Abstract
The aberrant misfolding and self-assembly of human islet amyloid polypeptide (hIAPP)–a hormone that is co-secreted with insulin from pancreatic β-cells–into toxic oligomers, protofibrils and fibrils has been observed in type 2 diabetes mellitus (T2DM). The formation of these insoluble aggregates has been linked with the death and dysfunction of β-cells. Therefore, hIAPP aggregation has been identified as a therapeutic target for T2DM management. Several natural products are now being investigated for their potential to inhibit hIAPP aggregation and/or disaggregate preformed aggregates. In this study, we attempt to identify the anti-amyloidogenic potential of Myricetin (MYR)- a polyphenolic flavanoid, commonly found in fruits (like Syzygium cumini). Our results from biophysical studies indicated that MYR supplementation inhibits hIAPP aggregation and disaggregates preformed fibrils into non-toxic species. This protection was accompanied by inhibition of oxidative stress, reduction in lipid peroxidation and the associated membrane damage and restoration of mitochondrial membrane potential in INS-1E cells. MYR supplementation also reversed the loss of functionality in hIAPP exposed pancreatic islets via restoration of glucose-stimulated insulin secretion. Molecular dynamics simulation studies suggested that MYR molecules interact with the hIAPP pentameric fibril model at the amyloidogenic core region and thus prevents aggregation and distort the fibrils.
Funding source: University Grants Commission (UGC), Government of India
Award Identifier / Grant number: F.4-5(18-FRP)(IV-Cycle)/2017(BSR)
Funding source: Start-Up Research Grant by Science and Engineering Research Board
Award Identifier / Grant number: SB/YS/LS-23/2014; SERB
Funding source: Department of Biotechnology-DBT, Government of India
Award Identifier / Grant number: BT/RLF/Re-entry/11/2012
Funding source: CSIR, Government of India
Award Identifier / Grant number: RD/0111-CSIR000-016
Funding source: Savitribai Phule Pune University RUSA 2.0
Funding source: Ministry of Human Resource Development
Funding source: Indian Institute of Technology Bombay
Award Identifier / Grant number: 11IRCCSG003
Funding source: Department of Biotechnology, Government of India
Award Identifier / Grant number: Junior Research Fellowship (JRF)
Funding source: Wadhwani Research Center of Bioengineering
Award Identifier / Grant number: RD/018/-DONWR04-001/
Acknowledgments
The authors acknowledge Bio-AFM facility funded by RFIC-IIT Bombay; Central instrumentation facility at Savitribai Phule Pune University (SPPU); and the flow cytometer facility at Institute of Applied Biology Research and Development, Pune. We thank the staff of the National Facility for Gene Function in Health and Disease (NFGFHD) at IISER-Pune for technical support. R.D. is thankful for financial assistance from UGC-JRF, Government of India. R.P. acknowledges financial assistance from MHRD, Government of India. A.K. acknowledges funding from CSIR (RD/0111-CSIR000-016) Government of India and IIT Bombay Seed grant (11IRCCSG003). S.S. acknowledges funding from Ramalingaswami fellowship (BT/RLF/Re-entry/11/2012; Department of Biotechnology-DBT, Government of India); and University Grants Commission (UGC), Government of India F.4-5(18-FRP) (IV-Cycle)/2017(BSR)). The S.S. laboratory has been generously supported by Board of College and University Development (BCUD) grant (SPPU); Research and Development grant to the Department of Biotechnology, SPPU; and UPE Phase II grant, and RUSA 2.0 to SPPU. S.H.K. acknowledges DBT, GOI for her Master in Biotechnology fellowship and DMS acknowledges financial assistance from DBT-JRF, Government of India. J.D.A. acknowledges the funding from Start-Up Research Grant by Science and Engineering Research Board (SB/YS/LS-23/2014; SERB), Government of India. INS-1E cells were obtained as a kind gift from Prof. Claes Wollheim and Prof. Pierre Machler, University of Geneva Medical Centre. We are also very thankful to Professor Robert Tycko, NIH, for providing the pentameric coordinates of hIAPP for the molecular dynamics study.
