Exploiting the therapeutic potential of 8-β- d -glucopyranosylgenistein: Synthesis, antidiabetic activity, and molecular interaction with islet amyloid polypeptide and amyloid β-peptide (1-42)

Journal of Medicinal Chemistry

Volumn 57, Issue 22, 2014, Pages 9463-9472

  Jesus, Ana R ^a   Dias, Catarina ^a   Matos, Ana M ^a,b   De Almeida, Rodrigo F M ^a   Viana, Ana S ^a   Marcelo, Filipa ^d   Ribeiro, Rogério T ^b,c   Macedo, Maria P ^b,c   Airoldi, Cristina ^e   Nicotra, Francesco ^e   Martins, Alice ^a   Cabrita, Eurico J ^d   Jiménez Barbero, Jesús ^f   Rauter, Amélia P ^a  

^a UNIVERSITY OF LISBON   (Portugal)

^b NOVA MEDICAL SCHOOL   (Portugal)

^c APDP   (Portugal)

^d UNIVERSIDADE NOVA DE LISBOA   (Portugal)

^e UNIVERSITY OF MILANO BICOCCA   (Italy)

^f CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

1 [2 ACETOXY 4,6 DIBENZYLOXY 3 (2,3,4,6 TETRA O BENZYL BETA DEXTRO GLUCOPYRANOSYL)]PHENYL 3 (4 BENZYLOXYPHENYL)PRO 2 EN 1; 2,4 DIBENZYLOXY 6 HYDROXY 5 (2,3,4,6 TETRA O BENZYL BETA DEXTRO GLUCOPYRANOSYL)ACETOPHENONE; 2,4 DIBENZYLOXY 6 HYDROXYACETOPHENONE; 4',5,7 TRI O BENZYL 8 (2,3,4,6 TETRA O BENZYL BETA DEXTRO GLUCOCOPYRANOSYL)GENISTEIN; 8 BETA DEXTRO GLUCOPYRANOSYLGENISTEIN; AMYLIN; AMYLOID BETA PROTEIN[1-42]; ANTIDIABETIC AGENT; GENISTEIN; THIOFLAVINE; UNCLASSIFIED DRUG; AMYLOID BETA PROTEIN; EPITOPE; GENISTEIN-8-C-GLUCOSIDE; GLUCOSIDE; INSULIN; OXYGEN; PROTEIN BINDING; PROTEIN KINASE INHIBITOR; STREPTOZOCIN; THIAZOLE DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIDIABETIC ACTIVITY; ARTICLE; ATOMIC FORCE MICROSCOPY; CALCULATION; CONTROLLED STUDY; DIABETES MELLITUS; DRUG PROTEIN BINDING; DRUG SYNTHESIS; MALE; MOLECULAR RECOGNITION; NONHUMAN; PROTEIN CONFORMATION; RAT; ALZHEIMER DISEASE; ANALOGS AND DERIVATIVES; ANIMAL; BLOOD; CHEMISTRY; DIABETES MELLITUS, EXPERIMENTAL; DRUG DESIGN; FLUORESCENCE MICROSCOPY; GENISTA; HUMAN; HYPERGLYCEMIA; METABOLISM; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROCEDURES; WISTAR RAT;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; DIABETES MELLITUS, EXPERIMENTAL; DRUG DESIGN; EPITOPES; GENISTA; GENISTEIN; GLUCOSIDES; HUMANS; HYPERGLYCEMIA; HYPOGLYCEMIC AGENTS; INSULIN; ISLET AMYLOID POLYPEPTIDE; MAGNETIC RESONANCE SPECTROSCOPY; MICROSCOPY, ATOMIC FORCE; MICROSCOPY, FLUORESCENCE; OXYGEN; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN KINASE INHIBITORS; RATS; RATS, WISTAR; STREPTOZOCIN; THIAZOLES;

EID: 84913570540     PISSN: 00222623     EISSN: 15204804     Source Type: Journal    
DOI: 10.1021/jm501069h     Document Type: Article

References (50)

