Antioxidative and Antidiabetic Effects of Natural Polyphenols and Isoflavones

Aya Umeno, Masanori Horie, Kazutoshi Murotomi, Yoshihiro Nakajima, Yasukazu Yoshida, Aya Umeno, Masanori Horie, Kazutoshi Murotomi, Yoshihiro Nakajima, Yasukazu Yoshida

Abstract

Many polyphenols that contain more than two phenolic hydroxyl groups are natural antioxidants and can provide health benefits to humans. These polyphenols include, for example, oleuropein, hydroxytyrosol, catechin, chlorogenic acids, hesperidin, nobiletin, and isoflavones. These have been studied widely because of their strong radical-scavenging and antioxidative effects. These effects may contribute to the prevention of diseases, such as diabetes. Insulin secretion, insulin resistance, and homeostasis are important factors in the onset of diabetes, a disease that is associated with dysfunction of pancreatic β-cells. Oxidative stress is thought to contribute to this dysfunction and the effects of antioxidants on the pathogenesis of diabetes have, therefore, been investigated. Here, we summarize the antioxidative effects of polyphenols from the perspective of their radical-scavenging activities as well as their effects on signal transduction pathways. We also describe the preventative effects of polyphenols on diabetes by referring to recent studies including those reported by us. Appropriate analytical approaches for evaluating antioxidants in studies on the prevention of diabetes are comprehensively reviewed.

Keywords: catechin; chlorogenic acids; diabetes; glucose tolerance; hesperidin; hydroxytyrosol; insulin secretion; isoflavone; oleuropein; oxidative stress.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Assessment of (a) amount of radicals scavenged by antioxidant (stoichiometric number of antioxidants (n)) and (b) the effectiveness of radical-scavenging (RIH).
Figure 2
Figure 2
The preventative effect of polyphenol at each stage of diabetes.

References

    1. Butler A.E., Janson J., Bonner-Weir S., Ritzel R., Rizza R.A., Butler P.C. Beta-cell deficit and increased beta-cell apoptosis in humans with type 2 diabetes. Diabetes. 2003;52:102–110. doi: 10.2337/diabetes.52.1.102.
    1. Polonsky K.S. Dynamics of insulin secretion in obesity and diabetes. Int. J. Obes. Relat. Metab. Disord. 2000;24(Suppl. 2):S29–S31. doi: 10.1038/sj.ijo.0801273.
    1. Lenzen S., Drinkgern J., Tiedge M. Low antioxidant enzyme gene expression in pancreatic islets compared with various other mouse tissues. Free Radic. Biol. Med. 1996;20:463–466. doi: 10.1016/0891-5849(96)02051-5.
    1. Ogawa Y., Saito Y., Nishio K., Yoshida Y., Ashida H., Niki E. Gamma-tocopheryl quinone, not alpha-tocopheryl quinone, induces adaptive response through up-regulation of cellular glutathione and cysteine availability via activation of ATF4. Free Radic. Res. 2008;42:674–687. doi: 10.1080/10715760802277396.
    1. Foti M.C. Use and Abuse of the DPPH (•) Radical. J. Agric. Food Chem. 2015;63:8765–8776. doi: 10.1021/acs.jafc.5b03839.
    1. Amorati R., Valgimigli L. Advantages and limitations of common testing methods for antioxidants. Free Radic. Res. 2015;49:633–649. doi: 10.3109/10715762.2014.996146.
    1. Yang J., Ou B., Wise M.L., Chu Y. In vitro total antioxidant capacity and anti-inflammatory activity of three common oat-derived avenanthramides. Food Chem. 2014;160:338–345. doi: 10.1016/j.foodchem.2014.03.059.
    1. Takahashi S., Iwasaki-Kino Y., Aizawa K., Terao J., Mukai K. Development of Singlet Oxygen Absorption Capacity (SOAC) Assay Method Using a Microplate Reader. J. AOAC Int. 2016;99:193–197. doi: 10.5740/jaoacint.15-0165.
    1. Niki E. Assessment of antioxidant capacity in vitro and in vivo. Free Radic. Biol. Med. 2010;49:503–515. doi: 10.1016/j.freeradbiomed.2010.04.016.
    1. Takashima M., Horie M., Shichiri M., Hagihara Y., Yoshida Y., Niki E. Assessment of antioxidant capacity for scavenging free radicals in vitro: A rational basis and practical application. Free Radic. Biol. Med. 2012;52:1242–1252. doi: 10.1016/j.freeradbiomed.2012.01.010.