Author contribution: AK, RD & SS conceived and designed the experiments. RD, SHK, RP, DMS, JDA and SS performed the experiment. RD, SHK, DMS, JDA, SS and AK were involved in analysis and interpretation of data. SCD performed MD simulation study. NM performed the AFM imaging experiments. JC, SS and AK contributed regents/ materials/analysis tools. RD, SCD, SHK, DMS, JDA, SS and AK compiled the data. RD, SCD, JDA, JC, SS and AK wrote the manuscript. All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.
Research funding: Council of Scientific and industrial research, Government of India (RD/0111-CSIR000-016) and Indian Institute of Technology, Bombay (11IRCCSG003); Wadhwani Research Center of Bioengineering (RD/018/-DONWR04-001/); Ramalingaswami fellowship (BT/RLF/Re-entry/11/2012; Department of Biotechnology-DBT, Government of India); and University Grants Commission (UGC, Government of India F.4-5(18-FRP) (IV-Cycle)/2017(BSR))
Conflict of interest statement: The authors declare that they have no conflicts of interest with the contents of this article.
References
Akaishi, T., Morimoto, T., Shibao, M., Watanabe, S., Sakai-Kato, K., Utsunomiya-Tate, N., and Abe, K. (2008). Structural requirements for the flavonoid fisetin in inhibiting fibril formation of amyloid β protein. Neurosci. Lett. 444: 280–285. https://doi.org/10.1016/j.neulet.2008.08.052.Search in Google Scholar
Akter, R., Cao, P., Noor, H., Ridgway, Z., Tu, L.H., Wang, H., Wong, A.G., Zhang, X., Abedini, A., Schmidt, A.M., et al. (2016). Islet amyloid polypeptide: structure, function, and pathophysiology. J. Diabetes Res. 2016: 1–18. https://doi.org/10.1155/2016/2798269.Search in Google Scholar
Apetz, N., Munch, G., Govindaraghavan, S., and Gyengesi, E. (2014). Natural compounds and plant extracts as therapeutics against chronic inflammation in Alzheimer’s disease–a translational perspective. CNS Neurol. Disord. Drug Targets 13: 1175–1191. https://doi.org/10.2174/1871527313666140917110635.Search in Google Scholar
Barth, A. (2007). Infrared spectroscopy of proteins. Biochim. Biophys. Acta Bioenerg. 1767: 1073–1101. https://doi.org/10.1016/j.bbabio.2007.06.004.Search in Google Scholar
Berendsen, H.J., van der Spoel, D., and van Drunen, R. (1995). GROMACS: a message-passing parallel molecular dynamics implementation. Comput. Phys. Commun. 91: 43–56. https://doi.org/10.1016/0010-4655(95)00042-e.Search in Google Scholar
Besler, B.H., Merz, K.M. Jr, and Kollman, P.A. (1990). Atomic charges derived from semiempirical methods. J. Comput. Chem. 11: 431–439. https://doi.org/10.1002/jcc.540110404.Search in Google Scholar
Biancalana, M. and Koide, S. (2010). Molecular mechanism of Thioflavin-T binding to amyloid fibrils. Biochim. Biophys. Acta Proteins Proteomics 1804: 1405–1412. https://doi.org/10.1016/j.bbapap.2010.04.001.Search in Google Scholar PubMed PubMed Central
Biancalana, M., Makabe, K., Koide, A., and Koide, S. (2009). Molecular mechanism of thioflavin-T binding to the surface of β-rich peptide self-assemblies. J. Mol. Biol. 385: 1052–1063. https://doi.org/10.1016/j.jmb.2008.11.006.Search in Google Scholar PubMed PubMed Central
