Polyphenols can inhibit furin in vitro as A result of the reactivity of their auto-oxidation products to proteins

Current Medicinal Chemistry

Volumn 20, Issue 6, 2013, Pages 840-850

  Zhu, J ^a   Van de Ven, W J M ^a,c   Verbiest, T ^a   Koeckelberghs, G ^a   Chen, C ^b   Cui, Y ^b   Vermorken, A J M ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b NORTHWEST UNIVERSITY   (China)

^c FLORIDA ATLANTIC UNIVERSITY   (United States)

Author keywords

( )Egcg; Bovine Serum Albumin; Furin Mediated Substrate Processing; Glutathione; Hydrogen Peroxide; Polyphenols; Promiscuous Inhibitors; Proprotein Convertase; Screening

Indexed keywords

CATECHIN; EPICATECHIN; EPICATECHIN GALLATE; EPIGALLOCATECHIN; EPIGALLOCATECHIN GALLATE; FURIN; GALLIC ACID; GLUTATHIONE; HYDROGEN PEROXIDE; POLYPHENOL; QUERCETIN;

ARTICLE; AUTOOXIDATION; ELECTROPHILICITY; HUMAN; IN VITRO STUDY; NUCLEOPHILICITY; OXIDATION REDUCTION REACTION;

EID: 84877978868     PISSN: 09298673     EISSN: 1875533X     Source Type: Journal    
DOI: 10.2174/092986713805076702     Document Type: Article

References (63)