    1. Takashima M., Shichiri M., Hagihara Y., Yoshida Y., Niki E. Reactivity toward oxygen radicals and antioxidant action of thiol compounds. Biofactors. 2012;38:240–248. doi: 10.1002/biof.1014.
    1. Miller H.E. A simplified method for the evaluation of antioxidants. J. Am. Oil Chem. Soc. 1971;48:91. doi: 10.1007/BF02635693.
    1. Lissi E., Pascual C., del Castillo M.D. On the use of the quenching of luminol luminescence to evaluate SOD activity. Free Radic. Biol. Med. 1994;16:833–837. doi: 10.1016/0891-5849(94)90200-3.
    1. Peskin A.V., Winterbourn C.C. A microtiter plate assay for superoxide dismutase using a water-soluble tetrazolium salt (WST-1) Clin. Chim. Acta. 2000;293:157–166. doi: 10.1016/S0009-8981(99)00246-6.
    1. Sutherland M.W., Learmonth B.A. The tetrazolium dyes MTS and XTT provide new quantitative assays for superoxide and superoxide dismutase. Free Radic. Res. 1997;27:283–289. doi: 10.3109/10715769709065766.
    1. Diczfalusy U. Analysis of cholesterol oxidation products in biological samples. J. AOAC Int. 2004;87:467–473.
    1. Erickson S.K., Cooper A.D., Matsui S.M., Gould R.G. 7-Ketocholesterol. Its effects on hepatic cholesterogenesis and its hepatic metabolism in vivo and in vitro. J. Biol. Chem. 1977;252:5186–5193.
    1. Song W., Pierce W.M., Jr., Saeki Y., Redinger R.N., Prough R.A. Endogenous 7-oxocholesterol is an enzymatic product: Characterization of 7α--hydroxycholesterol dehydrogenase activity of hamster liver microsomes. Arch. Biochem. Biophys. 1996;328:272–282. doi: 10.1006/abbi.1996.0173.
    1. Brown A.J., Jessup W. Oxysterols and atherosclerosis. Atherosclerosis. 1999;142:1–28. doi: 10.1016/S0021-9150(98)00196-8.
    1. Yoshida Y., Umeno A., Shichiri M. Lipid peroxidation biomarkers for evaluating oxidative stress and assessing antioxidant capacity in vivo. J. Clin. Biochem. Nutr. 2013;52:9–16. doi: 10.3164/jcbn.12-112.
    1. Yoshida Y., Yoshikawa A., Kinumi T., Ogawa Y., Saito Y., Ohara K., Yamamoto H., Imai Y., Niki E. Hydroxyoctadecadienoic acid and oxidatively modified peroxiredoxins in the blood of Alzheimer’s disease patients and their potential as biomarkers. Neurobiol. Aging. 2009;30:174–185. doi: 10.1016/j.neurobiolaging.2007.06.012.
    1. Umeno A., Shichiri M., Ishida N., Hashimoto Y., Abe K., Kataoka M., Yoshino K., Hagihara Y., Aki N., Funaki M., et al. Singlet Oxygen Induced Products of Linoleates, 10-and 12-(Z,E)-Hydroxyoctadecadienoic Acids (HODE), Can Be Potential Biomarkers for Early Detection of Type 2 Diabetes. PLoS ONE. 2013;8:e63542. doi: 10.1371/journal.pone.0063542.
    1. Umeno A., Yoshino K., Hashimoto Y., Shichiri M., Kataoka M., Yoshida Y. Multi-biomarkers for early detection of type 2 diabetes, including 10- and 12-(Z,E)-hydroxyoctadecadienoic acids, insulin, leptin, and adiponectin. PLoS ONE. 2015;10:e0130971. doi: 10.1371/journal.pone.0130971.
    1. Yoshida Y., Umeno A., Akazawa Y., Shichiri M., Murotomi K., Horie M. Chemistry of lipid peroxidation products and their use as biomarkers in early detection of diseases. J. Oleo Sci. 2015;64:347–356. doi: 10.5650/jos.ess14281.
    1. Soriguer F., Rojo-Martínez G., Goday A., Bosch-Comas A., Bordiú E., Caballero-Díaz F., Calle-Pascual A., Carmena R., Casamitjana R., Castaño L., et al. Olive oil has a beneficial effect on impaired glucose regulation and other cardiometabolic risk factors. Di@bet.es study. Eur. J. Clin. Nutr. 2013;67:911–916. doi: 10.1038/ejcn.2013.130.
