Stabilizing Off-pathway Oligomers by Polyphenol Nanoassemblies for IAPP Aggregation Inhibition

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Nedumpully Govindan, Praveen ^a   Kakinen, Aleksandr ^b   Pilkington, Emily H ^b   Davis, Thomas P ^b,c   Chun Ke, Pu ^b   Ding, Feng ^a  

^a CLEMSON UNIVERSITY   (United States)

^b MONASH UNIVERSITY   (Australia)

^c UNIVERSITY OF WARWICK   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLSALICYLIC ACID; AMYLIN; CURCUMIN; NANOMATERIAL; POLYPHENOL; PROTEIN AGGREGATE; PROTEIN BINDING; RESVERATROL; STILBENE DERIVATIVE;

CHEMICAL PHENOMENA; CHEMISTRY; CONFORMATION; DRUG EFFECTS; METABOLISM; MOLECULAR MODEL; PROTEIN AGGREGATION, PATHOLOGICAL;

ASPIRIN; CURCUMIN; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; ISLET AMYLOID POLYPEPTIDE; MODELS, MOLECULAR; MOLECULAR CONFORMATION; NANOSTRUCTURES; POLYPHENOLS; PROTEIN AGGREGATES; PROTEIN AGGREGATION, PATHOLOGICAL; PROTEIN BINDING; STILBENES;

EID: 84954105795     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep19463     Document Type: Article

References (66)

