Residue-specific, real-time characterization of lag-phase species and fibril growth during amyloid formation: A combined fluorescence and IR study of p-cyanophenylalanine analogs of islet amyloid polypeptide

Journal of Molecular Biology

Volumn 400, Issue 4, 2010, Pages 878-888

  Marek, Peter ^a   Mukherjee, Sudipta ^b   Zanni, Martin T ^b   Raleigh, Daniel P ^a  

^a STONY BROOK UNIVERSITY   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Amylin; Amyloid; IAPP; Lag phase; P cyanophenylalanine

Indexed keywords

4 CYANOPHENYLALANINE; AMYLOID; PHENYLALANINE; POLYPEPTIDE; THIOFLAVINE; TYROSINE; UNCLASSIFIED DRUG;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ELECTRON MICROSCOPY; FIBER; FLUORESCENCE ANALYSIS; INFRARED RADIATION; INFRARED SPECTROSCOPY; PRIORITY JOURNAL; SEQUENCE ANALYSIS; STRUCTURE ANALYSIS; SUBSTITUTION REACTION;

EID: 77954384842     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2010.05.041     Document Type: Article

References (58)

1. Glenner G.G. Amyloid deposits and amyloidosis; the β-fibrilloses. N. Engl. J. Med. 1980, 302:1283-1292.
2. Sipe J.D., Cohen A.S. Amyloidosis. Crit. Rev. Clin. Lab. Sci. 1994, 31:325-354.
3. Selkoe D.J. Cell biology of protein misfolding: the examples of Alzheimer's and Parkinson's diseases. Nat. Cell Biol. 2004, 6:1054-1061.
4. Chiti F., Dobson C.M. Protein misfolding, functional amyloid and human disease. Annu. Rev. Biochem. 2006, 75:333-366.
5. Dobson C.M. Protein misfolding, evolution and disease. Trends Biochem. Sci. 1999, 24:329-332.
6. Nilsberth C., Westlind-Danielsson A., Eckman C.B., Condron M.M., Axelman K., Forsell C., et al. The 'Arctic' APP mutation (E693G) causes Alzheimer's disease by enhanced A-beta protofibril formation. Nat. Neurosci. 2001, 4:887-893.
7. Marina K.D., Bitan G., Teplow D.B. Paradigm shifts in Alzheimer's disease and other neurodegenerative disorders: the emerging role of oligomeric assemblies. Neurosci. Res. 2002, 69:567-577.
8. Caughey C., Lansbury P.T. Protofibrils, pores, fibrils, and neurodegeneration: separating the responsible protein aggregates from the innocent bystanders. Annu. Rev. Neurosci. 2003, 26:267-298.
9. Petkova A.T., Leapman R.D., Guo Z., Yau W.-M., Mattson M.P., Tycko R. Self-propagating, molecular-level polymorphism in Alzheimer's β-amyloid fibrils. Science 2005, 307:262-265.
10. Nilsson M.R., Driscoll M.D., Raleigh D.P. Low levels of asparagine deamidation have a dramatic effect on aggregation: implications for the study of amyloid formation. Protein Sci. 2002, 11:342-349.
11. Abedini A., Raleigh D. A critical assessment of the role of helical intermediates in amyloid formation by natively unfolded proteins and polypeptides. Protein Eng. Des. Sel. 2009, 22:453-459.
12. Chang E.S.-H., Liao T.-Y., Lim T.-S., Fann W., Chen R.P.-Y. A new amyloid-like β-aggregate with amyloid characteristics, except fibril morphology. J. Mol. Biol. 2009, 385:1257-1265.
13. Shim S.-H., Gupta R., Ling Y.L., Strasfeld D.B., Raleigh D.P., Zanni M.T. Two-dimensional IR spectroscopy and isotope labeling defines the pathway of amyloid formation with residue-specific resolution. Proc. Natl Acad. Sci. USA 2009, 106:6614-6619.
14. Krebs M.R.H., Bromley E.H.C., Donald A.M. The binding of thioflavin-T to amyloid fibrils: localisation and implications. J. Struct. Biol. 2005, 149:30-37.
15. Levine H. Quantification of beta-sheet amyloid fibril structures with thioflavin T. Methods Enzymol. 1999, 309:274-284.
16. Biancalana M., Makabe K., Koide A., Koide S. Molecular mechanism of thioflavin-T binding to the surface of β-rich-peptide self-assemblies. J. Mol. Biol. 2009, 385:1052-1063.
17. Groenning M., Olsen L., van de Weert M., Flink J.M., Frokjaer S., Jørgensen F.S. Study on the binding of thioflavin-T to β-sheet-rich and non-β-sheet cavities. J. Struct. Biol. 2007, 158:358-369.
18. Meng F., Marek P., Potter K., Verchere B., Raleigh D.P. Rifampicin does not prevent amyloid fibril formation by human islet amyloid polypeptide but does inhibit fibril thioflavin-T interactions: implications for mechanistic studies of β-cell death. Biochemistry 2008, 47:6016-6024.