    1. Sleiman D., Al-Badri M.R., Azar S.T. Effect of mediterranean diet in diabetes control and cardiovascular risk modification: A systematic review. Front. Public Health. 2015;3:69. doi: 10.3389/fpubh.2015.00069.
    1. Guasch-Ferré M., Hruby A., Salas-Salvadó J., Martínez-González M.A., Sun Q., Willett W.C., Hu F.B. Olive oil consumption and risk of type 2 diabetes in US women. Am. J. Clin. Nutr. 2015;102:479–486. doi: 10.3945/ajcn.115.112029.
    1. Roche E., Ramírez-Tortosa C.L., Arribas M.I., Ochoa J.J., Sirvent-Belando J.E., Battino M., Ramírez-Tortosa M.C., González-Alonso A., Pérez-López M.P., Quiles J.L. Comparative analysis of pancreatic changes in aged rats fed life long with sunflower, fish, or olive oils. J. Gerontol. A Biol. Sci. Med. Sci. 2014;69:934–944. doi: 10.1093/gerona/glt157.
    1. Martínez-González M.A., Salas-Salvadó J., Estruch R., Corella D., Fitó M., Ros E. Benefits of the Mediterranean Diet: Insights from the PREDIMED Study. Prog. Cardiovasc. Dis. 2015;58:50–60. doi: 10.1016/j.pcad.2015.04.003.
    1. Schwingshackl L., Hoffmann G. Monounsaturated fatty acids, olive oil and health status: A systematic review and meta-analysis of cohort studies. Lipids Health Dis. 2014;13:154. doi: 10.1186/1476-511X-13-154.
    1. Medina I., Satué-Gracia M.T., German J.B., Frankel E.N. Comparison of natural polyphenol antioxidants from extra virgin olive oil with synthetic antioxidants in tuna lipids during thermal oxidation. J. Agric. Food Chem. 1999;47:4873–4879. doi: 10.1021/jf990188+.
    1. Pellegrini N., Visioli F., Buratti S., Brighenti F. Direct analysis of total antioxidant activity of olive oil and studies on the influence of heating. J. Agric. Food Chem. 2001;49:2532–2538. doi: 10.1021/jf001418j.
    1. Zoidou E., Melliou E., Gikas E., Tsarbopoulos A., Magiatis P., Skaltsounis A.L. Identification of Throuba Thassos, a traditional Greek table olive variety, as a nutritional rich source of oleuropein. J. Agric. Food Chem. 2010;58:46–50. doi: 10.1021/jf903405e.
    1. Ortega-García F., Blanco S., Peinado M.A., Peragón J. Polyphenol oxidase and its relationship with oleuropein concentration in fruits and leaves of olive (Olea europaea) cv. ‘Picual’ trees during fruit ripening. Tree Physiol. 2008;28:45–54. doi: 10.1093/treephys/28.1.45.
    1. Susalit E., Agus N., Effendi I., Tjandrawinata R.R., Nofiarny D., Perrinjaquet-Moccetti T., Verbruggen M. Olive (Olea europaea) leaf extract effective in patients with stage-1 hypertension: Comparison with Captopril. Phytomedicine. 2011;18:251–258. doi: 10.1016/j.phymed.2010.08.016.
    1. Petroni M.L., Jazrawi R.P., Grundy A., Lanzin I.A., Pigozzi M.G., Biasio A., Heaton K.W., Virjee J., Northfield T.C. Prospective, multicenter study on value of computerized tomography (CT) in gallstone disease in predicting response to bile acid therapy. Dig. Dis. Sci. 1995;40:1956–1962. doi: 10.1007/BF02208664.
    1. Misra A., Singhal N., Khurana L. Obesity, the metabolic syndrome, and type 2 diabetes in developing countries: Role of dietary fats and oils. J. Am. Coll. Nutr. 2010;29(Suppl. 3):289S–301S. doi: 10.1080/07315724.2010.10719844.
    1. Hamdi H.K., Castellon R. Oleuropein, a non-toxic olive iridoid, is an anti-tumor agent and cytoskeleton disruptor. Biochem. Biophys. Res. Commun. 2005;334:769–778. doi: 10.1016/j.bbrc.2005.06.161.
    1. Santiago-Mora R., Casado-Díaz A., de Castro M.D., Quesada-Gómez J.M. Oleuropein enhances osteoblastogenesis and inhibits adipogenesis: The effect on differentiation in stem cells derived from bone marrow. Osteoporos. Int. 2011;22:675–684. doi: 10.1007/s00198-010-1270-x.