1. Glabe, C. G. Common mechanisms of amyloid oligomer pathogenesis in degenerative disease. Neurobiol. Aging 27, 570-575 (2006).
2. Kayed, R. et al. Conformational transitions of islet amyloid polypeptide (IAPP) in amyloid formation in Vitro 1. J. Mol. Biol. 287, 781-796 (1999).
3. Macdonald, I. A. Amylin and the gastrointestinal tract. Diabet. Med. J. Br. Diabet. Assoc. 14 Suppl 2, S24-28 (1997).
4. Young, D. A., Deems, R. O., Deacon, R. W., McIntosh, R. H. & Foley, J. E. Effects of amylin on glucose metabolism and glycogenolysis in vivo and in vitro. Am. J. Physiol.-Endocrinol. Metab. 259, E457 (1990).
5. Cohen, F. E. & Kelly, J. W. Therapeutic approaches to protein-misfolding diseases. Nature 426, 905-909 (2003).
6. Klabunde, T. et al. Rational design of potent human transthyretin amyloid disease inhibitors. Nat. Struct. Biol. 7, 312-321 (2000).
7. Ray, S. S., Nowak, R. J., Brown, R. H. & Lansbury, P. T. Small-molecule-mediated stabilization of familial amyotrophic lateral sclerosis-linked superoxide dismutase mutants against unfolding and aggregation. Proc. Natl. Acad. Sci. USA 102, 3639-3644 (2005).
8. Nowak, R. J., Cuny, G. D., Choi, S., Lansbury, P. T. & Ray, S. S. Improving binding specificity of pharmacological chaperones that target mutant superoxide dismutase-1 linked to familial amyotrophic lateral sclerosis using computational methods. J. Med. Chem. 53, 2709-2718 (2010).
9. Nedumpully-Govindan, P. & Ding, F. Inhibition of IAPP aggregation by insulin depends on the insulin oligomeric state regulated by zinc ion concentration. Sci. Rep. 5, 8240 (2015).
10. DeMattos, R. B. et al. Peripheral anti-A beta antibody alters CNS and plasma A beta clearance and decreases brain A beta burden in a mouse model of Alzheimer's disease. Proc. Natl. Acad. Sci. USA 98, 8850-8855 (2001).
11. Bieschke, J. et al. Small-molecule conversion of toxic oligomers to nontoxic β-sheet-rich amyloid fibrils. Nat. Chem. Biol. 8, 93-101 (2012).
12. Feng, B. Y. et al. Small-molecule aggregates inhibit amyloid polymerization. Nat. Chem. Biol. 4, 197-199 (2008).
13. Ehrnhoefer, D. E. et al. EGCG redirects amyloidogenic polypeptides into unstructured, off-pathway oligomers. Nat. Struct. Mol. Biol. 15, 558-566 (2008).
14. Sparks, S., Liu, G., Robbins, K. J. & Lazo, N. D. Curcumin modulates the self-assembly of the islet amyloid polypeptide by disassembling α-helix. Biochem. Biophys. Res. Commun. 422, 551-555 (2012).
15. Daval, M. et al. The effect of curcumin on human islet amyloid polypeptide misfolding and toxicity. Amyloid 17, 118-128 (2010).
16. Ladiwala, A. R. A. et al. Resveratrol selectively remodels soluble oligomers and fibrils of amyloid Abeta into off-pathway conformers. J. Biol. Chem. 285, 24228-24237 (2010).
17. Mishra, R., Sellin, D., Radovan, D., Gohlke, A. & Winter, R. Inhibiting Islet Amyloid Polypeptide Fibril Formation by the Red Wine Compound Resveratrol. ChemBioChem 10, 445-449 (2009).
18. Tu, L.-H. et al. 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 (Mosc.) (2014) doi: 10.1021/bi501016r.
19. Meng, F., Abedini, A., Plesner, A., Verchere, C. B. & Raleigh, D. P. The Flavanol (-)-Epigallocatechin 3-Gallate Inhibits Amyloid Formation by Islet Amyloid Polypeptide, Disaggregates Amyloid Fibrils, and Protects Cultured Cells against IAPP-Induced Toxicity. Biochemistry (Mosc.) 49, 8127-8133 (2010).
20. Young, L. M. et al. Screening and classifying small-molecule inhibitors of amyloid formation using ion mobility spectrometry-mass spectrometry. Nat. Chem. 7, 73-81 (2015).
21. Cheng, B. et al. Coffee Components Inhibit Amyloid Formation of Human Islet Amyloid Polypeptide in Vitro: Possible Link between Coffee Consumption and Diabetes Mellitus. J. Agric. Food Chem. 59, 13147-13155 (2011).