Blanchard, B.J., Chen, A., Rozeboom, L.M., Stafford, K.A., Weigele, P., and Ingram, V.M. (2004). Efficient reversal of Alzheimer’s disease fibril formation and elimination of neurotoxicity by a small molecule. Proc. Natl. Acad. Sci. U. S. A. 101: 14326–14332. https://doi.org/10.1073/pnas.0405941101.Search in Google Scholar PubMed PubMed Central
Blau, C. and Grubmuller, H. (2013). g_contacts: fast contact search in bio-molecular ensemble data. Comput. Phys. Commun. 184: 2856–2859. https://doi.org/10.1016/j.cpc.2013.07.018.Search in Google Scholar
Borchi, E., Bargelli, V., Guidotti, V., Berti, A., Stefani, M., Nediani, C., and Rigacci, S. (2014). Mild exposure of RIN-5F β-cells to human islet amyloid polypeptide aggregates upregulates antioxidant enzymes via NADPH oxidase-RAGE: an hormetic stimulus. Redox Biol. 2: 114–122. https://doi.org/10.1016/j.redox.2013.12.005.Search in Google Scholar PubMed PubMed Central
Borde, P., Mohan, M., and Kasture, S. (2011). Effect of myricetin on deoxycorticosterone acetate (DOCA)-salt-hypertensive rats. Nat. Prod. Res. 25: 1549–1559. https://doi.org/10.1080/14786410903335190.Search in Google Scholar PubMed
Brender, J.R., Hartman, K., Nanga, R.P.R., Popovych, N., de la Salud Bea, R., Vivekanandan, S., Marsh, E.N.G., and Ramamoorthy, A. (2010). Role of zinc in human islet amyloid polypeptide aggregation. J. Am. Chem. Soc. 132: 8973–8983. https://doi.org/10.1021/ja1007867.Search in Google Scholar PubMed PubMed Central
Buchanan, L.E., Dunkelberger, E.B., Tran, H.Q., Cheng, P.N., Chiu, C.C., Cao, P., Raleigh, D.P., De Pablo, J.J., Nowick, J.S., and Zanni, M.T. (2013). Mechanism of IAPP amyloid fibril formation involves an intermediate with a transient β-sheet. Proc. Natl. Acad. Sci. U. S. A. 110: 19285–19290. https://doi.org/10.1073/pnas.1314481110.Search in Google Scholar PubMed PubMed Central
Cadavez, L., Montane, J., Alcarraz-Vizán, G., Visa, M., Vidal-Fàbrega, L., Servitja, J.M., and Novials, A. (2014). Chaperones ameliorate beta cell dysfunction associated with human islet amyloid polypeptide overexpression. PLoS One 9: e101797. https://doi.org/10.1371/journal.pone.0101797.Search in Google Scholar PubMed PubMed Central
Cao, P., Marek, P., Noor, H., Patsalo, V., Tu, L.H., Wang, H., Abedini, A., and Raleigh, D.P. (2013). Islet amyloid: from fundamental. FEBS Lett. 587: 1106–1118. https://doi.org/10.1016/j.febslet.2013.01.046.Search in Google Scholar PubMed PubMed Central
Chang, H., Mi, M.T., Gu, Y.Y., Yuan, J.L., Ling, W.H., and Lin, H. (2007). Effects of flavonoids with different structures on proliferation of leukemia cell line HL-60. Ai zheng = Aizheng = Chin. J. Cancer 26: 1309–1314.Search in Google Scholar
Chaudhury, A., Duvoor, C., Reddy Dendi, V.S., Kraleti, S., Chada, A., Ravilla, R., Marco, A., Shekhawat, N.S., Montales, M.T., Kuriakose, K., et al. (2017). Clinical review of antidiabetic drugs: implications for type 2 diabetes mellitus management. Front. Endocrinol. 8: 6. https://doi.org/10.3389/fendo.2017.00006.Search in Google Scholar PubMed PubMed Central
Cheng, B., Gong, H., Li, X., Sun, Y., Zhang, X., Chen, H., Liu, X., Zheng, L., and Huang, K. (2012). Silibinin inhibits the toxic aggregation of human islet amyloid polypeptide. Biochem. Biophys. Res. Commun. 419: 495–499. https://doi.org/10.1016/j.bbrc.2012.02.042.Search in Google Scholar PubMed
