Quaternary conformational stability: The effect of reversible self-association on the fibrillation of two insulin analogs

Biotechnology and Bioengineering

Volumn 108, Issue 10, 2011, Pages 2359-2370

  Ludwig, D Brett ^a   Webb, Jonathan N ^b   Fernández, Cristina ^c   Carpenter, John F ^d   Randolph, Theodore W ^a  

^a University of Colorado at Boulder   (United States)

^b ELI LILLY AND COMPANY   (United States)

^c NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^d UNIVERSITY OF COLORADO   (United States)

Author keywords

Conformational stability; Protein aggregation; Quaternary structure; Reversible self association

Indexed keywords

AGGREGATION MODEL; COMPETITIVE INHIBITION; COMPOSITION GRADIENT; CONFORMATIONAL STABILITIES; FAR ULTRAVIOLET; FIBRIL GROWTH; FIRST-ORDER RATE CONSTANTS; FOURIER TRANSFORM INFRARED; FTIR; MONOMER ADDITION; MULTI-ANGLE LIGHT SCATTERINGS; PROTEIN AGGREGATION; PROTEIN CONCENTRATIONS; PROTEIN SECONDARY STRUCTURE; QUATERNARY STRUCTURE; ROOM TEMPERATURE; SECOND DERIVATIVES; SELF-ASSOCIATIONS; SOLUBLE PROTEINS;

AGGLOMERATION; ASSOCIATION REACTIONS; CONFORMATIONS; DICHROISM; DIMERS; FOURIER TRANSFORMS; PH EFFECTS; PROTEINS; RATE CONSTANTS; SPECTROSCOPIC ANALYSIS;

INSULIN;

DIMER; HUMAN INSULIN; INSULIN DERIVATIVE; INSULIN LISPRO; MONOMER; INSULIN; PROTEIN AGGREGATE;

ALPHA HELIX; ARTICLE; BETA SHEET; CIRCULAR DICHROISM; COMPETITIVE INHIBITION; CONCENTRATION (PARAMETERS); CONFORMATION; DRUG STABILITY; FIBER; FOURIER TRANSFORM MASS SPECTROMETRY; LIGHT SCATTERING; PROTEIN AGGREGATION; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; ULTRAVIOLET RADIATION; CHEMISTRY; HUMAN; INFRARED SPECTROSCOPY; PH; PROTEIN QUATERNARY STRUCTURE;

CIRCULAR DICHROISM; HUMANS; HYDROGEN-ION CONCENTRATION; INSULIN; PROTEIN AGGREGATES; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; SPECTROSCOPY, FOURIER TRANSFORM INFRARED;

EID: 80051800704     PISSN: 00063592     EISSN: 10970290     Source Type: Journal    
DOI: 10.1002/bit.23188     Document Type: Article

References (60)