1. Khan, N.; Afaq, F.; Mukhtar, H. Cancer chemoprevention through dietary antioxidants: progress and promise. Antioxid Redox Signal. 2008, 10, 475-510
2. Seidah, N.G.; Prat, A. The biology and therapeutic targeting of the proprotein convertases. Nat Rev Drug Discov. 2012, 11, 367-383
3. Artenstein, A.W.; Opal, S.M. Proprotein convertases in health and disease. N Engl J Med. 2011, 365, 2507-2518
4. Majumdar, S.; Mohanta, B.C.; Chowdhury, D.R.; Banik, R.; Dinda, B.; Basak, A. Proprotein convertase inhibitory activities of flavonoids isolated from Oroxylum indicum. Curr Med Chem. 2010, 17, 2049-2058
5. Zhu, J.; Declercq, J.; Creemers, J.W.; Chen, C.; Cui, Y.; Van de Ven, W.J.; Vermorken, A.J. Limitations of Inhibitory Activities of Polyphenols on Furin-Mediated Substrate Processing. Curr Med Chem. 2012, 19, 3641-3650.
6. Becker, G.L.; Sielaff, F.; Than, M.E.; Lindberg, I.; Routhier, S.; Day, R.; Lu, Y.; Garten, W.; Steinmetzer, T. Potent inhibitors of furin and furin-like proprotein convertases containing decarboxylated P1 arginine mimetics. J Med Chem. 2009, 53, 1067-1075
7. Jiao, G.S.; Cregar, L.; Wang, J.; Millis, S.Z.; Tang, C.; O'Malley, S.; Johnson, A.T.; Sareth, S.; Larson, J.; Thomas, G. Synthetic small molecule furin inhibitors derived from 2,5-dideoxystreptamine. Proc Natl Acad Sci U S A. 2006, 103, 19707-19712 (Pubitemid 46037496)
8. Komiyama, T.; Coppola, J.M.; Larsen, M.J.; van Dort, M.E.; Ross, B.D.; Day, R.; Rehemtulla, A.; Fuller, R.S. Inhibition of furin/proprotein convertase-catalyzed surface and intracellular processing by small molecules. J Biol Chem. 2009, 284, 15729-15738
9. Sielaff, F.; Than, M.E.; Bevec, D.; Lindberg, I.; Steinmetzer, T. New furin inhibitors based on weakly basic amidinohydrazones. Bioorg Med Chem Lett. 2010, 21, 836-840
10. Wu, Y.W.; Alexandrov, K.; Brunsveld, L. Synthesis of a fluorescent analogue of geranylgeranyl pyrophosphate and its use in a high-Throughput fluorometric assay for Rab geranylgeranyltransferase. Nat Protoc. 2007, 2, 2704-2711
11. McGovern, S.L.; Caselli, E.; Grigorieff, N.; Shoichet, B.K. A common mechanism underlying promiscuous inhibitors from virtual and highthroughput screening. J Med Chem. 2002, 45, 1712-1722 (Pubitemid 34293537)
12. Seidler, J.; McGovern, S.L.; Doman, T.N.; Shoichet, B.K. Identification and prediction of promiscuous aggregating inhibitors among known drugs. J Med Chem. 2003, 46, 4477-4486 (Pubitemid 37238749)
13. McGovern, S.L.; Helfand, B.T.; Feng, B.; Shoichet, B.K. A specific mechanism of nonspecific inhibition. J Med Chem. 2003, 46, 4265-4272 (Pubitemid 37153008)
14. Feng, B.Y.; Shoichet, B.K. A detergent-based assay for the detection of promiscuous inhibitors. Nat Protoc. 2006, 1, 550-553
15. Yang, C.S.; Maliakal, P.; Meng, X. Inhibition of carcinogenesis by tea. Annu Rev Pharmacol Toxicol. 2002, 42, 25-54 (Pubitemid 34160518)
16. Davies, S.P.; Reddy, H.; Caivano, M.; Cohen, P. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J. 2000, 351, 95-105
17. Fesen, M.R.; Kohn, K.W.; Leteurtre, F.; Pommier, Y. Inhibitors of human immunodeficiency virus integrase. Proc Natl Acad Sci U S A. 1993, 90, 2399-2403 (Pubitemid 23078634)
18. Matter, W.F.; Brown, R.F.; Vlahos, C.J. The inhibition of phosphatidylinositol 3-kinase by quercetin and analogs. Biochem Biophys Res Commun. 1992, 186, 624-631
19. McGovern, S.L.; Shoichet, B.K. Kinase inhibitors: not just for kinases anymore. J Med Chem. 2003, 46, 1478-1483 (Pubitemid 36512711)
20. Bertoldi, M.; Gonsalvi, M.; Voltattorni, C.B. Green tea polyphenols: novel irreversible inhibitors of dopa decarboxylase. Biochem Biophys Res Commun. 2001, 284, 90-93 (Pubitemid 32924313)
21. Fang, M.Z.; Wang, Y.; Ai, N.; Hou, Z.; Sun, Y.; Lu, H.; Welsh, W.; Yang, C.S. Tea polyphenol (-)-epigallocatechin-3-gallate inhibits DNA methyltransferase and reactivates methylation-silenced genes in cancer cell lines. Cancer Res. 2003, 63, 7563-7570 (Pubitemid 37466673)
22. Hiipakka, R.A.; Zhang, H.Z.; Dai, W.; Dai, Q.; Liao, S. Structure-Activity relationships for inhibition of human 5alpha-reductases by polyphenols. Biochem Pharmacol. 2002, 63, 1165-1176 (Pubitemid 34267032)