Cheng, B., Gong, H., Li, X., Sun, Y., Chen, H., Zhang, X., Wu, Q., Zheng, L., and Huang, K. (2013). Salvianolic acid B inhibits the amyloid formation of human islet amyloid polypeptide and protects pancreatic beta‐cells against cytotoxicity. Proteins Struct. Funct. Bioinf. 81: 613–621. https://doi.org/10.1002/prot.24216.Search in Google Scholar PubMed
Chhikara, N., Kaur, R., Jaglan, S., Sharma, P., Gat, Y., and Panghal, A. (2018). Bioactive compounds and pharmacological and food applications of Syzygium cumini–a review. Food Funct. 9: 6096–6115. https://doi.org/10.1039/c8fo00654g.Search in Google Scholar PubMed
Cooper, G.J., Leighton, B., Dimitriadis, G.D., Parry-Billings, M., Kowalchuk, J.M., Howland, K., Rothbard, J.B., Willis, A.C., and Reid, K.B. (1988). Amylin found in amyloid deposits in human type 2 diabetes mellitus may be a hormone that regulates glycogen metabolism in skeletal muscle. Proc. Natl. Acad. Sci. U. S. A. 85: 7763–7766. https://doi.org/10.1073/pnas.85.20.7763.Search in Google Scholar PubMed PubMed Central
Coulson, C.A. (1938). Self-consistent field for molecular hydrogen. Math. Proc. Camb. Philos. Soc. 34: 204–212. https://doi.org/10.1017/s0305004100020089.Search in Google Scholar
Dantu, S.C., Khavnekar, S., and Kale, A. (2017). Conformational dynamics of Peb4 exhibit “mother’s arms” chain model: a molecular dynamics study. J. Biomol. Struct. Dyn. 35: 2186–2196. https://doi.org/10.1080/07391102.2016.1209131.Search in Google Scholar PubMed
Dobson, C.M. (2003). Protein folding and misfolding. Nature 426: 884–890. https://doi.org/10.1038/nature02261.Search in Google Scholar PubMed
Dubey, R., Minj, P., Malik, N., Sardesai, D.M., Kulkarni, S.H., Acharya, J.D., Bhavesh, N.S., Sharma, S., and Kumar, A. (2017). Recombinant human islet amyloid polypeptide forms shorter fibrils and mediates β-cell apoptosis via generation of oxidative stress. Biochem. J. 474: 3915–3934. https://doi.org/10.1042/bcj20170323.Search in Google Scholar PubMed
Dubey, R., Patil, K., Dantu, S.C., Sardesai, D.M., Bhatia, P., Malik, N., Acharya, J.D., Sarkar, S., Ghosh, S., Chakrabarti, R., et al. (2019). Azadirachtin inhibits amyloid formation, disaggregates pre-formed fibrils and protects pancreatic β-cells from human islet amyloid polypeptide/amylin-induced cytotoxicity. Biochem. J. 476: 889–907. https://doi.org/10.1042/bcj20180820.Search in Google Scholar PubMed
Fernández-Gómez, I., Sablón-Carrazana, M., Bencomo-Martínez, A., Domínguez, G., Lara-Martínez, R., Altamirano-Bustamante, N.F., Jiménez-García, L.F., Pasten-Hidalgo, K., Castillo-Rodríguez, R.A., Altamirano, P., et al. (2018). Diabetes drug discovery: hIAPP1–37 polymorphic amyloid structures as novel therapeutic targets. Molecules 23: 686. https://doi.org/10.3390/molecules23030686.Search in Google Scholar PubMed PubMed Central
Frieden, C. (2007). Protein aggregation processes: in search of the mechanism. Protein Sci. 16: 2334–2344. https://doi.org/10.1110/ps.073164107.Search in Google Scholar PubMed PubMed Central
Frisch, M.J., Trucks, G.W., Schlegel, H.B., Scuseria, G.E., Robb, M.A., Cheeseman, J.R., Scalmani, G., Barone, V., Mennucci, B., Petersson, G.A., et al. (2009). Gaussian 09, Revision A.1, Vol. 121. Gaussian. Inc., Wallingford CT, pp. 150–166.Search in Google Scholar
