Tyrosine autofluorescence as a measure of bovine insulin fibrillation

Biophysical Journal

Volumn 97, Issue 9, 2009, Pages 2521-2531

  Bekard, Innocent B ^a   Dunstan, Dave E ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

INSULIN; THIOFLAVINE; TYROSINE;

AMINO ACID SEQUENCE; ARTICLE; AUTOFLUORESCENCE IMAGING; CONTROLLED STUDY; COW; KINETICS; LIGHT SCATTERING; NONHUMAN; PROTEIN AGGREGATION; TEMPERATURE MEASUREMENT;

BOVINAE;

EID: 72249104137     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2009.07.064     Document Type: Article

References (58)

1. Dobson, C. M. 2003. Protein folding and misfolding. Nature. 426:884-890.
2. Agorogiannis, E. I., G. I. Agorogiannis, A. Papadimitriou, and G. M. Hadjigeorgiou. 2004. Protein misfolding in neurodegenerative diseases. Neuropathol. Appl. Neurobiol. 30:215-224.
3. Stefani, M., and C. M. Dobson. 2003. Protein aggregation and aggregate toxicity: new insights into protein folding, misfolding diseases and biological evolution. J. Mol. Med. 81:678-699.
4. Brange, J. 1987. Galenics of Insulin: The Physico-Chemical and Pharmaceutical Aspects of Insulin and Insulin Preparations. Springer- Verlag, Berlin/Heidelberg.
5. Brange, J., and L. Langkjaer. 1993. Insulin structure and stability. In Stability and Characterization of Protein and Peptide Drugs: Case Histories. Y. J. Wang and R. Pearlman, editors. Springer, New York. 315-350.
6. Whittingham, J. L., D. J. Scott, K. Chance, A. Wilson, J. Finch, et al. 2002. Insulin at pH 2: structural analysis of the conditions promoting insulin fibre formation. J. Mol. Biol. 318:479-490.
7. Betz, S. F. 1993. Disulfide bonds and the stability of globular proteins. Protein Sci. 2:1551-1558.
8. Lee, C. C., A. Nayak, A. Sethuraman, G. Belfort, and G. J. McRae. 2007. A three-stage kinetic model of amyloid fibrillation. Biophys. J. 92:3448-3458.
9. Baker, E. N., T. L. Blundell, J. F. Cutfield, S. M. Cutfield, E. J. Dodson, et al. 1988. The structure of 2Zn pig insulin crystals at 1.5 A resolution. Philos. Trans. R. Soc. Lond. B Biol. Sci. 319:369-456.
10. Kline, A. D., and R. M. Justice, Jr. 1990. Complete sequence-specific proton NMR assignments for human insulin. Biochemistry. 29:2906-2913.
11. Hua, Q. X., S. E. Shoelson, M. Kochoyan, and M. A. Weiss. 1991. Receptor binding redefined by a structural switch in a mutant human insulin. Nature. 354:238-241. (Pubitemid 21896824)
12. Derewenda, U., Z. Derewenda, E. J. Dodson, G. G. Dodson, C. D. Reynolds, et al. 1989. Phenol stabilizes more helix in a new symmetrical zinc insulin hexamer. Nature. 338:594-596.
13. Uversky, V. N., L. N. Garriques, I. S. Millett, S. Frokjaer, J. Brange, et al. 2003. Prediction of the association state of insulin using spectral parameters. J. Pharm. Sci. 92:847-858.
14. Bryant, C., D. B. Spencer, A. Miller, D. L. Bakaysa, K. S. McCune, et al. 1993. Acid stabilization of insulin. Biochemistry. 32:8075-8082.
15. Pillai, O., and R. Panchagnula. 2001. Insulin therapies-past, present and future. Drug Discov. Today. 6:1056-1061.
16. Sluzky, V., J. A. Tamada, A. M. Klibanov, and R. Langer. 1991. Kinetics of insulin aggregation in aqueous solutions upon agitation in the presence of hydrophobic surfaces. Proc. Natl. Acad. Sci. USA. 88:9377-9381.
17. Nielsen, L., R. Khurana, A. Coats, S. Frokjaer, J. Brange, et al. 2001. Effect of environmental factors on the kinetics of insulin fibril formation: elucidation of the molecular mechanism. Biochemistry. 40:6036-6046.