1. Chiti, F.; Dobson, C. M. Protein misfolding, functional amyloid, and human disease Annu. Rev. Biochem. 2006, 75, 333-366
2. Glabe, C. Common mechanisms of amyloid oligomer pathogenesis in degenerative diseases Neurobiol. Aging 2006, 27, 570-575
3. Meier, J. J.; Kayed, R.; Lin, C.; Gurlo, T.; Haataja, L.; Jayasinghe, S.; Langen, R.; Glabe, C. G.; Butler, P. C. Inhibition of human IAPP fibril formation does not prevent β-cell death: evidence for distinct actions of oligomers and fibrils of human IAPP Am. J. Physiol.: Endocrinol. Metab. 2006, 291, 1317-1324
4. Baglioni, S.; Casamenti, F.; Bucciantini, M.; Luheshi, L. M.; Taddei, N.; Chiti, F.; Dobson, C. M.; Stefani, M. Prefibrillar amyloid aggregates could be generic toxins in higher organisms J. Neurobiol. 2006, 26, 8160-8167
5. Ladiwala, A. R.; Dordick, J. S.; Tessier, P. M. Aromatic small molecules remodel toxic soluble oligomers of amyloid β through three independent pathways J. Biol. Chem. 2011, 286, 3209-3218
6. Hirohata, M.; Ono, K.; Takasaki, J.; Takahashi, R.; Ikeda, T.; Morinaga, A.; Yamada, M. Anti-amyloidogenic effects of soybean isoflavones in vitro: fluorescence spectroscopy demonstrating direct binding to Aβ monomers, oligomers and fibrils Biochim. Biophys. Acta 2012, 1822, 1316-1324
7. Cao, P.; Raleigh, D. P. Analysis of the inhibition and remodeling of islet amyloid polypeptide amyloid fibers by flavanols Biochemistry 2012, 51, 2670-2683
8. 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 2010, 49, 8127-8133
9. Fujiwara, H.; Tabuchi, M.; Yamaguchi, T.; Iwasaki, K.; Furukawa, K.; Sekiguchi, K.; Ikarashi, W.; Kudo, Y.; Higuchi, M.; Saido, T. C.; Maeda, S.; Takashima, A.; Hara, M.; Yaegashi, N.; Kase, Y.; Arai, H. A traditional medicinal herb Paeonia suffruticosa and its active constituent 1,2,3,4,6-penta- O -galloyl-β- d -glucopyranose have potent anti-aggregation effects on Alzheimer's amyloid β proteins in vitro and in vivo J. Neurochem. 2009, 109, 1648-1657
10. Bruno, E.; Pereira, C.; Roman, K. P.; Takiguchi, M.; Kao, P.; Nogaj, L. A.; Moffet, D. A. IAPP aggregation and cellular toxicity are inhibited by 1,2,3,4,6-penta- O -galloyl-β- d -glucose Amyloid 2013, 20, 34-38
11. Wolfram, S.; Raederstorff, D.; Preller, M.; Wang, Y.; Teixeira, S. R.; Riegger, C.; Weber, P. Epigallocatechin gallate supplementation alleviates diabetes in rodents J. Nutr. 2006, 136, 2512-2518
12. Fu, Z.; Zhen, W.; Yuskavage, J.; Liu, D. Epigallocatechin gallate delays the onset of type 1 diabetes in spontaneous non-obese diabetic mice Br. J. Nutr. 2011, 105, 1218-1225
13. Mohan, C. G.; Viswanatha, G. L.; Savinay, G.; Rajendra, C. E.; Halemani, P. D. 1,2,3,4,6-Penta- O -galloyl-β- d -glucose, a bioactivity guided isolated compound from Mangifera indica inhibits 11β-HSD-1 and ameliorates high fat diet-induced diabetes in C57BL/6 mice Phytomedicine 2013, 20, 417-426
14. Salimifar, M.; Fatehi-Harranabad, Z.; Fatehi, M. A review on natural products for controlling type 2 diabetes with an emphasis on their mechanisms of actions Curr. Diabetes Rev. 2013, 9, 402-411
15. Chang, C. L. T.; Chen, W. C.; Chen, H. M.; Yang, N. S.; Yang, W. C. Natural cures for type 1 diabetes: a review of phytochemicals, biological actions, and clinical potential Curr. Med. Chem. 2013, 20, 899-907
16. Qi, L.; Liu, E.; Chu, C.; Peng, Y. B.; Cai, H. X.; Li, P. Anti-diabetic agents from natural products-an update from 2004 to 2009 Curr. Top. Med. Chem. 2010, 10, 434-457
17. Stefani, M.; Rigacci, S. Protein folding and aggregation into amyloid: the interference by natural phenolic compounds Int. J. Mol. Sci. 2013, 14, 12411-12457