Gajera, H.P., Gevariya, S.N., Hirpara, D.G., Patel, S.V., and Golakiya, B.A. (2017). Antidiabetic and antioxidant functionality associated with phenolic constituents from fruit parts of indigenous black jamun (Syzygium cumini L.) landraces. J. Food Sci. Technol. 54: 3180–3191. https://doi.org/10.1007/s13197-017-2756-8.Search in Google Scholar PubMed PubMed Central
Gazit, E. (2002). A possible role for π‐stacking in the self‐assembly of amyloid fibrils. FASEB. J. 16: 77–83. https://doi.org/10.1096/fj.01-0442hyp.Search in Google Scholar PubMed
Hamaguchi, T., Ono, K., Murase, A., and Yamada, M. (2009). Phenolic compounds prevent Alzheimer’s pathology through different effects on the amyloid-β aggregation pathway. Am. J. Pathol. 175: 2557–2565. https://doi.org/10.2353/ajpath.2009.090417.Search in Google Scholar PubMed PubMed Central
He, L., Wang, X., Zhao, C., Wang, H., and Du, W. (2013). Ruthenium complexes as novel inhibitors of human islet amyloid polypeptide fibril formation. Metallomics 5: 1599–1603. https://doi.org/10.1039/c3mt00146f.Search in Google Scholar PubMed
He, J., Wang, Y., Chang, A.K., Xu, L., Wang, N., Chong, X., Li, H., Zhang, B., Jones, G.W., and Song, Y. (2014). Myricetin prevents fibrillogenesis of hen egg white lysozyme. J. Agric. Food Chem. 62: 9442–9449. https://doi.org/10.1021/jf5025449.Search in Google Scholar PubMed
Hernández, M.G., Aguilar, A.G., Burillo, J., Oca, R.G., Manca, M.A., Novials, A., Alcarraz-Vizan, G., Guillén, C., and Benito, M. (2018). Pancreatic β cells overexpressing hIAPP impaired mitophagy and unbalanced mitochondrial dynamics. Cell Death Dis. 9: 1–11. https://doi.org/10.1038/s41419-018-0533-x.Search in Google Scholar PubMed PubMed Central
Hiermann, A., Schramm, H.W., and Laufer, S. (1998). Anti-inflammatory activity of myricetin-3-O-β-D-glucuronide and related compounds. Inflamm. Res. 47: 421–427. https://doi.org/10.1007/s000110050355.Search in Google Scholar PubMed
Jayakanthan, K., Mohan, S., and Pinto, B.M. (2009). Structure proof and synthesis of kotalanol and de-O-sulfonated kotalanol, glycosidase inhibitors isolated from an herbal remedy for the treatment of type-2 diabetes. J. Am. Chem. Soc. 131: 5621–5626. https://doi.org/10.1021/ja900867q.Search in Google Scholar PubMed
Jiang, P., Li, W., Shea, J.E., and Mu, Y. (2011). Resveratrol inhibits the formation of multiple-layered β-sheet oligomers of the human islet amyloid polypeptide segment 22–27. Biophys. J. 100: 1550–1558. https://doi.org/10.1016/j.bpj.2011.02.010.Search in Google Scholar PubMed PubMed Central
Jurgens, C.A., Toukatly, M.N., Fligner, C.L., Udayasankar, J., Subramanian, S.L., Zraika, S., Aston-Mourney, K., Carr, D.B., Westermark, P., Westermark, G.T., et al. (2011). β-cell loss and β-cell apoptosis in human type 2 diabetes are related to islet amyloid deposition. Am. J. Pathol. 178: 2632–2640. https://doi.org/10.1016/j.ajpath.2011.02.036.Search in Google Scholar PubMed PubMed Central
Karker, M., Falleh, H., Msaada, K., Smaoui, A., Abdelly, C., Legault, J., and Ksouri, R. (2016). Antioxidant, anti-inflammatory and anticancer activities of the medicinal halophyte Reaumuria vermiculata. Excli Journal 15: 297–307. https://doi.org/10.17179/excli2016-187.Search in Google Scholar PubMed PubMed Central
