Mutational analysis of the ability of resveratrol to inhibit amyloid formation by islet amyloid polypeptide: Critical evaluation of the importance of aromatic-inhibitor and histidine-inhibitor interactions

Biochemistry

Volumn 54, Issue 3, 2015, Pages 666-676

  Tu, Ling Hsien ^a   Young, Lydia M ^b   Wong, Amy G ^a   Ashcroft, Alison E ^b   Radford, Sheena E ^b   Raleigh, Daniel P ^a  

^a STONY BROOK UNIVERSITY   (United States)

^b UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; AROMATIC COMPOUNDS; CELL DEATH; MASS SPECTROMETRY; NEURODEGENERATIVE DISEASES; RESVERATROL; TRANSMISSION ELECTRON MICROSCOPY;

ALZHEIMER'S DISEASE; AROMATIC INHIBITORS; CRITICAL EVALUATION; FLUORESCENCE ASSAY; ISLET AMYLOID POLYPEPTIDES; MECHANISM OF ACTION; MUTATIONAL ANALYSIS; TRUNCATION MUTANTS;

GLYCOPROTEINS;

AMYLIN; AMYLOID; ARGININE; EPIGALLOCATECHIN GALLATE; HISTIDINE; LEUCINE; LYSINE; PHENYLALANINE; RESVERATROL; THIOFLAVINE; TYROSINE; AROMATIC AMINO ACID; CATECHIN; MUTANT PROTEIN; STILBENE DERIVATIVE; THIAZOLE DERIVATIVE;

ARTICLE; CONTROLLED STUDY; DRUG PROTEIN BINDING; ELECTROSPRAY MASS SPECTROMETRY; FLUORESCENCE ANALYSIS; MASS SPECTROMETRY; MUTATIONAL ANALYSIS; PEPTIDE SYNTHESIS; PRIORITY JOURNAL; TRANSMISSION ELECTRON MICROSCOPY; AMINO ACID SEQUENCE; ANALOGS AND DERIVATIVES; CHEMISTRY; DNA MUTATIONAL ANALYSIS; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; STRUCTURE ACTIVITY RELATION; ULTRASTRUCTURE;

AMINO ACID SEQUENCE; AMINO ACIDS, AROMATIC; AMYLOID; ARGININE; CATECHIN; DNA MUTATIONAL ANALYSIS; HISTIDINE; HUMANS; ISLET AMYLOID POLYPEPTIDE; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; STILBENES; STRUCTURE-ACTIVITY RELATIONSHIP; THIAZOLES;

EID: 84921836834     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi501016r     Document Type: Article

References (44)