    1. Efentakis P., Iliodromitis E.K., Mikros E., Papachristodoulou A., Dagres N., Skaltsounis A.L., Andreadou I. Effects of the olive tree leaf constituents on myocardial oxidative damage and atherosclerosis. Planta Med. 2015;81:648–654. doi: 10.1055/s-0035-1546017.
    1. Corona G., Tzounis X., Assunta Dessì M., Deiana M., Debnam E., Visioli F., Spencer J.P. The fate of olive oil polyphenols in the gastrointestinal tract: Implications of gastric and colonic microflora-dependent biotransformation. Free Radic. Res. 2006;40:647–658. doi: 10.1080/10715760500373000.
    1. Granados-Principal S., Quiles J.L., Ramirez-Tortosa C., Camacho-Corencia P., Sanchez-Rovira P., Vera-Ramirez L., Ramirez-Tortosa M.C. Hydroxytyrosol inhibits growth and cell proliferation and promotes high expression of sfrp4 in rat mammary tumours. Mol. Nutr. Food Res. 2011;55:S117–S126. doi: 10.1002/mnfr.201000220.
    1. Mateos R., Martínez-López S., Baeza Arévalo G., Amigo-Benavent M., Sarriá B., Bravo-Clemente L. Hydroxytyrosol in functional hydroxytyrosol-enriched biscuits is highly bioavailable and decreases oxidised low density lipoprotein levels in humans. Food Chem. 2016;205:248–256. doi: 10.1016/j.foodchem.2016.03.011.
    1. Granados-Principal S., El-Azem N., Pamplona R., Ramirez-Tortosa C., Pulido-Moran M., Vera-Ramirez L., Quiles J.L., Sanchez-Rovira P., Naudí A., Portero-Otin M., et al. Hydroxytyrosol ameliorates oxidative stress and mitochondrial dysfunction in doxorubicin-induced cardiotoxicity in rats with breast cancer. Biochem. Pharmacol. 2014;90:25–33. doi: 10.1016/j.bcp.2014.04.001.
    1. Zheng A., Li H., Cao K., Xu J., Zou X., Li Y., Chen C., Liu J., Feng Z. Maternal hydroxytyrosol administration improves neurogenesis and cognitive function in prenatally stressed offspring. J. Nutr. Biochem. 2015;26:190–199. doi: 10.1016/j.jnutbio.2014.10.006.
    1. Bullon P., Quiles J.L., Morillo J.M., Rubini C., Goteri G., Granados-Principal S., Battino M., Ramirez-Tortosa M. Gingival vascular damage in atherosclerotic rabbits: Hydroxytyrosol and squalene benefits. Food Chem. Toxicol. 2009;47:2327–2331. doi: 10.1016/j.fct.2009.06.026.
    1. Incani A., Deiana M., Corona G., Vafeiadou K., Vauzour D., Dessì M.A., Spencer J.P. Involvement of ERK, Akt and JNK signalling in H2O2-induced cell injury and protection by hydroxytyrosol and its metabolite homovanillic alcohol. Mol. Nutr. Food Res. 2010;54:788–796. doi: 10.1002/mnfr.200900098.
    1. Deiana M., Corona G., Incani A., Loru D., Rosa A., Atzeri A., Paola Melis M., Assunta Dessì M. Protective effect of simple phenols from extravirgin olive oil against lipid peroxidation in intestinal Caco-2 cells. Food Chem. Toxicol. 2010;48:3008–3016. doi: 10.1016/j.fct.2010.07.041.
    1. Sgarbossa A., Dal Bosco M., Pressi G., Cuzzocrea S., Dal Toso R., Menegazz I.M. Phenylpropanoid glycosides from plant cell cultures induce heme oxygenase 1 gene expression in a human keratinocyte cell line by affecting the balance of NRF2 and BACH1 transcription factors. Chem. Biol. Interact. 2012;199:87–95. doi: 10.1016/j.cbi.2012.06.006.
    1. Valavanidis A., Nisiotou C., Papageorgiou Y., Kremli I., Satravelas N., Zinieris N., Zygalaki H. Comparison of the radical scavenging potential of polar and lipidic fractions of olive oil and other vegetable oils under normal conditions and after thermal treatment. J. Agric. Food Chem. 2004;52:2358–2365. doi: 10.1021/jf030491h.
    1. Rietjens S.J., Bast A., Haenen G.R. New insights into controversies on the antioxidant potential of the olive oil antioxidant hydroxytyrosol. J. Agric. Food Chem. 2007;55:7609–7614. doi: 10.1021/jf0706934.