Kusakabe, T., Ebihara, K., Sakai, T., Miyamoto, L., Aotani, D., Yamamoto, Y., Yamamoto-Kataoka, S., Aizawa-Abe, M., Fujikura, J., Hosoda, K., et al. (2012). Amylin improves the effect of leptin on insulin sensitivity in leptin-resistant diet-induced obese mice. Am. J. Physiol. Endocrinol. Metab. 302: E924–E931. https://doi.org/10.1152/ajpendo.00198.2011.Search in Google Scholar PubMed
Lee, J., Cheng, X., Swails, J.M., Yeom, M.S., Eastman, P.K., Lemkul, J.A., Wei, S., Buckner, J., Jeong, J.C., Qi, Y., et al. (2016). CHARMM-GUI input generator for NAMD, GROMACS, AMBER, OpenMM, and CHARMM/OpenMM simulations using the CHARMM36 additive force field. J. Chem. Theory Comput. 12: 405–413. https://doi.org/10.1021/acs.jctc.5b00935.Search in Google Scholar
Li, Y. and Ding, Y. (2012). Minireview: therapeutic potential of myricetin in diabetes mellitus. Food Sci. Hum. Well. 1: 19–25. https://doi.org/10.1016/j.fshw.2012.08.002.Search in Google Scholar
Li, X.L., Xu, G., Chen, T., Wong, Y.S., Zhao, H.L., Fan, R.R., Gu, X.M., Tong, P.C., and Chan, J.C. (2009). Phycocyanin protects INS-1E pancreatic beta cells against human islet amyloid polypeptide-induced apoptosis through attenuating oxidative stress and modulating JNK and p38 mitogen-activated protein kinase pathways. Int. J. Biochem. Cell Biol. 41: 1526–1535. https://doi.org/10.1016/j.biocel.2009.01.002.Search in Google Scholar
Li, J., Guan, M., Li, C., Lyv, F., Zeng, Y., Zheng, Z., Wang, C., and Xue, Y. (2014). The dipeptidyl peptidase-4 inhibitor sitagliptin protects against dyslipidemia-related kidney injury in apolipoprotein E knockout mice. Int. J. Mol. Sci. 15: 11416–11434. https://doi.org/10.3390/ijms150711416.Search in Google Scholar
Li, Y., Zheng, X., Yi, X., Liu, C., Kong, D., Zhang, J., and Gong, M. (2017). Myricetin: a potent approach for the treatment of type 2 diabetes as a natural class B GPCR agonist. FASEB. J. 31: 2603–2611. https://doi.org/10.1096/fj.201601339r.Search in Google Scholar
Ma, L., Li, X., Wang, Y., Zheng, W., and Chen, T. (2014). Cu (II) inhibits hIAPP fibrillation and promotes hIAPP-induced beta cell apoptosis through induction of ROS-mediated mitochondrial dysfunction. J. Inorg. Biochem. 140: 143–152. https://doi.org/10.1016/j.jinorgbio.2014.07.002.Search in Google Scholar
Mahoney, M.W. and Jorgensen, W.L. (2000). A five-site model for liquid water and the reproduction of the density anomaly by rigid, nonpolarizable potential functions. J. Chem. Phys. 112: 8910–8922. https://doi.org/10.1063/1.481505.Search in Google Scholar
Marzban, L., Park, K., and Verchere, C.B. (2003). Islet amyloid polypeptide and type 2 diabetes. Exp. Gerontol. 38: 347–351. https://doi.org/10.1016/s0531-5565(03)00004-4.Search in Google Scholar
Merglen, A., Theander, S., Rubi, B., Chaffard, G., Wollheim, C.B., and Maechler, P. (2004). Glucose sensitivity and metabolism-secretion coupling studied during two-year continuous culture in INS-1E insulinoma cells. Endocrinology 145: 667–678. https://doi.org/10.1210/en.2003-1099.Search in Google Scholar PubMed
Mukherjee, A., Morales-Scheihing, D., Butler, P.C., and Soto, C. (2015). Type 2 diabetes as a protein misfolding disease. Trends Mol. Med. 21: 439–449. https://doi.org/10.1016/j.molmed.2015.04.005.Search in Google Scholar PubMed PubMed Central
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. https://doi.org/10.1002/pro.2023.Search in Google Scholar