1. Adler AJ, Greenfield NJ, Fasman GD. 1973. Circular dichroism and optical rotatory dispersion of proteins and polypeptides. Methods Enzymol 27:675-735.
2. Ahmad A, Millett IS, Doniach S, Uversky VN, Fink AL. 2003. Partially folded intermediates in insulin fibrillation. Biochemistry 42(39): 11404-11416.
3. Alford JR, Kendrick BS, Carpenter JF, Randolph TW. 2008. High concentration formulations of recombinant human interleukin-1 receptor antagonist: II. Aggregation kinetics. J Pharm Sci 97(8): 3005-3021.
4. Anchordoquy TJ, Izutsu KI, Randolph TW, Carpenter JF. 2001. Maintenance of quaternary structure in the frozen state stabilizes lactate dehydrogenase during freeze-drying. Arch Biochem Biophys 390(1): 35-41.
5. Andrews JM, Roberts CJ. 2007. A Lumry-Eyring nucleated polymerization model of protein aggregation kinetics: 1. Aggregation with pre-equilibrated unfolding. J Phys Chem B 111(27): 7897-7913.
6. Attri AK, Minton AP. 2005. New methods for measuring macromolecular interactions in solution via static light scattering: Basic methodology and application to nonassociating and self-associating proteins. Anal Biochem 337(1): 103-110.
7. Attri, A, Fernandez, C. Minton, AP. 2010. pH-dependent self-association of zinc-free insulin characterized by concentration-gradient static light scattering. Biophys Chem 337(1-3): 28-33.
8. Bakaysa DL, Radziuk J, Havel HA, Brader ML, Li S, Dodd SW, Beals JM, Pekar AH, Brems DN. 1996. Physicochemical basis for the rapid time-action of LysB28ProB29-insulin: Dissociation of a protein-ligand complex. Protein Sci 5(12): 2521-2531.
9. Banting FG, Best CH, Collip JB, Campbell WR, Fletcher AA. 1922. Pancreatic extracts in the treatment of diabetes mellitus. Toronto: The University Library: pub. by the librarian, p. 6.
10. Brange J. 1994. Stability of insulin: Studies on the physical and chemical stability of insulin in pharmaceutical formulation. London: Kluwer Academic Publishers.
11. Brange J, Owens DR, Kang S, Volund A. 1990. Monomeric insulins and their experimental and clinical implications. Diabetes Care 13(9): 923-954.
12. Brange J, Andersen L, Laursen ED, Meyn G, Rasmussen E. 1997. Toward understanding insulin fibrillation. J Pharm Sci 86(5): 517-525.
13. Brems DN, Alter LA, Beckage MJ, Chance RE, DiMarchi RD, Green LK, Long HB, Pekar AH, Shields JE, Frank BH. 1992. Altering the association properties of insulin by amino acid replacement. Protein Eng 5(6): 527-533.
14. Chance RE, Frank BH. 1993. Research, development, production, and safety of biosynthetic human insulin. Diabetes Care 16 (Suppl 3): 133-142.
15. Ciszak E, Beals JM, Frank BH, Baker JC, Carter ND, Smith GD. 1995. Role of C-terminal B-chain residues in insulin assembly: The structure of hexameric LysB28ProB29-human insulin. Structure 3(6): 615-622.
16. Cromwell ME, Hilario E, Jacobson F. 2006. Protein aggregation and bioprocessing. AAPS J 8(3): E572-E579.
17. Dische FE, Wernstedt C, Westermark GT, Westermark P, Pepys MB, Rennie JA, Gilbey SG, Watkins PJ. 1988. Insulin as an amyloid-fibril protein at sites of repeated insulin injections in a diabetic patient. Diabetologia 31(3): 158-161.
18. Dong A, Huang P, Caughey WS. 1990. Protein secondary structures in water from second-derivative amide I infrared spectra. Biochemistry 29(13): 3303-3308.
19. Dong A, Caughey B, Caughey WS, Bhat KS, Coe JE. 1992. Secondary structure of the pentraxin female protein in water determined by infrared spectroscopy: Effects of calcium and phosphorylcholine. Biochemistry 31:9364-9370.
20. Dong A, Meyer JD, Brown JL, Manning MC, Carpenter JF. 2000. Comparative Fourier transform infrared and circular dichroism spectroscopic analysis of alpha1-proteinase inhibitor and ovalbumin in aqueous solution. Arch Biochem Biophys 383(1): 148-155.
21. Federwisch M, Dieken ML, De Meyts P. 2002. Insulin and related proteins-Structure to function and pharmacology. London: Kluwer Academic Publishers.
22. Feingold V, Jenkins AB, Kraegen EW. 1984. Effect of contact material on vibration-induced insulin aggregation. Diabetologia 27(3): 373-378.
23. Frank BH, Veros AJ. 1968. Physical studies on proinsulin-association behavior and conformation in solution. Biochem Biophys Res Commun 32(2): 155-160.
24. Fredericq E. 1956. The association of insulin molecular units in aqueous solutions. Arch Biochem Biophys 65(1): 218-228.
25. Goldman J, Carpenter FH. 1974. Zinc binding, circular dichroism, and equilibrium sedimentation studies on insulin (bovine) and several of its derivatives. Biochemistry 13(22): 4566-4574.
26. Hua QX, Weiss MA. 2004. Mechanism of insulin fibrillation: The structure of insulin under amyloidogenic conditions resembles a protein-folding intermediate. J Biol Chem 279(20): 21449-21460.
27. Jeffrey PD, Coates JH. 1966. An equilibrium ultracentrifuge study of the self-association of bovine insulin. Biochemistry 5(2): 489-498.