    1. Umeno A., Takashima M., Murotomi K., Nakajima Y., Koike T., Matsuo T., Yoshida Y. Radical-scavenging activity and antioxidative effects of olive leaf components oleuropein and hydroxytyrosol in comparison with homovanillic alcohol. J. Oleo Sci. 2015;64:793–800. doi: 10.5650/jos.ess15042.
    1. Murotomi K., Umeno A., Yasunaga M., Shichiri M., Ishida N., Koike T., Matsuo T., Abe H., Yoshida Y., Nakajima Y. Oleuropein-rich diet attenuates hyperglycemia and impaired glucose tolerance in type 2 diabetes model mouse. J. Agric. Food Chem. 2015;63:6715–6722. doi: 10.1021/acs.jafc.5b00556.
    1. Matsuzaki T., Hara Y. Antioxidative activity of tea leaf catechins. Nippon Nogeikagaku Kaishi. 1985;59:129–134. doi: 10.1271/nogeikagaku1924.59.129.
    1. Sano M., Tabata M., Suzuki M., Degawa M., Miyase T., Maeda-Yamamoto M. Simultaneous determination of twelve tea catechins by high-performance liquid chromatography with electrochemical detection. Analyst. 2001;126:816–820. doi: 10.1039/b102541b.
    1. Nishizawa C., Nguyen V.C. The Comparison between Coffee and Teas on Desmutagenicity, Radical Scavenging Activity and Antioxidative Activity. Nippon Shokuhin Kagaku Kogaku Kaishi. 2001;48:533–538. doi: 10.3136/nskkk.48.533.
    1. Pullikotil P., Chen H., Muniyappa R., Greenberg C.C., Yang S., Reiter C.E., Lee J.W., Chung J.H., Quon M.J. Epigallocatechin gallate induces expression of heme oxygenase-1 in endothelial cells via p38 MAPK and Nrf-2 that suppresses proinflammatory actions of TNF-α. J. Nutr. Biochem. 2012;23:1134–1145. doi: 10.1016/j.jnutbio.2011.06.007.
    1. Sahin K., Tuzcu M., Gencoglu H., Dogukan A., Timurkan M., Sahin N., Aslan A., Kucuk O. Epigallocatechin-3-gallate activates Nrf2/HO-1 signaling pathway in cisplatin-induced nephrotoxicity in rats. Life Sci. 2010;87:240–245. doi: 10.1016/j.lfs.2010.06.014.
    1. Romeo L., Intrieri M., D’Agata V., Mangano N.G., Oriani G., Ontario M.L., Scapagnini G. The major green tea polyphenol, (−)-epigallocatechin-3-gallate, induces heme oxygenase in rat neurons and acts as an effective neuroprotective agent against oxidative stress. Am. Coll. Nutr. 2009;28:492S–499S. doi: 10.1080/07315724.2009.10718116.
    1. Shin D.W., Kim S.N., Lee S.M., Lee W., Song M.J., Park S.M., Lee T.R., Baik J.H., Kim H.K., Hong J.H., et al. (−)-Catechin promotes adipocyte differentiation in human bone marrow mesenchymal stem cells through PPARγ transactivation. Biochem. Pharmacol. 2009;77:125–133. doi: 10.1016/j.bcp.2008.09.033.
    1. Takahashi M., Miyashita M., Suzuki K., Bae S.R., Kim H.K., Wakisaka T., Matsui Y., Takeshita M., Yasunaga K. Acute ingestion of catechin-rich green tea improves postprandial glucose status and increases serum thioredoxin concentrations in postmenopausal women. Br. J. Nutr. 2014;112:1542–1550. doi: 10.1017/S0007114514002530.
    1. Subramanian N., Venkatesh P., Ganguli S., Sinkar V.P. Role of polyphenol oxidase and peroxidase in the generation of black tea theaflavins. J. Agric. Food Chem. 1999;47:2571–2578. doi: 10.1021/jf981042y.
    1. Stodt U.W., Blauth N., Niemann S., Stark J., Pawar V., Jayaraman S., Koek J., Engelhardt U.H. Investigation of processes in black tea manufacture through model fermentation (oxidation) experiments. J. Agric. Food Chem. 2014;62:7854–7861. doi: 10.1021/jf501591j.
    1. Maron D.J., Lu G.P., Cai N.S., Wu Z.G., Li Y.H., Chen H., Zhu J.Q., Jin X.J., Wouters B.C., Zhao J. Cholesterol-lowering effect of a theaflavin-enriched green tea extract: A randomized controlled trial. Arch. Intern. Med. 2003;163:1448–1453. doi: 10.1001/archinte.163.12.1448.