23. No, J.K.; Soung, D.Y.; Kim, Y.J.; Shim, K.H.; Jun, Y.S.; Rhee, S.H.; Yokozawa, T.; Chung, H.Y. Inhibition of tyrosinase by green tea components. Life Sci. 1999, 65, PL241-246
24. Sanchez-del-Campo, L.; Saez-Ayala, M.; Chazarra, S.; Cabezas-Herrera, J.; Rodriguez-Lopez, J.N. Binding of natural and synthetic polyphenols to human dihydrofolate reductase. Int J Mol Sci. 2009, 10, 5398-5410
25. Dixon, M. The determination of enzyme inhibitor constants. Biochem J. 1953, 55, 170-171
26. Ishii, T.; Mori, T.; Tanaka, T.; Mizuno, D.; Yamaji, R.; Kumazawa, S.; Nakayama, T.; Akagawa, M. Covalent modification of proteins by green tea polyphenol (-)-epigallocatechin-3-gallate through autoxidation. Free Radic Biol Med. 2008, 45, 1384-1394
27. Li, W.; Zhu, S.; Li, J.; Assa, A.; Jundoria, A.; Xu, J.; Fan, S.; Eissa, N.T.; Tracey, K.J.; Sama, A.E.; Wang, H. EGCG stimulates autophagy and reduces cytoplasmic HMGB1 levels in endotoxin-stimulated macrophages. Biochem Pharmacol. 2011, 81, 1152-1163
28. Kacprzak, M.M.; Peinado, J.R.; Than, M.E.; Appel, J.; Henrich, S.; Lipkind, G.; Houghten, R.A.; Bode, W.; Lindberg, I. Inhibition of furin by polyarginine-containing peptides: nanomolar inhibition by nona-D-Arginine. J Biol Chem. 2004, 279, 36788-36794 (Pubitemid 39129027)
29. Little, W.C.; Schwartlander, R.; Smith, M.L.; Gourdon, D.; Vogel, V. Stretched extracellular matrix proteins turn fouling and are functionally rescued by the chaperones albumin and casein. Nano Lett. 2009, 9, 4158-4167
30. Marini, I.; Moschini, R.; Del Corso, A.; Mura, U. Chaperone-like features of bovine serum albumin: A comparison with alpha-crystallin. Cell Mol Life Sci. 2005, 62, 3092-3099 (Pubitemid 43004757)
31. Coan, K.E.; Maltby, D.A.; Burlingame, A.L.; Shoichet, B.K. Promiscuous aggregate-based inhibitors promote enzyme unfolding. J Med Chem. 2009, 52, 2067-2075
32. Candiano, G.; Petretto, A.; Bruschi, M.; Santucci, L.; Dimuccio, V.; Prunotto, M.; Gusmano, R.; Urbani, A.; Ghiggeri, G.M. The oxido-redox potential of albumin methodological approach and relevance to human diseases. J Proteomics. 2009, 73, 188-195
33. Diaz, M.; Dunn, C.M.; McClements, D.J.; Decker, E.A. Use of caseinophosphopeptides as natural antioxidants in oil-in-water emulsions. J Agric Food Chem. 2003, 51, 2365-2370
34. Quinlan, G.J.; Martin, G.S.; Evans, T.W. Albumin: biochemical properties and therapeutic potential. Hepatology. 2005, 41, 1211-1219 (Pubitemid 40770271)
35. Akagawa, M.; Shigemitsu, T.; Suyama, K. Production of hydrogen peroxide by polyphenols and polyphenol-rich beverages under quasi-physiological conditions. Biosci Biotechnol Biochem. 2003, 67, 2632-2640 (Pubitemid 39251617)
36. Nakagawa, H.; Hasumi, K.; Woo, J.T.; Nagai, K.; Wachi, M. Generation of hydrogen peroxide primarily contributes to the induction of Fe(II)-dependent apoptosis in Jurkat cells by (-)-epigallocatechin gallate. Carcinogenesis. 2004, 25, 1567-1574 (Pubitemid 39214298)
37. Spencer, J.D.; Gibbons, N.C.; Bohm, M.; Schallreuter, K.U. The Ca2+-binding capacity of epidermal furin is disrupted by H2O2-mediated oxidation in vitiligo. Endocrinology. 2008, 149, 1638-1645 (Pubitemid 351468307)
38. Ashani, Y.; Catravas, G.N. Highly reactive impurities in Triton X-100 and Brij 35: partial characterization and removal. Anal Biochem. 1980, 109, 55-62
39. Lever, M. Peroxides in Detergents as Interfering Factors in Biochemical Analysis. Analytical Biochemistry. 1977, 83, 274-284 (Pubitemid 8218310)
40. Arakawa, H.; Maeda, M.; Okubo, S.; Shimamura, T. Role of hydrogen peroxide in bactericidal action of catechin. Biol Pharm Bull. 2004, 27, 277-281 (Pubitemid 41685465)
41. Babich, H.; Krupka, M.E.; Nissim, H.A.; Zuckerbraun, H.L. Differential in vitro cytotoxicity of (-)-epicatechin gallate (ECG) to cancer and normal cells from the human oral cavity. Toxicol In Vitro. 2005, 19, 231-242 (Pubitemid 40092747)
42. Mori, T.; Ishii, T.; Akagawa, M.; Nakamura, Y.; Nakayama, T. Covalent binding of tea catechins to protein thiols: the relationship between stability and electrophilic reactivity. Biosci Biotechnol Biochem. 2010, 74, 2451-2456
43. van Zanden, J.J.; Ben Hamman, O.; van Iersel, M.L.; Boeren, S.; Cnubben, N.H.; Lo Bello, M.; Vervoort, J.; van Bladeren, P.J.; Rietjens, I.M. Inhibition of human glutathione S-Transferase P1-1 by the flavonoid quercetin. Chem Biol Interact. 2003, 145, 139-148 (Pubitemid 36398427)