22. Mishra, R. et al. Small-Molecule Inhibitors of Islet Amyloid Polypeptide Fibril Formation. Angew. Chem. Int. Ed. 47, 4679-4682 (2008).
23. Cheng, B. et al. Silibinin inhibits the toxic aggregation of human islet amyloid polypeptide. Biochem. Biophys. Res. Commun. 419, 495-499 (2012).
24. Yang, F. et al. Curcumin Inhibits Formation of Amyloid β Oligomers and Fibrils, Binds Plaques, and Reduces Amyloid in Vivo. J. Biol. Chem. 280, 5892-5901 (2005).
25. Savaskan, E. et al. Red Wine Ingredient Resveratrol Protects from β-Amyloid Neurotoxicity. Gerontology 49, 380-383 (2003).
26. Pandey, N., Strider, J., Nolan, W. C., Yan, S. X. & Galvin, J. E. Curcumin inhibits aggregation of α-synuclein. Acta Neuropathol. (Berl.) 115, 479-489 (2008).
27. Caruana, M. et al. Inhibition and disaggregation of α-synuclein oligomers by natural polyphenolic compounds. FEBS Lett. 585, 1113-1120 (2011).
28. Adessi, C. & Soto, C. Converting a peptide into a drug: strategies to improve stability and bioavailability. Curr. Med. Chem. 9, 963-978 (2002).
29. Jiang, P., Li, W., Shea, J.-E. & Mu, Y. Resveratrol Inhibits the Formation of Multiple-Layered β-Sheet Oligomers of the Human Islet Amyloid Polypeptide Segment 22-27. Biophys. J. 100, 1550-1558 (2011).
30. Lolicato, F., Raudino, A., Milardi, D. & La Rosa, C. Resveratrol interferes with the aggregation of membrane-bound human-IAPP: A molecular dynamics study. Eur. J. Med. Chem. 92, 876-881 (2015).
31. Wang, Q., Ning, L., Niu, Y., Liu, H. & Yao, X. Molecular Mechanism of the Inhibition and Remodeling of Human Islet Amyloid Polypeptide (hIAPP1-37) Oligomer by Resveratrol from Molecular Dynamics Simulation. J. Phys. Chem. B 119, 15-24 (2014).
32. Luca, S., Yau, W.-M., Leapman, R. & Tycko, R. Peptide Conformation and Supramolecular Organization in Amylin Fibrils: Constraints from Solid-State NMR. Biochemistry (Mosc.) 46, 13505-13522 (2007).
33. Thomas, T., Nadackal, G. T. & Thomas, K. Aspirin and diabetes: inhibition of amylin aggregation by nonsteroidal anti-inflammatory drugs. Exp. Clin. Endocrinol. Diabetes Off. J. Ger. Soc. Endocrinol. Ger. Diabetes Assoc. 111, 8-11 (2003).
34. Tu, L.-H., Noor, H., Cao, P. & Raleigh, D. P. Aspirin, Diabetes, and Amyloid: Re-examination of the Inhibition of Amyloid Formation by Aspirin and Ketoprofen. ACS Chem. Biol. 9, 1632-1637 (2014).
35. Ding, F., Tsao, D., Nie, H. & Dokholyan, N. V. Ab Initio Folding of Proteins with All-Atom Discrete Molecular Dynamics. Structure 16, 1010-1018 (2008).
36. Shirvanyants, D., Ding, F., Tsao, D., Ramachandran, S. & Dokholyan, N. V. Discrete Molecular Dynamics: An Efficient And Versatile Simulation Method For Fine Protein Characterization. J. Phys. Chem. B 116, 8375-8382 (2012).
37. Khare, S. D., Ding, F. & Dokholyan, N. V. Folding of Cu, Zn Superoxide Dismutase and Familial Amyotrophic Lateral Sclerosis. J. Mol. Biol. 334, 515-525 (2003).
38. Kurien, B. T., Singh, A., Matsumoto, H. & Scofield, R. H. Improving the solubility and pharmacological efficacy of curcumin by heat treatment. Assay Drug Dev. Technol. 5, 567-576 (2007).
39. Santos, A. C., Veiga, F. & Ribeiro, A. J. New delivery systems to improve the bioavailability of resveratrol. Expert Opin. Drug Deliv. 8, 973-990 (2011).
40. Jaikaran, E. T. A. S. & Clark, A. Islet amyloid and type 2 diabetes: from molecular misfolding to islet pathophysiology. Biochim. Biophys. Acta BBA-Mol. Basis Dis. 1537, 179-203 (2001).
41. Tenidis, K. et al. Identification of a penta- and hexapeptide of islet amyloid polypeptide (IAPP) with amyloidogenic and cytotoxic properties. J. Mol. Biol. 295, 1055-1071 (2000).
42. 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. 18, 1521-1530 (2009).
43. Williamson, J. A. & Miranker, A. D. Direct detection of transient α-helical states in islet amyloid polypeptide. Protein Sci. 16, 110-117 (2007).