Ochterski, J.W., Petersson, G.A., and Montgomery, J.A. Jr (1996). A complete basis set model chemistry. V. Extensions to six or more heavy atoms. J. Chem. Phys. 104: 2598–2619. https://doi.org/10.1063/1.470985.Search in Google Scholar
Okada, A.K., Teranishi, K., Isas, J.M., Bedrood, S., Chow, R.H., and Langen, R. (2016). Diabetic risk factors promote islet amyloid polypeptide misfolding by a common, membrane-mediated mechanism. Sci. Rep. 6: 1–10. https://doi.org/10.1038/srep31094.Search in Google Scholar
Ono, K., Yoshiike, Y., Takashima, A., Hasegawa, K., Naiki, H., and Yamada, M. (2003). Potent anti‐amyloidogenic and fibril‐destabilizing effects of polyphenols in vitro: implications for the prevention and therapeutics of Alzheimer’s disease. J. Neurochem. 87: 172–181. https://doi.org/10.1046/j.1471-4159.2003.01976.x.Search in Google Scholar
Padrick, S.B. and Miranker, A.D. (2001). Islet amyloid polypeptide: identification of long-range contacts and local order on the fibrillogenesis pathway. J. Mol. Biol. 308: 783–794. https://doi.org/10.1006/jmbi.2001.4608.Search in Google Scholar
Patel, D.K., Prasad, S.K., Kumar, R., and Hemalatha, S. (2012). An overview on antidiabetic medicinal plants having insulin mimetic property. Asian Pac. J. Trop. Biomed. 2: 320–330. https://doi.org/10.1016/s2221-1691(12)60032-x.Search in Google Scholar
Petersson, A., Bennett, A., Tensfeldt, T.G., Al‐Laham, M.A., Shirley, W.A., and Mantzaris, J. (1988). A complete basis set model chemistry. I. The total energies of closed‐shell atoms and hydrides of the first‐row elements. J. Chem. Phys. 89: 2193–2218. https://doi.org/10.1063/1.455064.Search in Google Scholar
Pilkington, E.H., Gurzov, E.N., Kakinen, A., Litwak, S.A., Stanley, W.J., Davis, T.P., and Ke, P.C. (2016). Pancreatic β-cell membrane fluidity and toxicity induced by human islet amyloid polypeptide species. Sci. Rep. 6: 21274. https://doi.org/10.1038/srep21274.Search in Google Scholar PubMed PubMed Central
Pithadia, A., Brender, J.R., Fierke, C.A., and Ramamoorthy, A. (2016). Inhibition of IAPP aggregation and toxicity by natural products and derivatives. J. Diabetes Res. 2016: 1–12. https://doi.org/10.1155/2016/2046327.Search in Google Scholar PubMed PubMed Central
Sciacca, M.F., Chillemi, R., Sciuto, S., Greco, V., Messineo, C., Kotler, S.A., Lee, D.K., Brender, J.R., Ramamoorthy, A., La Rosa, C., et al. (2018). A blend of two resveratrol derivatives abolishes hIAPP amyloid growth and membrane damage. Biochim. Biophys. Acta Biomembr. 1860: 1793–1802. https://doi.org/10.1016/j.bbamem.2018.03.012.Search in Google Scholar PubMed
Semwal, D.K., Semwal, R.B., Combrinck, S., and Viljoen, A. (2016). Myricetin: a dietary molecule with diverse biological activities. Nutrients 8: 90. https://doi.org/10.3390/nu8020090.Search in Google Scholar PubMed PubMed Central
Sgarbossa, A. (2012). Natural biomolecules and protein aggregation: emerging strategies against amyloidogenesis. Int. J. Mol. Sci. 13: 17121–17137. https://doi.org/10.3390/ijms131217121.Search in Google Scholar PubMed PubMed Central
Sim, L., Jayakanthan, K., Mohan, S., Nasi, R., Johnston, B.D., Pinto, B.M., and Rose, D.R. (2010). New glucosidase inhibitors from an ayurvedic herbal treatment for type 2 diabetes: structures and inhibition of human intestinal maltase-glucoamylase with compounds from Salacia reticulata. Biochemistry 49: 443–451. https://doi.org/10.1021/bi9016457.Search in Google Scholar PubMed
