; DRUG BINDING; DRUG FORMULATION; DRUG STRUCTURE; MOLECULAR WEIGHT; PRIORITY JOURNAL; PROTEIN FOLDING;

ACETYLATION; AMINO ACID SEQUENCE; CIRCULAR DICHROISM; CRYSTALLOGRAPHY, X-RAY; HUMANS; INSULIN, LONG-ACTING; LIGANDS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHENOL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; RESORCINOLS; SCATTERING, SMALL ANGLE; ULTRACENTRIFUGATION; X-RAY DIFFRACTION; ZINC;

EID: 84872522953     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi3008609     Document Type: Article

References (63)

1. DeFelippis, M. R., Chance, R. E., and Frank, B. H. (2001) Insulin self-association and the relationship to pharmacokinetics and pharmacodynamics Crit. Rev. Ther. Drug Carrier Syst. 18, 201-264
2. Brange, J., Ribel, U., Hansen, J. F., Dodson, G., Hansen, M. T., Havelund, S., Melberg, S. G., Norris, F., Norris, K., Snel, L., Soerensen, A. R., and Voight, H. O. (1988) Monomeric insulins obtained by protein engineering and their medical implications Nature 333, 679-682
3. Brange, J. and Volund, A. (1999) Insulin analogs with improved pharmacokinetic profiles Adv. Drug Delivery Rev. 35, 307-335
4. Brems, D. N., Alter, L. A., Beckage, M. J., Chance, R. E., DiMarchi, R. D., Green, L. K., Long, H. B., Pekar, A. H., Shields, J. E., and Frank, B. H. (1992) Altering the association properties of insulin by amino acid replacement Protein Eng. 5, 527-533
5. Kurtzhals, P., Havelund, S., Jonassen, I., Kiehr, B., Larsen, U. D., Ribel, U., and Markussen, J. (1995) Albumin binding of insulins acylated with fatty acids: Characterization of the ligand-protein interaction and correlation between binding affinity and timing of the insulin effect in vivo Biochem. J. 312, 725-731
6. Jonassen, I., Havelund, S., Ribel, U., Plum, A., Loftager, M., Hoeg-Jensen, T., Volund, A., and Markussen, J. (2006) Biochemical and physiological properties of a novel series of long-acting insulin analogs obtained by acylation with cholic acid derivatives Pharm. Res. 23, 49-55
7. Olsen, H. B. and Kaarsholm, N. C. (2000) Structural effects of protein lipidation as revealed by LysB29-myristoyl, des(B30) insulin Biochemistry 39, 11893-11900
8. Havelund, S., Plum, A., Ribel, U., Jonassen, I., Volund, A., Markussen, J., and Kurtzhals, P. (2004) The mechanism of protraction of insulin detemir, a long-acting, acylated analog of human insulin Pharm. Res. 21, 1498-1504
9. Clodfelter, D. K., Pekar, A. H., Rebhun, D. M., Destrampe, K. A., Havel, H. A., Myers, S. R., and Brader, M. L. (1998) Effects of non-covalent self-association on the subcutaneous absorption of a therapeutic peptide Pharm. Res. 15, 254-262
10. Steensgaard, D. B., Thomsen, J. K., Olsen, H. B., and Knudsen, L. B. (2008) The molecular basis for the delayed absorption of the once-daily human GLP-1 analogue, liraglutide Diabetes 57 (Suppl. 1) A164
11. Birkeland, K. I., Home, P. D., Wendisch, U., Ratner, R. E., Johansen, T., Endahl, L. A., Lyby, K., Jendle, J. H., Roberts, A. P., DeVries, J. H., and Meneghini, L. F. (2011) Insulin degludec in type 1 diabetes: A randomized controlled trial of a new-generation ultra-long-acting insulin compared with insulin glargine Diabetes Care 34, 661-665
12. Heise, T., Tack, C. J., Cuddihy, R., Davidson, J., Gouet, D., Liebl, A., Romero, E., Mersebach, H., Dykiel, P., and Jorde, R. (2011) A new-generation ultra-long-acting basal insulin with a bolus boost compared with insulin glargine in insulin-naive people with type 2 diabetes: A randomized, controlled trial Diabetes Care 34, 669-674
13. Jonassen, I., Havelund, S., Hoeg-Jensen, T., Steensgaard, D. B., Wahlund, P. O., and Ribel, U. (2012) Design of the Novel Protraction Mechanism of Insulin Degludec, an Ultra-long Acting Basal Insulin Pharm. Res. 29, 2104-2114
14. Dunn, M. F. (2005) Zinc-ligand interactions modulate assembly and stability of the insulin hexamer: A review BioMetals 18, 295-303
15. Ludvigsen, S., Roy, M., Thogersen, H., and Kaarsholm, N. C. (1994) High-resolution structure of an engineered biologically potent insulin monomer, B16 Tyr → His, as determined by nuclear-magnetic-resonance spectroscopy Biochemistry 33, 7998-8006
16. Olsen, H. B., Ludvigsen, S., and Kaarsholm, N. C. (1996) Solution structure of an engineered insulin monomer at neutral pH Biochemestry 35, 8836-8845