44. Mochizuki, M.; Yamazaki, S.; Kano, K.; Ikeda, T. Kinetic analysis and mechanistic aspects of autoxidation of catechins. Biochim Biophys Acta. 2002, 1569, 35-44 (Pubitemid 34165555)
45. Coan, K.E.; Shoichet, B.K. Stability and equilibria of promiscuous aggregates in high protein milieus. Mol Biosyst. 2007, 3, 208-213 (Pubitemid 46293327)
46. Hodnick, W.F.; Kalyanaraman, B.; Pritsos, C.A.; Pardini, R.S. The production of hydroxyl and semiquinone free radicals during the autoxidation of redox active flavonoids. Basic Life Sci. 1988, 49, 149-152
47. Canada, A.T.; Giannella, E.; Nguyen, T.D.; Mason, R.P. The production of reactive oxygen species by dietary flavonols. Free Radic Biol Med. 1990, 9, 441-449 (Pubitemid 120037538)
48. Metodiewa, D.; Jaiswal, A.K.; Cenas, N.; Dickancaite, E.; Segura-Aguilar, J. Quercetin may act as a cytotoxic prooxidant after its metabolic activation to semiquinone and quinoidal product. Free Radic Biol Med. 1999, 26, 107-116 (Pubitemid 29001498)
49. Boersma, M.G.; Vervoort, J.; Szymusiak, H.; Lemanska, K.; Tyrakowska, B.; Cenas, N.; Segura-Aguilar, J.; Rietjens, I.M. Regioselectivity and reversibility of the glutathione conjugation of quercetin quinone methide. Chem Res Toxicol. 2000, 13, 185-191 (Pubitemid 30169963)
50. Awad, H.M.; Boersma, M.G.; Boeren, S.; van Bladeren, P.J.; Vervoort, J.; Rietjens, I.M. Structure-Activity study on the quinone/quinone methide chemistry of flavonoids. Chem Res Toxicol. 2001, 14, 398-408 (Pubitemid 32367473)
51. Awad, H.M.; Boersma, M.G.; Boeren, S.; van Bladeren, P.J.; Vervoort, J.; Rietjens, I.M. The regioselectivity of glutathione adduct formation with flavonoid quinone/quinone methides is pH-dependent. Chem Res Toxicol. 2002, 15, 343-351 (Pubitemid 34241372)
52. Azam, S.; Hadi, N.; Khan, N.U.; Hadi, S.M. Prooxidant property of green tea polyphenols epicatechin and epigallocatechin-3-gallate: implications for anticancer properties. Toxicol In Vitro. 2004, 18, 555-561 (Pubitemid 38900862)
53. Walle, T.; Vincent, T.S.; Walle, U.K. Evidence of covalent binding of the dietary flavonoid quercetin to DNA and protein in human intestinal and hepatic cells. Biochem Pharmacol. 2003, 65, 1603-1610 (Pubitemid 36577273)
54. Sang, S.; Yang, I.; Buckley, B.; Ho, C.T.; Yang, C.S. Autoxidative quinone formation in vitro and metabolite formation in vivo from tea polyphenol (-)-epigallocatechin-3-gallate: studied by real-Time mass spectrometry combined with tandem mass ion mapping. Free Radic Biol Med. 2007, 43, 362-371 (Pubitemid 46977623)
55. Galati, G.; Lin, A.; Sultan, A.M.; O'Brien, P.J. Cellular and in vivo hepatotoxicity caused by green tea phenolic acids and catechins. Free Radic Biol Med. 2006, 40, 570-580 (Pubitemid 43170808)
56. Rishton, G.M. Reactive compounds and in vitro false positives in HTS. Drug Discovery Today. 1997, 2, 382-384 (Pubitemid 27368216)
57. Bae, M.J.; Ishii, T.; Minoda, K.; Kawada, Y.; Ichikawa, T.; Mori, T.; Kamihira, M.; Nakayama, T. Albumin stabilizes (-)-epigallocatechin gallate in human serum: binding capacity and antioxidant property. Mol Nutr Food Res. 2009, 53, 709-715
58. Goddard, J.P.; Reymond, J.L. Enzyme assays for high-Throughput screening. Curr Opin Biotechnol. 2004, 15, 314-322
59. Wolcke, J.; Ullmann, D. Miniaturized HTS technologies -uHTS. Drug Discov Today. 2001, 6, 637-646
60. Yang, C.S.; Lambert, J.D.; Ju, J.; Lu, G.; Sang, S. Tea and cancer prevention: molecular mechanisms and human relevance. Toxicol Appl Pharmacol. 2007, 224, 265-273 (Pubitemid 47592860)
61. Yuan, J.M.; Sun, C.; Butler, L.M. Tea and cancer prevention: epidemiological studies. Pharmacol Res. 2011, 64, 123-135
62. Li, N.; Sun, Z.; Han, C.; Chen, J. The chemopreventive effects of tea on human oral precancerous mucosa lesions. Proc Soc Exp Biol Med. 1999, 220, 218-224
63. Lopez de Cicco, R.; Watson, J.C.; Bassi, D.E.; Litwin, S.; Klein-Szanto, A.J. Simultaneous expression of furin and vascular endothelial growth factor in human oral tongue squamous cell carcinoma progression. Clin Cancer Res. 2004, 10, 4480-4488 (Pubitemid 38878892)