18. Brange, J., L. Andersen, E. D. Laursen, G. Meyn, and E. Rasmussen. 1997. Toward understanding insulin fibrillation. J. Pharm. Sci. 86:517-525.
19. Ehrlich, J. C., and I. M. Ratner. 1961. Amyloidosis of the islets of Langerhans: a restudy of islet hyalin in diabetic and nondiabetic individuals. Am. J. Pathol. 38:49-59.
20. Dobson, C. M. 2004. Principles of protein folding, misfolding and aggregation. Semin. Cell Dev. Biol. 15:3-16.
21. Meredith, S. C. 2005. Protein denaturation and aggregation: cellular responses to denatured and aggregated proteins. Ann. N.Y. Acad. Sci. 1066:181-221.
22. Mauro, M., E. F. Craparo, A. Podestà, D. Bulone, R. Carrotta, et al. 2007. Kinetics of different processes in human insulin amyloid formation. J. Mol. Biol. 366:258-274.
23. Ahmad, A., V. N. Uversky, D.Hong, and A. L. Fink. 2005. Early events in the fibrillation of monomeric insulin. J. Biol. Chem. 280:42669-42675.
24. Levine, 3rd, H. 1999. Quantification of b-sheet amyloid fibril structures with thioflavin T. Methods Enzymol. 309:274-284.
25. Groenning, M., L. Olsen, M. van de Weert, J. M. Flink, S. Frokjaer, et al. 2007. Study on the binding of Thioflavin T to β-sheet-rich and non-b-sheet cavities. J. Struct. Biol. 158:358-369.
26. Permyakov, E. A., V. V. Yarmolenko, E. A. Burstein, and C. Gerday. 1982. Intrinsic fluorescence spectra of a tryptophan-containing parvalbumin as a function of thermal, pH and urea denaturation. Biophys. Chem. 15:19-26.
27. Arutyunyan, A. G., K. M. L'Vov, A. O. Mnatsakanyan, V. A. Oganesyan, and N. V. Shakhnazaryan. 1985. Light quenching of fluorescence of aromatic amino acids. J. Appl. Spectrosc. 43:992-994.
28. Teale, F. W. J. 1960. The ultraviolet fluorescence of proteins in neutral solution. Biochem. J. 76:381-388.
29. Bushueva, T. L., E. P. Busel, and E. A. Burstein. 1978. Relationship of thermal quenching of protein fluorescence to intramolecular structural mobility. Biochim. Biophys. Acta. 534:141-152.
30. Ahmad, A., I. S. Millett, S. Doniach, V. N. Uversky, and A. L. Fink. 2003. Partially folded intermediates in insulin fibrillation. Biochemistry. 42:11404-11416. (Pubitemid 37205734)
31. Permyakov, E. A., editor. 1992. Luminiscent Spectroscopy of Proteins. CRC Press, London.
32. Strickland, E. H., and D. Mercola. 1976. Near-ultraviolet tyrosyl circular dichroism of pig insulin monomers, dimers, and hexamers. Dipole-dipole coupling calculations in the monopole approximation. Biochemistry. 15:3875-3884.
33. Nettleton, E. J., P. Tito, M. Sunde, M. Bouchard, C. M. Dobson, et al. 2000. Characterization of the oligomeric states of insulin in self-assembly and amyloid fibril formation by mass spectrometry. Biophys. J. 79:1053-1065.
34. Manno, M., E. F. Craparo, V. Martorana, D. Bulone, and P. L. San Biagio. 2006. Kinetics of insulin aggregation: disentanglement of amyloid fibrillation from large-size cluster formation. Biophys. J. 90:4585-4591. (Pubitemid 43830902)
35. Burstein, E. A., editor. 1977. Intrinsic Protein Luminescence (Origins and Applications). VINITI, Moscow.
36. Podesta, A., G. Tiana, P. Milani, and M. Manno. 2006. Early events in insulin fibrillization studied by time-lapse atomic force microscopy. Biophys. J. 90:589-597.
37. Rayner, D. M., D. T. Krajcarski, and A. G. Szabo. 1978. Excited state acid-base equilibrium of tyrosine. Can. J. Chem. 56:1238-1245.
38. Waugh, D. F. 1946. A fibrous modification of insulin. I. The heat precipitate of insulin. J. Am. Chem. Soc. 68:247-250.