17. Jorgensen, A. M., Kristensen, S. M., Led, J. J., and Balschmidt, P. (1992) Three-dimensional solution structure of an insulin dimer. A study of the B9(Asp) mutant of human insulin using nuclear magnetic resonance, distance geometry and restrained molecular dynamics J. Mol. Biol. 227, 1146-1163
18. Adams, M. J., Blundell, T. L., Dodson, E. J., Dodson, G. G., Vijayan, M., Baker, E. N., Harding, M. M., Hodgkin, D. C., Rimmer, B., and Sheat, S. (1969) Structure of Rhombohedral 2 Zinc Insulin Crystals Nature 224, 491-495
19. 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
20. Kaarsholm, N. C., Ko, H.-C., and Dunn, M. F. (1989) Comparison of Solution Structural Flexibility and Zinc Binding Domains for Insulin, Proinsulin, and Miniproinsulin Biochemistry 28, 4427-4435
21. Dodson, G. G., Cutfield, S., Hoenjet, E., Wollmer, A., and Brandenburg, D. (1979) Crystal Structure, Aggregation, and Biological Potency of Beef Insulin Cross Linked at A1 and B29 by Diaminosuberic Acid. In Insulin: Chemistry, Structure, and Function of Insulin and Related Hormones. Proceedings of the Second International Insulin Symposium (Brandenburg, D. and Wollmer, A., Eds.) pp 17-26, Aachen, Germany, September 4-7, De Gruyter, Berlin.
22. Huang, S. T., Choi, W. E., Bloom, C., 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
23. Rahuel-Clermont, S., French, C. A., Kaarsholm, N. C., Dunn, M. F., and Chou, C. I. (1997) Mechanisms of stabilization of the insulin hexamer through allosteric ligand interactions Biochemistry 36, 5837-5845
24. Seydoux, F., Malhotra, O. P., Bernhard, S. A., and Stark, G. (1974) Half-Site Reactivity Crit. Rev. Biochem. Mol. Biol. 2, 227-257
25. 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
26. Bloom, C. R., Kaarsholm, N. C., Ha, J., and Dunn, M. F. (1997) Half-site reactivity, negative cooperativity, and positive cooperativity: Quantitative considerations of a plausible model Biochemistry 36, 12759-12765
27. Kabsch, W. (2010) XDS Acta Crystallogr. D66, 125-132
28. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data Methods Enzymol. 276, 307-326
29. Bailey, S. (1994) The CCP4 suite: Programs for protein crystallography Acta Crystallogr. D50, 760-763
30. Adams, P. D., Grosse-Kunstleve, R. W., Hung, L. W., Ioerger, T. R., McCoy, A. J., Moriarty, N. W., Read, R. J., Sacchettini, J. C., Sauter, N. K., and Terwilliger, T. C. (2002) PHENIX: Building new software for automated crystallographic structure determination Acta Crystallogr. D58, 1948-1954
31. Schuck, P. (2000) Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and Lamm equation modeling Biophys. J. 78, 1606-1619
32. Stafford, W. F., III (1992) Boundary analysis in sedimentation transport experiments: A procedure for obtaining sedimentation coefficient distributions using the time derivative of the concentration profile Anal. Biochem. 203, 295-301
33. Yphantis, D. A. (1964) Equilibrium ultracentrifugation of dilute solutions Biochemistry 3, 297-317
34. Roessle, M. W., Klaering, R., Ristau, U., Robrahn, B., Jahn, D., Gehrmann, T., Konarev, P., Round, A., Fiedler, S., Hermes, C., and Svergun, D. (2007) Upgrade of the small-angle X-ray scattering beamline X33 at the European Molecular Biology Laboratory, Hamburg J. Appl. Crystallogr. 40, 190-194
35. Petoukhov, M. V., Konarev, P. V., Kikhney, A. G., and Svergun, D. I. (2007) ATSAS 2.1: Towards automated and web-supported small-angle scattering data analysis J. Appl. Crystallogr. 40, 223-228
36. Konarev, P. V., Volkov, V. V., Sokolova, A. V., Koch, M. H. J., and Svergun, D. I. (2003) PRIMUS: A Windows PC-based system for small-angle scattering data analysis J. Appl. Crystallogr. 36, 1277-1282
37. Svergun, D. (1992) Determination of the regularization parameter in indirect-transform methods using perceptual criteria J. Appl. Crystallogr. 25, 495-503
38. Svergun, D., Barberato, C., and Koch, M. H. J. (1995) CRYSOL: A Program to Evaluate X-ray Solution Scattering of Biological Macromolecules from Atomic Coordinates J. Appl. Crystallogr. 28, 768-773
39. Franke, D. and Svergun, D. I. (2009) DAMMIF, a program for rapid ab-initio shape determination in small-angle scattering J. Appl. Crystallogr. 42, 342-346