    1. Miyata Y., Tamaru S., Tanaka T., Tamaya K., Matsui T., Nagata Y., Tanaka K. Theflavins and theasinensin A derived from fermented tea have antihyperglycemic and hypotriacylglycerolemic effects in KK-A(y) mice and Sprague-Dawley rats. J. Agric. Food Chem. 2013;61:9366–9372. doi: 10.1021/jf400123y.
    1. Satoh T., Igarashi M., Yamada S., Takahashi N., Watanabe K. Inhibitory effect of black tea and its combination with acarbose on small intestinal α-glucosidase activity. J. Ethnopharmacol. 2015;161:147–155. doi: 10.1016/j.jep.2014.12.009.
    1. Rodríguez-Ramiro I., Ramos S., Bravo L., Goya L., Martín M.Á. Procyanidin B2 and a cocoa polyphenolic extract inhibit acrylamide-induced apoptosis in human Caco-2 cells by preventing oxidative stress and activation of JNK pathway. J. Nutr. Biochem. 2011;22:1186–1194. doi: 10.1016/j.jnutbio.2010.10.005.
    1. Oboh G., Ademosun A.O., Ademiluyi A.O., Omojokun O.S., Nwanna E.E., Longe K.O. In Vitro studies on the antioxidant property and inhibition of α-amylase, α-glucosidase, and angiotensin I-converting enzyme by polyphenol-rich extracts from cocoa (theobroma cacao) bean. Pathol. Res. Int. 2014;2014:549287. doi: 10.1155/2014/549287.
    1. Mellor D.D., Sathyapalan T., Kilpatrick E.S., Beckett S., Atkin S.L. High-cocoa polyphenol-rich chocolate improves HDL cholesterol in Type 2 diabetes patients. Diabet. Med. 2010;27:1318–1321. doi: 10.1111/j.1464-5491.2010.03108.x.
    1. Mellor D.D., Madden L.A., Smith K.A., Kilpatrick E.S., Atkin S.L. High-polyphenol chocolate reduces endothelial dysfunction and oxidative stress during acute transient hyperglycaemia in Type 2 diabetes: A pilot randomized controlled trial. Diabet. Med. 2013;30:478–483. doi: 10.1111/dme.12030.
    1. Kameya H., Ukai M. Hydroxyl Radical Scavenging Ability of Instant Coffee Evaluated by ESR Spin Trapping. J. Cook. Sci. Jpn. 2012;45:33–36.
    1. Predes F.S., Ruiz A.L., Carvalho J.E., Foglio M.A., Dolder H. Antioxidative and in vitro antiproliferative activity of Arctium lappa root extracts. BMC Complement. Altern. Med. 2011;11:25. doi: 10.1186/1472-6882-11-25.
    1. Sueishi Y., Hori M., Ishikawa M., Matsu-Ura K., Kamogawa E., Honda Y., Kita M., Ohara K. Scavenging rate constants of hydrophilic antioxidants against multiple reactive oxygen species. J. Clin. Biochem. Nutr. 2014;54:67–74. doi: 10.3164/jcbn.13-53.
    1. Laranjinha J.A., Almeida L.M., Madeira V.M. Reactivity of dietary phenolic acids with peroxyl radicals: Antioxidant activity upon low density lipoprotein peroxidation. Biochem. Pharmacol. 1994;48:487–494. doi: 10.1016/0006-2952(94)90278-X.
    1. Tang Y.Z., Liu Z.Q. Chemical kinetic behavior of chlorogenic acid in protecting erythrocyte and DNA against radical-induced oxidation. J. Agric. Food Chem. 2008;56:11025–11029. doi: 10.1021/jf802462h.
    1. Kamitani Y., Iwai K., Fukunaga T., Kimura R., Nakagiri O. In vitro Analysis on Inhibitory Activity of Amylolytic Enzymes in Decaffeinated Green Coffee Bean Extracts and Contributions of Chlorogenic Acids. Nippon Shokuhin Kagaku Kogaku Kaishi. 2009;56:336–342. doi: 10.3136/nskkk.56.336.
    1. Ota N., Soga S., Murase T., Shimotoyodome A., Hase T. Consumption of Coffee Polyphenols Increases Fat Utilization in Humans. J. Health Sci. 2010;56:745–751. doi: 10.1248/jhs.56.745.