18. Ansari, N.; Khodagholi, F. Natural products as promising drug candidates for the treatment of Alzheimer's disease: molecular mechanism Aspect Curr. Neuropharmacol. 2013, 11, 414-429
19. Borges, C.; Martinho, P.; Martins, A.; Rauter, A. P.; Ferreira, M. A. A. Characterization of flavonoids extracted of Genista tenera by FAB MS/MS Rapid Commun. Mass Spectrom. 2001, 15, 1760-1767
20. Rauter, A. P.; Martins, A.; Borges, C.; Ferreira, J.; Justino, J.; Bronze, M. R.; Coelho, A. V.; Choi, Y. H.; Verpoorte, R. Liquid chromatography-diode array detection-electrospray ionisation mass spectrometry/nuclear magnetic resonance analyses of the anti-hyperglycemic flavonoid extract of Genista tenera. Structure elucidation of a flavonoid-C-glycoside J. Chromatogr., A 2005, 1089, 59-64
21. Edwards, E. L.; Rodrigues, J. A.; Ferreira, J.; Goodall, D. M.; Rauter, A. P.; Justino, J.; Thomas-Oates, J. Capillary electrophoresis-mass spectrometry characterization of secondary metabolites from the anti-hyperglycemic plant Genista tenera Electrophoresis 2006, 27, 2164-2170
22. Rauter, A. P.; Ferreira, J.; Martins, A.; Santos, R. G.; Serralheiro, M. L.; Borges, C.; Araújo, M. E.; Silva, F.; Goulart, M.; Justino, J.; Rodrigues, J.; Edwards, E.; Thomas-Oates, J. P.; Noronha, J. P.; Pinto, R.; Mota-Filipe, H. Bioactivity studies and chemical profile of the antidiabetic plant Genista tenera J. Ethnopharmacol. 2009, 122, 384-393
23. Rauter, A. P.; Martins, A.; Borges, C.; Mota-Filipe, H.; Pinto, R.; Sepodes, B.; Justino, J. Antihyperglycaemic and protective effects of flavonoids on streptozotocin-induced diabetic rats Phytother. Res. 2010, 24, S133-S138
24. Rauter, A. P.; Jesus, A. R.; Martins, A.; Dias, C.; Ribeiro, R.; Macedo, M.-P.; Justino, J.; Mota-Filipe, H.; Pinto, R.; Sepodes, B.; Medeiros, M.; Barbero, J. J.; Airoldi, C.; Nicotra, F. New C-glycosylpolyphenol antidiabetic agents, effect on glucose tolerance and interactionwith beta-amyloid. Therapeutic applications of the synthesized agent(s) and of Genista tenera ethyl acetate extracts containing some of those agents. WO 2013132470A2, 2013, (submitted Mar 9, 2012; publication date, Sep 12, 2013).
25. Kumazawa, T.; Kimura, T.; Matsuba, S.; Sato, S.; Onodera, J. Synthesis of 8- C -glucosylflavones Carbohydr. Res. 2001, 334, 183-193
26. Sato, S.; Hiroe, K.; Kumazawa, T.; Jun-Ichi, O. Environmentally friendly C -glycosylation of phloroacetophenone with unprotected d -glucose using scandium(III) trifluoromethanesulfonate in aquous media: key compounds for the synthesis of mono- and di-C-glycosylflavonoids Carbohydr. Res. 2006, 341, 1091-1095
27. Westermark, P.; Engström, U.; Johnson, K. H.; Westermark, G. T.; Betsholtz, C. Islet amyloid polypeptide: pinpointing amino acid residues linked to amyloid fibril formation Proc. Natl. Acad. Sci. U.S.A. 1990, 87, 5036-5040
28. Wei, L.; Jiang, P.; Xu, W.; Li, H.; Zhang, H.; Yan, L.; Chan-Park, M. B.; Liu, X.; Tang, K.; Mu, Y.; Pervushin, K. The molecular basis of distinct aggregation pathways of islet amyloid polypeptide J. Biol. Chem. 2011, 286, 6291-6300
29. Mehla, J.; Chauhan, B. C.; Chauhan, N. B. Experimental induction of type 2 diabetes in aging-accelerated mice triggered Alzheimer-like pathology and memory deficits J. Alzheimer's Dis. 2014, 39, 145-162
30. Kim, B.; Backus, C.; Oh, S.; Feldman, E. L. Hyperglycemia-induced tau cleavage in vitro and in vivo: a possible link between diabetes and Alzheimer's disease J. Alzheimer's Dis. 2013, 34, 729-739
31. Morris, J. K.; Vidoni, E. D.; Honea, R. A.; Burns, J. M. Impaired glycemia and Alzheimer's disease Neurobiol. Aging 2014, 35, 585-589
32. Mayer, M.; Meyer, B. Characterization of ligand binding by saturation transfer difference NMR spectroscopy Angew. Chem., Int. Ed. 1999, 38, 1784-1788