19. Tomiyama T., Kaneko H., Kataoka K.-i., Asano S., Endo N. Rifampicin inhibits the toxicity of pre-aggregated amyloid peptides by binding to peptide fibrils and preventing amyloid-cell interaction. Biochem. J. 1997, 322:859-865.
20. Marek P., Gupta R., Raleigh D. The fluorescent amino acid p-cyanophenylalanine provides an intrinsic probe of amyloid formation. ChemBioChem 2008, 9:1372-1374.
21. Aprilakis K.N., Taskent H., Raleigh D.P. Use of the novel fluorescent amino acid p-cyanophenylalanine offers a direct probe of hydrophobic core formation during the folding of the N-terminal domain of the ribosomal protein L9 and provides evidence for two-state folding. Biochemistry 2007, 46:12308-12313.
22. Schultz K.C., Supekova L., Ryu Y., Xie J., Perera R., Schultz P.G. A genetically encoded infrared probe. J. Am. Chem. Soc. 2006, 128:13984-13985.
23. Tucker M.J., Oyola R., Gai F. A novel fluorescent probe for protein binding and folding studies: p-cyanophenylalanine. Bioploymers 2006, 83:571-576.
24. Serrano A.L., Troxler T., Tucker M.J., Gai F. Photophysics of a fluorescent non-natural amino acid: p-cyanophenylalanine. Chem. Phys. Lett. 2010, 487:303-306.
25. Tang J., Signarvic R.S., DeGrado W.F., Gai F. Role of helix nucleation in the kinetics of binding of mastoparan X to phospholipid bilayer. Biochemistry 2007, 46:13856-13863.
26. Tucker M.J., Tang J., Gai F. Probing the kinetics of membrane-mediated helix folding. J. Phys. Chem. B 2006, 110:8105-8109.
27. Rogers J.M., Lippert L.G., Gai F. Non-natural amino acid fluorophores for one- and two-step fluorescence resonance energy transfer applications. Anal. Biochem. 2010, 399:182-189.
28. Tucker M.J., Oyola R., Gai F. Conformational distribution of a 14-residue peptide in solution: a fluorescence resonance energy transfer study. J. Phys. Chem. B 2005, 109:4788-4795.
29. Taskent-Sezgin H., Chung J., Patsalo V., Miyake-Stoner S.J., Miller A.M., Brewer S.H., et al. Interpretation of p-cyanophenylalanine fluorescence in proteins in terms of solvent exposure and contribution of side-chain quenchers: a combined fluorescence, IR and molecular dynamics study. Biochemistry 2009, 48:9040-9046.
30. Getahun Z., Huang C.Y., Wang T., Leon B.D., DeGrado W.F., Gai F. Using nitrile-derivatized amino acids as infrared probes of local environment. J. Am. Chem. Soc. 2003, 125:405-411.
31. Tucker M.J., Getahun Z., Nanda V., DeGrado W.F., Gai F. A new method for determining the local environment and orientation of individual side chains of membrane-binding peptides. J. Am. Chem. Soc. 2004, 126:5078-5079.
32. Suydam I.T., Boxer S.G. Vibrational stark effects calibrate the sensitivity of vibrational probes for electric fields in proteins. Biochemistry 2003, 42:12050-12055.
33. Dalosto S.D., Vanderkooi J.M., Sharp K.A. Vibrational stark effects on carbonyl, nitrile, and nitrosyl compounds including heme ligands, CO, CN, and NO, studied with density functional theory. J. Phys. Chem. B 2004, 108:6450-6457.
34. Cooper G., Willis A.C., Clark A., Turner R.C., Sim R.B., Reid K.B.M. Purification and characterization of a peptide from amyloid-rich pancreases of type 2 diabetic patients. Proc. Natl Acad. Sci. USA 1987, 84:8628-8632.
35. Westermark P., Wernstedt C., Wilander E., Hayden D.W., O'Brien T.D., Johnson K.H. Amyloid fibrils in human insulinoma and islets of Langerhans of the diabetic cat are derived from a neuropeptide-like protein also present in normal islet cells. Proc. Natl Acad. Sci. USA 1987, 84:3881-3885.
36. Kahn S.E., D'Alessio D.A., Schwartz M.W., Fujimoto W.Y., Ensinck J.W., Taborsky G.J., Porte D. Evidence of cosecretion of islet amyloid polypeptide and insulin by beta-cells. Diabetes 1990, 39:634-638.
37. Kahn S.E., Andrikopoulos S., Verchere C.B. Islet amyloid: a long-recognized but underappreciated pathological feature of type 2 diabetes. Diabetes 1999, 48:241-253.
38. de Koning E.J., Bodkin N.L., Hansen B.C., Clark A. Diabetes mellitus in Macaca mulatta monkeys is characterised by islet amyloidosis and reduction in beta-cell population. Diabetologia 1993, 36:378-384.