44. Liu, G. et al. Mechanistic Studies of Peptide Self-Assembly: Transient α-Helices to Stable β-Sheets. J. Am. Chem. Soc. 132, 18223-18232 (2010).
45. Pannuzzo, M., Raudino, A., Milardi, D., La Rosa, C. & Karttunen, M. α-Helical Structures Drive Early Stages of Self-Assembly of Amyloidogenic Amyloid Polypeptide Aggregate Formation in Membranes. Sci. Rep. 3, 2781 (2013).
46. Abedini, A. & Raleigh, D. P. A role for helical intermediates in amyloid formation by natively unfolded polypeptides? Phys. Biol. 6, 015005 (2009).
47. 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. 131, 7079-7085 (2009).
48. Evers, F. et al. 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 (2009).
49. Bitan, G. et al. Amyloid β-protein (Aβ) assembly: Aβ40 and Aβ42 oligomerize through distinct pathways. Proc. Natl. Acad. Sci. 100, 330-335 (2003).
50. Teplow, D. B. et al. Elucidating Amyloid β-Protein Folding and Assembly: A Multidisciplinary Approach. Acc. Chem. Res. 39, 635-645 (2006).
51. Urbanc, B. et al. In silico study of amyloid β-protein folding and oligomerization. Proc. Natl. Acad. Sci. USA 101, 17345-17350 (2004).
52. Urbanc, B., Betnel, M., Cruz, L., Bitan, G. & Teplow, D. B. Elucidation of Amyloid β-Protein Oligomerization Mechanisms: Discrete Molecular Dynamics Study. J. Am. Chem. Soc. 132, 4266-4280 (2010).
53. Vaiana, S. M., Ghirlando, R., Yau, W.-M., Eaton, W. A. & Hofrichter, J. Sedimentation Studies on Human Amylin Fail to Detect Low-Molecular-Weight Oligomers. Biophys. J. 94, L45-L47 (2008).
54. Milardi, D., Sciacca, M. F. M., Pappalardo, M., Grasso, D. M. & Rosa, C. L. The role of aromatic side-chains in amyloid growth and membrane interaction of the islet amyloid polypeptide fragment LANFLVH. Eur. Biophys. J. 40, 1-12 (2010).
55. Urbanc, B. et al. Structural basis for Aβ1-42 toxicity inhibition by Aβ C-terminal fragments: Discrete molecular dynamics study. J. Mol. Biol. 410, 316-328 (2011).
56. Janson, J., Ashley, R. H., Harrison, D., McIntyre, S. & Butler, P. C. The mechanism of islet amyloid polypeptide toxicity is membrane disruption by intermediate-sized toxic amyloid particles. Diabetes 48, 491-498 (1999).
57. Brooks, B. R. et al. CHARMM: A program for macromolecular energy, minimization, and dynamics calculations. J. Comput. Chem. 4, 187-217 (1983).
58. Lazaridis, T. & Karplus, M. Effective energy function for proteins in solution. Proteins Struct. Funct. Bioinforma. 35, 133-152 (1999).
59. Ding, F., Borreguero, J. M., Buldyrey, S. V., Stanley, H. E. & Dokholyan, N. V. Mechanism for the α-helix to β-hairpin transition. Proteins Struct. Funct. Bioinforma. 53, 220-228 (2003).
60. Ding, F. & Dokholyan, N. V. Incorporating Backbone Flexibility in MedusaDock Improves Ligand-Binding Pose Prediction in the CSAR2011 Docking Benchmark. J. Chem. Inf. Model. 53, 1871-1879 (2013).
61. Nedumpully-Govindan, P., Jemec, D. B. & Ding, F. CSAR Benchmark of Flexible MedusaDock in Affinity Prediction and Nativelike Binding Pose Selection. J. Chem. Inf. Model., accepted, doi: 10.1021/acs.jcim.5b00303 (2015).
62. Geitner, N. K. et al. Structure-Function Relationship of PAMAM Dendrimers as Robust Oil Dispersants. Environ. Sci. Technol. 48, 12868-12875 (2014).
63. Wang, B. et al. Deviation from the Unimolecular Micelle Paradigm of PAMAM Dendrimers Induced by Strong Interligand Interactions. J. Phys. Chem. C 119, 19475-19484 (2015).
64. Nanga, R. P. R., Brender, J. R., Vivekanandan, S. & Ramamoorthy, A. Structure and membrane orientation of IAPP in its natively amidated form at physiological pH in a membrane environment. Biochim. Biophys. Acta BBA-Biomembr. 1808, 2337-2342 (2011).
65. 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. 97, 2948-2957 (2009).
66. Andersen, H. C. Molecular dynamics simulations at constant pressure and/or temperature. J. Chem. Phys. 72, 2384-2393 (1980).