33. Mayer, M.; Meyer, B. Group epitope mapping by saturation transfer difference NMR to identify segments of a ligand in direct contact with a protein receptor J. Am. Chem. Soc. 2001, 123, 6108-6117
34. Meyer, B.; Peters, T. NMR spectroscopy techniques for screening and identifying ligand binding to protein receptors Angew. Chem., Int. Ed. 2003, 42, 864-890
35. Airoldi, C.; Sironi, E.; Dias, C.; Marcelo, F.; Martins, A.; Rauter, A. P.; Nicotra, F.; Jiménez-Barbero, J. Natural compounds against Alzheimer's disease: molecular recognition of Aβ1-42 peptide by Salvia sclareoides extract and its major component, rosmarinic acid, as investigated by NMR Chem.-Asian J. 2013, 8, 596-602
36. Airoldi, C.; Cardona, F.; Sironi, E.; Colombo, L.; Salmona, M.; Cambianica, I.; Ornaghi, F.; Sancini, G.; Nicotra, F.; La Ferla, B. Fluorescent amyloid β-peptide ligand derivatives as potential diagnostic tools for Alzheimer's disease Pure Appl. Chem. 2013, 85, 1813-1823
37. Airoldi, C.; Colombo, L.; Manzoni, C.; Sironi, E.; Natalello, A.; Doglia, S. M.; Forloni, G.; Tagliavini, F.; Del Favero, E.; Cantu, L.; Nicotra, F.; Salmona, M. Tetracycline prevents Aβ oligomer toxicity through an atypical supramolecular interaction Org. Biomol. Chem. 2011, 9, 463-472
38. Airoldi, C.; Zona, C.; Sironi, E.; Colombo, L.; Messa, M.; Aurilia, D.; Gregori, M.; Masserini, M.; Salmona, M.; Nicotra, F.; La Ferla, B. Curcumin derivatives as new ligands of Aβ peptides J. Biotechnol. 2011, 156, 317-324
39. Airoldi, C.; Cardona, F.; Sironi, E.; Colombo, L.; Salmona, M.; Silva, A.; Nicotra, F.; La Ferla, B. cis -Glyco-fused benzopyran compounds as new amyloid-β peptideligands Chem. Commun. 2011, 47, 10266-10268
40. NMR Spectroscopy of Glycoconjugates; Jiménez-Barbero, J.; Peters, T., Eds.; Wiley-VCH: Weinheim, Germany, 2002.
41. Ni, F.; Zhu, Y. Accounting for ligand-protein interactions in the relaxation-matrix analysis of transferred nuclear Overhauser effects J. Magn. Reson. B 1994, 103, 180-184
42. Allinger, N. L.; Yuh, Y. H.; Lii, J. H. Molecular mechanics. The MM3 force field for hydrocarbons. 1 J. Am. Chem. Soc. 1989, 111, 8551-8566
43. Qutub, A. A.; Hunt, C. A. Glucose transport to the brain: a systems model Brain Res. 2005, 49, 595-617
44. Storr, T.; Merkel, M.; Song-Zhao, G. X.; Scott, L. E.; Green, D. E.; Bowen, M. L.; Thompson, K. H.; Patrick, B. O.; Schugar, H. J.; Orvic, C. Synthesis, characterization, and metal coordinating ability of multifunctional carbohydrate-containing compounds for Alzheimer's therapy J. Am. Chem. Soc. 2007, 129, 7453-7463
45. Ladiwala, A. R. A.; Mora-Pale, M.; Lin, J. C.; Bale, S. S.; Fishman, Z. S.; Dordick, J. S.; Tessier, P. M. Polyphenolic glycosides and aglycones utilize opposing pathways to selectively remodel and inactivate toxic oligomers of amyloid β ChemBioChem 2011, 12, 1749-1758
46. Zagorski, M. G.; Yang, J.; Shao, H.; Ma, K.; Zeng, H.; Hong, A. Methodological and chemical factors affecting amyloid beta peptide amyloidogenicity Methods Enzymol. 1999, 309, 189-203
47. MacroModel, version 9.6; Schrödinger, LLC: New York, 2008.
48. Maestro, version 9.1; Schrödinger, LLC: New York, 2010.
49. Martín-Pastor, M.; Espinosa, J. F.; Asensio, J. L.; Jiménez Barbero, J. A comparison of the geometry and of the energy results obtained by application of different molecular mechanics force fields to methyl α-lactoside and the C-analogue of lactose Carbohydr. Res. 1997, 298, 15-49
50. Still, W. C.; Tempczyk, A.; Hawley, R. C.; Hendrickson, T. Semianalytical treatment of solvation for molecular mechanics and dynamics J. Am. Chem. Soc. 1990, 112, 6127-6129