    1. Jokura H., Watanabe I., Umeda M., Hase T., Shimotoyodome A. Coffee polyphenol consumption improves postprandial hyperglycemia associated with impaired vascular endothelial function in healthy male adults. Nutr. Res. 2015;35:873–881. doi: 10.1016/j.nutres.2015.07.005.
    1. Nagao T., Ochiai R., Watanabe T., Kataoka K., Komikado M., Tokimitsu I., Tsuchida T. Visceral Fat-reducing Effect of Continuous Coffee Beverage Consumption in Obese Subjects. Jpn. Pharmacol. Ther. 2009;37:333–344.
    1. Wan C.W., Wong C.N., Pin W.K., Wong M.H., Kwok C.Y., Chan R.Y., Yu P.H., Chan S.W. Chlorogenic acid exhibits cholesterol lowering and fatty liver attenuating properties by up-regulating the gene expression of PPAR-α in hypercholesterolemic rats induced with a high-cholesterol diet. Phytother. Res. 2013;27:545–551. doi: 10.1002/ptr.4751.
    1. Li S.Y., Chang C.Q., Ma F.Y., Yu C.L. Modulating effects of chlorogenic acid on lipids and glucose metabolism and expression of hepatic peroxisome proliferator-activated receptor-alpha in golden hamsters fed on high fat diet. Biomed. Environ. Sci. 2009;22:122–129. doi: 10.1016/S0895-3988(09)60034-9.
    1. Hirata A., Murakami Y., Shoji M., Kadoma Y., Fujisawa S. Kinetics of radical-scavenging activity of hesperetin and hesperidin and their inhibitory activity on COX-2 expression. Anticancer. Res. 2005;25:3367–3374.
    1. Emim J.A., Oliveira A.B., Lapa A.J. Pharmacological evaluation of the anti-inflammatory activity of a citrus bioflavonoid, hesperidin, and the isoflavonoids, duartin and claussequinone, in rats and mice. J. Pharm. Pharmacol. 1994;46:118–122. doi: 10.1111/j.2042-7158.1994.tb03753.x.
    1. Akiyama S., Katsumata S., Suzuki K., Nakaya Y., Ishimi Y., Uehara M. Hypoglycemic and hypolipidemic effects of hesperidin and cyclodextrin-clathrated hesperetin in Goto-Kakizaki rats with type 2 diabetes. Biosci. Biotechnol. Biochem. 2009;73:2779–2782. doi: 10.1271/bbb.90576.
    1. Jung U.J., Lee M.K., Jeong K.S., Choi M.S. The hypoglycemic effects of hesperidin and naringin are partly mediated by hepatic glucose-regulating enzymes in C57BL/KsJ-db/db mice. J. Nutr. 2004;134:2499–2503.
    1. Kakadiya J., Mulani H., Shah N. Protective effect of hesperidin on cardiovascular complication in experimentally induced myocardial infarction in diabetes in rats. J. Basic. Clin. Pharm. 2010;1:85–91.
    1. Monforte M.T., Trovato A., Kirjavainen S., Forestieri A.M., Galati E.M., Lo Curto R.B. Biological effects of hesperidin, a Citrus flavonoid. (note II): Hypolipidemic activity on experimental hypercholesterolemia in rat. Farmaco. 1995;50:595–599.
    1. Agrawal Y.O., Sharma P.K., Shrivastava B., Ojha S., Upadhya H.M., Arya D.S., Goyal S.N. Hesperidin produces cardioprotective activity via PPAR-γ pathway in ischemic heart disease model in diabetic rats. PLoS ONE. 2014;9:e111212. doi: 10.1371/journal.pone.0111212.
    1. Kadota K., Semba K., Shakudo R., Sato H., Deki Y., Shirakawa Y., Tozuka Y. Inhibition of photodegradation of highly dispersed folic acid nanoparticles by the antioxidant effect of transglycosylated rutin. J. Agric. Food Chem. 2016;64:3062–3069. doi: 10.1021/acs.jafc.6b00334.
    1. Miwa Y., Mitsuzumi H., Yamada M., Arai N., Tanabe F., Okada K., Kubota M., Chaen H., Sunayama T., Kibata M. Suppression of apolipoprotein B secretion from HepG2 cells by glucosyl hesperidin. J. Nutr. Sci. Vitaminol. 2006;52:223–231. doi: 10.3177/jnsv.52.223.
    1. Miwa Y., Mitsuzumi H., Sunayama T., Yamada M., Okada K., Kubota M., Chaen H., Mishima Y., Kibata M. Glucosyl hesperidin lowers serum triglyceride level in hypertriglyceridemic subjects through the improvement of very low-density lipoprotein metabolic abnormality. J. Nutr. Sci. Vitaminol. 2005;51:460–470. doi: 10.3177/jnsv.51.460.