1. Kahn, S. E., Andrikopoulos, S., and Verchere, C. B. (1999) Islet amyloid: A long-recognized but underappreciated pathological feature of type 2 diabetes Diabetes 48, 241-253
2. Hull, R. L., Westermark, G. T., Westermark, P., and Kahn, S. E. (2004) Islet amyloid: A critical entity in the pathogenesis of type 2 diabetes J. Clin. Endocrinol. Metab. 89, 3629-3643
3. Konarkowska, B., Aitken, J. F., Kistler, J., Zhang, S. P., and Cooper, G. J. S. (2006) The aggregation potential of human amylin determines its cytotoxicity towards islet beta-cells FEBS J. 273, 3614-3624
4. Cheng, F. and Marzban, L. (2007) Cytotoxic effects of human islet amyloid polypeptide on primary islet α-cells and β-cells: Implications for understanding the pathogenesis of type 2 diabetes Diabetes 56, A410-A411
5. Haataja, L., Gurlo, T., Huang, C. J., and Butler, P. C. (2008) Islet amyloid in type 2 diabetes, and the toxic oligomer hypothesis Endocrinol. Rev. 29, 303-316
6. Westermark, P., Andersson, A., and Westermark, G. T. (2011) Islet amyloid polypeptide, islet amyloid, and diabetes mellitus Physiol. Rev. 91, 795-826
7. Westermark, G. T., Westermark, P., Nordin, A., Tornelius, E., and Andersson, A. (2003) Formation of amyloid in human pancreatic islets transplanted to the liver and spleen of nude mice Upsala J. Med. Sci. 108, 193-203
8. Westermark, G. T., Westermark, P., Berne, C., Korsgren, O., and Nordic Network for Clinical Islet Transplantation (2008) Widespread amyloid deposition in transplanted human pancreatic islets N. Engl. J. Med. 359, 977-979
9. Potter, K. J., Abedini, A., Marek, P., Klimek, A. M., Butterworth, S., Driscoll, M., Baker, R., Nilsson, M. R., Warnock, G. L., Oberholzer, J., Bertera, S., Trucco, M., Korbutt, G. S., Fraser, P. E., Raleigh, D. P., and Verchere, C. B. (2010) Islet amyloid deposition limits the viability of human islet grafts but not porcine islet grafts Proc. Natl. Acad. Sci. U.S.A. 107, 4305-4310
10. Kahn, S. E., Dalessio, D. A., Schwartz, M. W., Fujimoto, W. Y., Ensinck, J. W., Taborsky, G. J., and Porte, D. (1990) Evidence of cosecretion of islet amyloid polypeptide and insulin by β-cells Diabetes 39, 634-638
11. Young, D. A., Deems, R. O., Deacon, R. W., McIntosh, R. H., and Foley, J. E. (1990) Effects of amylin on glucose-metabolism and glycogenolysis in vivo and in vitro Am. J. Physiol. 259, E457-E461
12. Rezai-Zadeh, K., Arendash, G. W., Hou, H. Y., Fernandez, F., Jensen, M., Runfeldt, M., Shytle, R. D., and Tan, J. (2008) Green tea epigallocatechin-3-gallate (EGCG) reduces β-amyloid mediated cognitive impairment and modulates tau pathology in Alzheimer transgenic mice Brain Res. 1214, 177-187
13. Meng, F. L., Abedini, A., Plesner, A., Verchere, C. B., and Raleigh, D. P. (2010) The flavanol (-)-epigallocatechin 3-gallate inhibits amyloid formation by islet amyloid polypeptide, disaggregates amyloid fibrils, and protects cultured cells against IAPP-induced toxicity Biochemistry 49, 8127-8133
14. Bieschke, J., Russ, J., Friedrich, R. P., Ehrnhoefer, D. E., Wobst, H., Neugebauer, K., and Wanker, E. E. (2010) EGCG remodels mature α-synuclein and amyloid-β fibrils and reduces cellular toxicity Proc. Natl. Acad. Sci. U.S.A. 107, 7710-7715
15. Popovych, N., Brender, J. R., Soong, R., Vivekanandan, S., Hartman, K., Basrur, V., Macdonald, P. M., and Ramamoorthy, A. (2012) Site specific interaction of the polyphenol EGCG with the SEVI amyloid precursor peptide PAP(248-286) J. Phys. Chem. B 116, 3650-3658
16. Cao, P. and Raleigh, D. P. (2012) Analysis of the inhibition and remodeling of islet amyloid polypeptide amyloid fibers by flavanols Biochemistry 51, 2670-2683
17. Young, L. M., Cao, P., Raleigh, D. P., Ashcroft, A. E., and Radford, S. E. (2014) Ion mobility spectrometry-mass spectrometry defines the oligomeric intermediates in amylin amyloid formation and the mode of action of inhibitors J. Am. Chem. Soc. 136, 660-670
18. Palhano, F. L., Lee, J., Grimster, N. P., and Kelly, J. W. (2013) Toward the molecular mechanism(s) by which EGCG treatment remodels mature amyloid fibrils J. Am. Chem. Soc. 135, 7503-7510
19. Ehrnhoefer, D. E., Bieschke, J., Boeddrich, A., Herbst, M., Masino, L., Lurz, R., Engemann, S., Pastore, A., and Wanker, E. E. (2008) EGCG redirects amyloidogenic polypeptides into unstructured, off-pathway oligomers Nat. Struct. Mol. Biol. 15, 558-566
20. Sun, A. Y., Wang, Q., Simonyi, A., and Sun, G. Y. (2010) Resveratrol as a therapeutic agent for neurodegenerative diseases Mol. Neurobiol. 41, 375-383
21. Savaskan, E., Olivieri, G., Meier, F., Seifritz, E., Wirz-Justice, A., and Muller-Spahn, F. (2003) Red wine ingredient resveratrol protects from β-amyloid neurotoxicity Gerontology 49, 380-383