39. Dusa, A., J. Kaylor, S. Edridge, N. Bodner, D. P. Hong, et al. 2006. Characterization of oligomers during synuclein aggregation using intrinsic tryptophan fluorescence. Biochemistry. 45:2752-2760. (Pubitemid 43297333)
40. Whitmore, L., and B. A. Wallace. 2007. Protein secondary structure analyses from circular dichroism spectroscopy: Methods and reference databases. Biopolymers. 89:392-400.
41. Brems, D. N., P. L. Brown, L. A. Heckenlaible, and B. H. Frank. 1990. Equilibrium denaturation of insulin and proinsulin. Biochemistry. 29:9289-9293.
42. r = 9000), a protein with a single tyrosine residue. Biochem. J. 207:389-396.
43. Huus, K., S. Havelund, H. B. Olsen, M. van de Weert, and S. Frokjaer. 2005. Thermal dissociation and unfolding of insulin. Biochemistry. 44:11171-11177.
44. Dzwolak, W., R. Ravindra, J. Lendermann, and R. Winter. 2003. Aggregation of bovine insulin probed by DSC/PPC calorimetry and FTIR spectroscopy. Biochemistry. 42:11347-11355. (Pubitemid 37158902)
45. Kelly, S. M., and N. C. Price. 1997. The application of circular dichroism to studies of protein folding and unfolding. Biochim. Biophys Acta. 1338:161-185.
46. Sreerama, N., M. C. Manning, M. E. Powers, J. X. Zhang, D. P. Goldenberg, et al. 1999. Tyrosine, phenylalanine, and disulfide contributions to the circular dichroism of proteins: circular dichroism spectra of wild-type and mutant bovine pancreatic trypsin inhibitor. Biochemistry. 38:10814-10822.
47. Groenning, M., M. Norrman, J. M. Flink, M. van de Weert, J. T. Bukrinsky, et al. 2007. Binding mode of Thioflavin T in insulin amyloid fibrils. J. Struct. Biol. 159:483-497.
48. Murali, J., and R. Jayakumar. 2005. Spectroscopic studies on native and protofibrillar insulin. J. Struct. Biol. 150:180-189.
49. Cowgill, R. W. 1976. Tyrosyl fluorescence in proteins and model peptides. In Biochemical Fluorescence: Concepts 2. R. F. Chen and H. Edelhoch, editors. Marcel Dekker, New York. 441-486.
50. Karreman, G., R. H. Steele, and A. Szent-Gyorgyi. 1958. On resonance transfer of excitation energy between aromatic amino acids in proteins. Proc. Natl. Acad. Sci. USA. 44:140-143.
51. Weber, G. 1960. Fluorescence-polarization spectrum and electronic-energy transfer in tyrosine, tryptophan and related compounds. Biochem. J. 75:335-345.
52. Steiner, R. F. 1984. Location of a binding site for 1-anilinonaphthalene- 8-sulfonate on calmodulin. Arch. Biochem. Biophys. 228:105-112.
53. Saunders, A. J., G. B. Young, and G. J. Pielak. 1993. Polarity of disul- fide bonds. Protein Sci. 2:1183-1184.
54. Radzicka, A., and R. Wolfenden. 1988. Comparing the polarities of the amino acids: side-chain distribution coefficients between the vapor phase, cyclohexane, 1-octanol, and neutral aqueous solution. Biochemistry. 27:1664-1670.
55. Qiao, Z. S., Z. Y. Guo, and Y. M. Feng. 2001. Putative disulfide-forming pathway of porcine insulin precursor during its refolding in vitro. Biochemistry. 40:2662-2668.
56. Eftink, M. R., and C. A. Ghiron. 1975. Dynamics of a protein matrix revealed by fluorescence quenching. Proc. Natl. Acad. Sci. USA. 72:3290-3294.
57. Longworth, J. W. 1971. Luminescence of polypeptides and proteins. In Excited States of Proteins and Nucleic Acids. R. F. Steiner and I. Weinryb, editors. Plenum Press, New York. 319-483.
58. Havel, A. H., editor. 1996. Spectroscopic Methods for Determining Protein Structure in Solution. VCH Publishers, New York.