    1. Miwa Y., Yamada M., Sunayama T., Mitsuzumi H., Tsuzaki Y., Chaen H., Mishima Y., Kibata M. Effects of glucosyl hesperidin on serum lipids in hyperlipidemic subjects: Preferential reduction in elevated serum triglyceride level. J. Nutr. Sci. Vitaminol. 2004;50:211–218. doi: 10.3177/jnsv.50.211.
    1. Murakami A., Nakamura Y., Ohto Y., Yano M., Koshiba T., Koshimizu K., Tokuda H., Nishino H., Ohigashi H. Suppressive effects of citrus fruits on free radical generation and nobiletin, an anti-inflammatory polymethoxyflavonoid. Biofactors. 2000;12:187–192. doi: 10.1002/biof.5520120130.
    1. Mulvihill E.E., Assini J.M., Lee J.K., Allister E.M., Sutherland B.G., Koppes J.B., Sawyez C.G., Edwards J.Y., Telford D.E., Charbonneau A., et al. Nobiletin attenuates VLDL overproduction, dyslipidemia, and atherosclerosis in mice with diet-induced insulin resistance. Diabetes. 2011;60:1446–1457. doi: 10.2337/db10-0589.
    1. Nii Y., Okahisa N., Takata J., Mino Y., Shikishima Y. Sudachitin Contents and Antioxidative Activities of Sudachi Peel Extracts. Rep. Tokushima Prefect. Ind. Technol. Cent. 2014;23:15–19.
    1. Tsutsumi R., Yoshida T., Nii Y., Okahisa N., Iwata S., Tsukayama M., Hashimoto R., Taniguchi Y., Sakaue H., Hosaka T., et al. Sudachitin, a polymethoxylated flavone, improves glucose and lipid metabolism by increasing mitochondrial biogenesis in skeletal muscle. Nutr. Metab. 2014;11:32. doi: 10.1186/1743-7075-11-32.
    1. Miyake Y., Mochizuki M., Okada M., Hiramitsu M., Morimitsu Y., Osawa T. Isolation of antioxidative phenolic glucosides from lemon juice and their suppressive effect on the expression of blood adhesion molecules. Biosci. Biotechnol. Biochem. 2007;71:1911–1919. doi: 10.1271/bbb.70115.
    1. Minato K., Miyake Y., Fukumoto S., Yamamoto K., Kato Y., Shimomura Y., Osawa T. Lemon flavonoid, eriocitrin, suppresses exercise-induced oxidative damage in rat liver. Life Sci. 2003;72:1609–1616. doi: 10.1016/S0024-3205(02)02443-8.
    1. Fritz H., Seely D., Flower G., Skidmore B., Fernandes R., Vadeboncoeur S., Kennedy D., Cooley K., Wong R., Sagar S., et al. Soy, red clover, and isoflavones and breast cancer: A systematic review. PLoS ONE. 2013;8:e81968.
    1. Han R.M., Tian Y.X., Liu Y., Chen C.H., Ai X.C., Zhang J.P., Skibsted L.H. Comparison of flavonoids and isoflavonoids as antioxidants. J. Agric. Food Chem. 2009;57:3780–3785. doi: 10.1021/jf803850p.
    1. Zhang T., Wang F., Xu H.X., Yi L., Qin Y., Chang H., Mi M.T., Zhang Q.Y. Activation of nuclear factor erythroid 2-related factor 2 and PPARγ plays a role in the genistein-mediated attenuation of oxidative stress-induced endothelial cell injury. Br. J. Nutr. 2013;109:223–235. doi: 10.1017/S0007114512001110.
    1. Takashima M., Nara K., Niki E., Yoshida Y., Hagihara Y., Stowe M., Horie M. Evaluation of biological activities of a groundnut (Apios americana Medik) extract containing a novel isoflavone. Food Chem. 2013;138:298–305. doi: 10.1016/j.foodchem.2012.10.100.
    1. Ko K.P., Kim C.S., Ahn Y., Park S.J., Kim Y.J., Park J.K., Lim Y.K., Yoo K.Y., Kim S.S. Plasma isoflavone concentration is associated with decreased risk of type 2 diabetes in Korean women but not men: Results from the Korean Genome and Epidemiology Study. Diabetologia. 2015;58:726–735. doi: 10.1007/s00125-014-3463-x.

Source: PubMed

3
구독하다