28. Jeffrey PD, Milthorpe BK, Nichol LW. 1976. Polymerization pattern of insulin at pH 7.0. Biochemistry 15(21): 4660-4665.
29. Jimenez JL, Nettleton EJ, Bouchard M, Robinson CV, Dobson CM, Saibil HR. 2002. The protofilament structure of insulin amyloid fibrils. Proc Natl Acad Sci USA 99(14): 9196-9201.
30. Johnson WC Jr. 1988. Secondary structure of proteins through circular dichroism spectroscopy. Annu Rev Biophys Biophys Chem 17:145-166.
31. Kotarek JA, Johnson KC, Moss MA. 2008. Quartz crystal microbalance analysis of growth kinetics for aggregation intermediates of the amyloid-beta protein. Anal Biochem 378(1): 15-24.
32. Kruger P, Gilge G, Cabuk Y, Wollmer A. 1990. Cooperativity and intermediate states in the T-R-structural transformation of insulin. Biol Chem Hoppe Seyler 371(8): 669-673.
33. Laue T. 1992. Short column sedimentation equilibrium analysis for rapid characterization of macromolecules in solution. Fullerton, CA: Beckman Coulter.
34. Millican RL, Brems DN. 1994. Equilibrium intermediates in the denaturation of human insulin and two monomeric insulin analogs. Biochemistry 33(5): 1116-1124.
35. Murphy RM. 2002. Peptide aggregation in neurodegenerative disease. Annu Rev Biomed Eng 4:155-174.
36. Nayak A, Dutta AK, Belfort G. 2008. Surface-enhanced nucleation of insulin amyloid fibrillation. Biochem Biophys Res Commun 369(2): 303-307.
37. Nayak A, Sorci M, Krueger S, Belfort G. 2009. A universal pathway for amyloid nucleus and precursor formation for insulin. Proteins 74(3): 556-565.
38. Nicol D, Smith L. 1960. The amino acid sequence of human insulin. Nature 181:483-485.
39. Nielsen L, Frokjaer S, Brange J, Uversky VN, Fink AL. 2001a. Probing the mechanism of insulin fibril formation with insulin mutants. Biochemistry 40(28): 8397-8409.
40. Nielsen L, Khurana R, Coats A, Frokjaer S, Brange J, Vyas S, Uversky VN, Fink AL. 2001b. Effect of environmental factors on the kinetics of insulin fibril formation: Elucidation of the molecular mechanism. Biochemistry 40(20): 6036-6046.
41. Nozaki Y. 1972. The preparation of guanidine hydrochloride. Methods Enzymol 26 PtC:43-50.
42. Pace CN. 1986. Determination and analysis of urea and guanidine hydrochloride denaturation curves. Methods Enzymol 131:266-280.
43. Pekar AH, Frank BH. 1972. Conformation of proinsulin. A comparison of insulin and proinsulin self-association at neutral pH. Biochemistry 11(22): 4013-4016.
44. Pocker Y, Biswas SB. 1981. Self-association of insulin and the role of hydrophobic bonding: A thermodynamic model of insulin dimerization. Biochemistry 20(15): 4354-4361.
45. Provencher SW. 1979. Inverse problems in polymer characterization: Direct analysis of polydispersity with photon correlation spectroscopy. Die Makromol Chem 180:201.
46. Santoro MM, Bolen DW. 1988. Unfolding free energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethanesulfonyl alpha-chymotrypsin using different denaturants. Biochemistry 27(21): 8063-8068.
47. Sluzky V, Tamada JA, Klibanov AM, Langer R. 1991. Kinetics of insulin aggregation in aqueous solutions upon agitation in the presence of hydrophobic surfaces. Proc Natl Acad Sci USA 88(21): 9377-9381.
48. Sluzky V, Klibanov AM, Langer R. 1992. Mechanism of insulin aggregation and stabilization in agitated aqueous solutions. Biotechnol Bioeng 40(8): 895-903.
49. Sreerama N, Woody RW. 2000. Estimation of protein secondary structure from circular dichroism spectra: Comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set. Anal Biochem 287(2): 252-260.
50. Strickland EH. 1974. Aromatic contributions to circular dichroism spectra of proteins. CRC Crit Rev Biochem 2(1): 113-175.
51. Tanford C. 1961. Physical chemistry of macromolecules. New York: Wiler.
52. Teuscher A. 2007. Insulin: A voice for choice. Basel: Karger.
53. Theisen A, Johann C, Deacon MP, Harding SE. 2000. Refractive increment databook. Nottingham, UK: Nottingham University Press.
54. Waugh D. 1946. A fibrous modification of insulin. I. The heat precipitate of insulin. J Am Chem Soc 68(2): 247-250.
55. Waugh D. 1957. Mechanism for the formation of fibrils from protein molecules. J Cell Comp Physiol 49.
56. Whitmore L, Wallace BA. 2004. DICHROWEB, an online server for protein secondary structure analyses from circular dichroism spectroscopic data. Nucleic Acids Res 32(Web Server issue): W668-W673.
57. Whitmore L, Wallace BA. 2008. Protein secondary structure analyses from circular dichroism spectroscopy: Methods and reference databases. Biopolymers 89(5): 392-400.
58. Whittingham JL, Scott DJ, Chance K, Wilson A, Finch J, Brange J, Guy Dodson G. 2002. Insulin at pH2: Structural analysis of the conditions promoting insulin fibre formation. J Mol Biol 318(2): 479-490.
59. World-Health-Organization. 2008. Diabetes.
60. Worn A, Pluckthun A. 1998. Mutual stabilization of VL and VH in single-chain antibody fragments, investigated with mutants engineered for stability. Biochemistry 37(38): 13120-13127.