40. DeLano, W. L. (2002) The PyMOL Molecular Graphics System, DeLano Scientific, San Carlos, CA.
41. Berman, H., Henrick, K., Nakamura, H., and Markley, J. L. (2007) The worldwide Protein Data Bank (wwPDB): Ensuring a single, uniform archive of PDB data Nucleic Acids Res. 35, D301-D303
42. Diao, J. (2003) Crystallographic titration of cubic insulin crystals: pH affects GluB13 switching and sulfate binding Acta Crystallogr. D59, 670-676
43. Schachman, H. K. (1959) Ultracentrifugation in Biochemistry, Vol. 35, p 272, Academic Press, New York.
44. Svedberg, T. and Pedersen, K. O. (1940) Die Ultrazentrifuge. In Handbuch der Kolloidwissenschaft, Vol. 8, Steinkopff, Dresden.
45. Chervenka, C. H. (1969) A Manual of Methods for the Analytical Ultracentrifuge, Spinco Division of Beckman Instruments, Palo Alto, CA.
46. Attri, A. K., Fernandez, C., and Minton, A. P. (2010) pH-dependent self-association of zinc-free insulin characterized by concentration-gradient static light scattering Biophys. Chem. 148, 28-33
47. Jeffrey, P. D., Milthorpe, B. K., and Nichol, L. W. (1976) Polymerization pattern of insulin at pH 7.0 Biochemistry 15, 4660-4665
48. Mark, A. E. and Jeffrey, P. D. (1990) The self-association of zinc-free bovine insulin. Four model patterns and their significance Biol. Chem. Hoppe-Seyler 371, 1165-1174
49. Smith, G. D., Ciszak, E., Magrum, L. A., Pangborn, W. A., and Blessing, R. H. (2000) R6 hexameric insulin complexed with m-cresol or resorcinol Acta Crystallogr. D56, 1541-1548
50. Bentley, G., Dodson, G., and Lewitova, A. (1978) Rhombohedral insulin crystal transformation J. Mol. Biol. 126, 871-875
51. Wagner, A., Diez, J., Schulze-Briese, C., and Schluckebier, G. (2009) Crystal structure of ultralente: A microcrystalline insulin suspension Proteins 74, 1018-1027
52. Whittingham, J. L., Chaudhuri, S., Dodson, E. J., Moody, P. C., 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
53. Chayen, N. E., Stewart, P. D. S., and Blow, D. M. (1992) Microbatch crystallization under oil. A new technique allowing many small-volume crystallization trials J. Cryst. Growth 122, 176-180
54. Brader, M. L., Kaarsholm, N. C., Lee, R. W., 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
55. Kruger, P., Gilge, G., Cabuk, Y., and Wollmer, A. (1990) Cooperativity and intermediate states in the T-R-structural transformation of insulin Biol. Chem. Hoppe-Seyler 371, 669-673
56. Jimenez, J. L., Nettleton, E. J., Bouchard, M., Robinson, C. V., Dobson, C. M., and Saibil, H. R. (2002) The protofilament structure of insulin amyloid fibrils Proc. Natl. Acad. Sci. U.S.A. 99, 9196-9201
57. Harding, S. E. (1992) Sedimentation analysis of polysaccharides. In Analytical Ultracentrifugation in Biochemistry and Polymer Science, pp 495-516, The Royal Society of Chemistry, Nottingham, U.K.
58. Uversky, V. N. (2002) What does it mean to be natively unfolded? Eur. J. Biochem. 269, 2-12
59. Whittingham, J. L., Havelund, S., and Jonassen, I. (1997) Crystal structure of a prolonged-acting insulin with albumin-binding properties Biochemistry 36, 2826-2831
60. Monod, J., Wyman, J., and Changeux, J.-P. (1965) On the nature of allosteric transitions: A plausible model J. Mol. Biol. 12, 88-118
61. Hvidt, S. (1991) Insulin association in neutral solutions studied by light scattering Biophys. Chem. 39, 205-213
62. Attri, A. K., Fernandez, C., and Minton, A. P. (2010) Self-association of Zn-insulin at neutral pH: Investigation by concentration gradient-static and dynamic light scattering Biophys. Chem. 148, 23-27
63. Phillips, N. B., Wan, Z. L., Whittaker, L., Hu, S. Q., Huang, K., Hua, Q. X., Whittaker, J., Ismail-Beigi, F., and Weiss, M. A. (2010) Supramolecular protein engineering: Design of zinc-stapled insulin hexamers as a long acting depot J. Biol. Chem. 285, 11755-11759