22. Marambaud, P., Zhao, H. T., and Davies, P. (2005) Resveratrol promotes clearance of Alzheimer's disease amyloid-β peptides J. Biol. Chem. 280, 37377-37382
23. Ladiwala, A. R. A., Lin, J. C., Bale, S. S., Marcelino-Cruz, A. M., Bhattacharya, M., Dordick, J. S., and Tessier, P. M. (2010) Resveratrol selectively remodels soluble oligomers and fibrils of amyloid A-β into off-pathway conformers J. Biol. Chem. 285, 24228-24237
24. Mishra, R., Sellin, D., Radovan, D., Gohlke, A., and Winter, R. (2009) Inhibiting islet amyloid polypeptide fibril formation by the red wine compound resveratrol ChemBioChem 10, 445-449
25. Evers, F., Jeworrek, C., Tiemeyer, S., Weise, K., Sellin, D., Paulus, M., Struth, B., Tolan, M., and Winter, R. (2009) Elucidating the mechanism of lipid membrane-induced IAPP fibrillogenesis and its inhibition by the red wine compound resveratrol: A synchrotron X-ray reflectivity study J. Am. Chem. Soc. 131, 9516-9521
26. Radovan, D., Opitz, N., and Winter, R. (2009) Fluorescence microscopy studies on islet amyloid polypeptide fibrillation at heterogeneous and cellular membrane interfaces and its inhibition by resveratrol FEBS Lett. 583, 1439-1445
27. Wei, L., Jiang, P., Xu, W. X., Li, H., Zhang, H., Yan, L. Y., Chan-Park, M. B., Liu, X. W., Tang, K., Mu, Y. G., and Pervushin, K. (2011) The molecular basis of distinct aggregation pathways of islet amyloid polypeptide J. Biol. Chem. 286, 6291-6300
28. Tu, L. H., Serrano, A. L., Zanni, M. T., and Raleigh, D. P. (2014) Mutational analysis of preamyloid intermediates: The role of His-Tyr interactions in islet amyloid formation Biophys. J. 106, 1520-1527
29. Porat, Y., Mazor, Y., Efrat, S., and Gazit, E. (2004) Inhibition of islet amyloid polypeptide fibril formation: A potential role for heteroaromatic interactions Biochemistry 43, 14454-14462
30. Abedini, A. and Raleigh, D. P. (2005) Incorporation of pseudoproline derivatives allows the facile synthesis of human IAPP, a highly amyloidogenic and aggregation-prone polypeptide Org. Lett. 7, 693-696
31. Marek, P., Woys, A. M., Sutton, K., Zanni, M. T., and Raleigh, D. P. (2010) Efficient microwave-assisted synthesis of human islet amyloid polypeptide designed to facilitate the specific incorporation of labeled amino acids Org. Lett. 12, 4848-4851
32. Abedini, A., Singh, G., and Raleigh, D. P. (2006) Recovery and purification of highly aggregation-prone disulfide-containing peptides: Application to islet amyloid polypeptide Anal. Biochem. 351, 181-186
33. Porat, Y., Abramowitz, A., and Gazit, E. (2006) Inhibition of amyloid fibril formation by polyphenols: Structural similarity and aromatic interactions as a common inhibition mechanism Chem. Biol. Drug Des. 67, 27-37
34. Krebs, M. R. H., Bromley, E. H. C., and Donald, A. M. (2005) The binding of thioflavin-T to amyloid fibrils: Localisation and implications J. Struct. Biol. 149, 30-37
35. Marek, P., Mukherjee, S., Zanni, M. T., and Raleigh, D. P. (2010) 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 J. Mol. Biol. 400, 878-888
36. Hudson, S. A., Ecroyd, H., Kee, T. W., and Carver, J. A. (2009) The thioflavin T fluorescence assay for amyloid fibril detection can be biased by the presence of exogenous compounds FEBS J. 276, 5960-5972
37. Meng, F. L., Marek, P., Potter, K. J., Verchere, C. B., and Raleigh, D. P. (2008) Rifampicin does not prevent amyloid fibril formation by human islet amyloid polypeptide but does inhibit fibril thioflavin-T interactions: Implications for mechanistic studies β-cell death Biochemistry 47, 6016-6024
38. Marek, P., Abedini, A., Song, B. B., Kanungo, M., Johnson, M. E., Gupta, R., Zaman, W., Wong, S. S., and Raleigh, D. P. (2007) 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 46, 3255-3261
39. Tu, L. H. and Raleigh, D. P. (2013) Role of aromatic interactions in amyloid formation by islet amyloid polypeptide Biochemistry 52, 333-342
40. Noor, H., Cao, P., and Raleigh, D. P. (2012) Morin hydrate inhibits amyloid formation by islet amyloid polypeptide and disaggregates amyloid fibers Protein Sci. 21, 373-382
41. Trela, B. C. and Waterhouse, A. L. (1996) Resveratrol: Isomeric molar absorptivities and stability J. Agric. Food Chem. 44 (5) 1253-1257
42. Pineda-Sanabria, S. E., Robertson, I. M., and Sykes, B. D. (2011) Structure of trans-Resveratrol in Complex with the Cardiac Regulatory Protein Troponin C Biochemistry 50 (8) 1309-1320
43. Luca, S., Yau, W.-M., Leapman, R., and Tycko, R. (2007) Peptide conformation and supramolecular organization in amylin fibrils: Constraints from solid-state NMR Biochemistry 46 (47) 13505-13522
44. Wiltzius, J. J. W., Sievers, S. A., Sawaya, M. R., Cascio, D., Popov, D., and Riekel, C. 2008, Atomic structure of the cross-β spine of islet amyloid polypeptide (amylin) Protein Sci. 17 (9) 1467-1474