39. Butler A.E., Janson J., Bonner-Weir S., Ritzel R., Rizza R.A., Butler P.C. Beta-cell deficit and increased beta-cell apoptosis in humans with type 2 diabetes. Diabetes 2003, 52:102-110.
40. Konarkowska B., Aitken J.F., Kistler J., Zhang S., Cooper G.J. The aggregation potential of human amylin determines its cytotoxicity towards islet beta-cells. FEBS J. 2006, 273:3614-3624.
41. Guardado-Mendoza R., Davalli A.M., Chavez A.O., Hubbard G.B., Dick E.J., Majluf-Cruz A., et al. Pancreatic islet amyloidosis, beta-cell apoptosis, and alpha-cell proliferation are determinants of islet remodeling in type-2 diabetic baboons. Proc. Natl. Acad. Sci. USA 2009, 106:13992-13997.
42. Udayasankar J., Kodama K., Hull R.L., Zraika S., Aston-Mourney K., Subramanian S.L., et al. Amyloid formation results in recurrence of hyperglycaemia following transplantation of human IAPP transgenic mouse islets. Diabetologia 2009, 52:143-153.
43. Westermark G.T., Westermark P., Berne C., Korsgren O. Widespread amyloid deposition in transplanted human pancreatic islets. N. Engl. J. Med. 2008, 359:977-979.
44. Westermark P., Eizirik D.L., Pipeleers D.G., Hellerström C., Andersson A. Rapid deposition of amyloid in human islets transplanted into nude mice. Diabetologia 1995, 38:543-549.
45. Potter K., Abedini A., Marek P., Butterworth S., Driscoll M., Baker R., et al. Islet amyloid deposition limits the viability of human islet grafts but not porcine islet grafts. Proc. Natl Acad. Sci. 2010, 107:4305-4310.
46. Padrick S.B., Miranker A.D. Islet amyloid polypeptide: identification of long-range contacts and local order on the fibrillogenesis pathway. J. Mol. Biol. 2001, 308:783-794.
47. Goldsbury C., Goldie K., Pellaud J., Seelig J., Frey P., Muller S.A., et al. Amyloid fibril formation from full-length and fragments of amylin. J. Struct. Biol. 2000, 130:352-362.
48. Wiltzius J.J.W., Sievers S.A., Sawaya M.R., Eisenberg D. Atomic structures of IAPP (amylin) fusions suggest a mechanism for fibrillation and the role of insulin in the process. Protein Sci. 2009, 18:1521-1530.
49. Marek P., Abedini A., Song B., Kanungo M., Johnson M.E., Gupta R., et al. Aromatic interactions are not required for amyloid fibril formation by islet amyloid polypeptide but do influence the rate of fibril formation and fibril morphology. Biochemistry 2007, 46:3255-3261.
50. Koo B.W., Hebda J.A., Miranker A.D. Amide inequivalence in the fibrillar assembly of islet amyloid polypeptide. Protein Eng. Des. Sel. 2008, 21:147-154.
51. Abedini A., Raleigh D. The role of His-18 in amyloid formation by human islet amyloid polypeptide. Biochemistry 2005, 44:16284-16291.
52. Luca S., Yau W.M., Leapman R., Tycko R. Peptide conformation and supramolecular organization in amylin fibrils: constraints from solid-state NMR. Biochemistry 2007, 48:13505-13522.
53. Williamson J.A., Loria J.P., Miranker A.D. Helix stabilization precedes aqueous and bilayer-catalyzed fiber formation in islet amyloid polypeptide. J. Mol. Biol. 2009, 393:386-396.
54. Soong R., Brender J.R., Macdonald P.M., Ramamoorthy A. Association of highly compact type II diabetes related islet amyloid polypeptide intermediate species at physiological temperature revealed by diffusion NMR spectroscopy. J. Am. Chem. Soc. 2009, 131:7079-7085.
55. Vaiana S.M., Best R.B., Yau W.-M., Eaton W.A., Hofrichter J. Evidence for a partially structured state of the amylin monomer. Biophys. J. 2009, 97:2948-2957.
56. Abedini A., Raleigh D.P. Incorporation of pseudoproline derivatives allows the facile synthesis of human IAPP: a highly amyloidogenic and aggregation-prone polypeptide. Org. Lett. 2005, 7:693-696.
57. Abedini A., Singh G., Raleigh D.P. Recovery and purification of highly aggregation-prone disulfide-containing peptides: application to islet amyloid polypeptide. Anal. Biochem. 2005, 351:181-186.
58. Nilsson M., Raleigh D.P. Analysis of amylin cleavage products provides new insights into the amyloidogenic region of human amylin. J. Mol. Biol. 1999, 294:1375-1385.