Singh, U.C. and Kollman, P.A. (1984). An approach to computing electrostatic charges for molecules. J. Comput. Chem. 5: 129–145. https://doi.org/10.1002/jcc.540050204.Search in Google Scholar
Stanković, I.M., Niu, S., Hall, M.B., and Zarić, S.D. (2020). Role of aromatic amino acids in amyloid self-assembly. Int. J. Biol. Macromol. 156: 949–959. https://doi.org/10.1016/j.ijbiomac.2020.03.064.Search in Google Scholar PubMed
Stefani, M. and Rigacci, S. (2013). Protein folding and aggregation into amyloid: the interference by natural phenolic compounds. Int. J. Mol. Sci. 14: 12411–12457. https://doi.org/10.3390/ijms140612411.Search in Google Scholar PubMed PubMed Central
Stridsberg, M. and Wilander, E. (1991). Islet amyloid polypeptide (IAPP) a short review. Acta Oncol. 30: 451–456. https://doi.org/10.3109/02841869109092400.Search in Google Scholar PubMed
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. https://doi.org/10.1007/s12035-010-8111-y.Search in Google Scholar PubMed PubMed Central
Tu, L.H. and Raleigh, D.P. (2013). Role of aromatic interactions in amyloid formation by islet amyloid polypeptide. Biochemistry 52: 333–342. https://doi.org/10.1021/bi3014278.Search in Google Scholar PubMed PubMed Central
Tu, L.H., Young, L.M., Wong, A.G., Ashcroft, A.E., Radford, S.E., and Raleigh, D.P. (2015). 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 54: 666–676. https://doi.org/10.1021/bi501016r.Search in Google Scholar PubMed PubMed Central
Van Der Spoel, D., Lindahl, E., Hess, B., Groenhof, G., Mark, A.E., and Berendsen, H.J. (2005). GROMACS: fast, flexible, and free. J. Comput. Chem. 26: 1701–1718. https://doi.org/10.1002/jcc.20291.Search in Google Scholar PubMed
Velander, P., Wu, L., Ray, W.K., Helm, R.F., and Xu, B. (2016). Amylin amyloid inhibition by flavonoid baicalein: key roles of its vicinal dihydroxyl groups of the catechol moiety. Biochemistry 55: 4255–4258. https://doi.org/10.1021/acs.biochem.6b00578.Search in Google Scholar PubMed
Wang, Z.H., Kang, K.A., Zhang, R., Piao, M.J., Jo, S.H., Kim, J.S., Kang, S.S., Lee, J.S., Park, D.H., and Hyun, J.W. (2010). Myricetin suppresses oxidative stress-induced cell damage via both direct and indirect antioxidant action. Environ. Toxicol. Pharmacol. 29: 12–18. https://doi.org/10.1016/j.etap.2009.08.007.Search in Google Scholar PubMed
Zelus, C., Fox, A., Calciano, A., Faridian, B.S., Nogaj, L.A., and Moffet, D.A. (2012). Myricetin inhibits islet amyloid polypeptide (IAPP) aggregation and rescues living mammalian cells from IAPP toxicity. Open Biochem. J. 6: 66–70. https://doi.org/10.2174/1874091x01206010066.Search in Google Scholar PubMed PubMed Central
Zraika, S., Hull, R.L., Udayasankar, J., Aston-Mourney, K., Subramanian, S.L., Kisilevsky, R., Szarek, W.A., and Kahn, S.E. (2009). Oxidative stress is induced by islet amyloid formation and time-dependently mediates amyloid-induced beta cell apoptosis. Diabetologia 52: 626–635. https://doi.org/10.1007/s00125-008-1255-x.Search in Google Scholar PubMed PubMed Central
Supplementary material
The online version of this article offers supplementary material (https://doi.org/10.1515/hsz-2020-0176).
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