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Over 3 decades of research on dietary flavonoid antioxidants and cancer prevention: What have we achieved?

  • Hajara H. Alfa
  • Randolph R. J. ArrooEmail author
Article
  • 25 Downloads

Abstract

Epidemiological studies keep confirming that the so-called Mediterranean Diet, which is characterised by a relatively high intake of fruit and vegetables, enhances health and provides protection against cancer. The first step in carcinogenesis, and possibly in a range of other degenerative diseases such as heart disease or degenerative dementia, is most likely damage to DNA and other macromolecules. Radical oxygen species—i.e. superoxide anion, hydrogen peroxide, and the hydroxyl radical—are generally considered a major cause of damage to macromolecules. It was long suggested that the antioxidant properties of food ingredients are essential to understanding the mechanism of action of what constitutes a healthy diet, i.e. a diet that prevents the onset of degenerative diseases. However, since the levels of antioxidants in blood plasma required to see any health benefits is much higher that what we get through our diet, the role of dietary phytochemicals acting as anti-oxidants is now in doubt. Nevertheless, a correlation between presence of flavonoids in the diet and prevention of degenerative diseases has remained. Though there is a putative role for dietary flavonoids in the prevention of degenerative diseases, the exact mechanism of action of these phytonutrients is still a matter of debate. The human body has its own defences against oxidative stress in the form of the enzymes superoxide dismutase (SOD) and catalase (CAT), and reduced glutathione (GSH). Rather than being antioxidants in their own right, plant constituents are more likely to act as triggers or inducers of expression of the human antioxidants SOD, CAT, and GSH.

Keywords

Polyphenols Antioxidants Flavonoids Kaempferol Quercetin Oxidative stress 

Notes

Funding

Funding was provided by TETFund (Nigeria).

References

  1. Abdel-Daim MM, Khalifa HA, Abushouk AI, Dkhil MA, Al-Quraishy SA (2017) Diosmin attenuates methotrexate-induced hepatic, renal, and cardiac injury: a biochemical and histopathological study in mice. Oxidative Med Cell Longev. 3281670.  https://doi.org/10.1155/2017/3281670
  2. Abdel-Daim MM, Samak DH, El-Sayed YS, Aleya L, Alarifi S, Alkahtani S (2018) Curcumin and quercetin synergistically attenuate subacute diazinon-induced inflammation and oxidative neurohepatic damage, and acetylcholinesterase inhibition in albino rats. Environ Sci Pollut Res 26(4):3659–3665.  https://doi.org/10.1007/s11356-018-3907-9 Google Scholar
  3. Agbor GA, Vinson JA, Donnelly PE (2014) Folin-ciocalteau reagent for polyphenolic assay. Int J Food Sci Nutr Diet 3(8):147–156.  https://doi.org/10.19070/2326-3350-1400028 Google Scholar
  4. Aksu EH, Kandemir FM, Özkaraca M, Ömür AD, Küçükler S, Çomaklı S (2017) Rutin ameliorates cisplatin-induced reproductive damage via suppression of oxidative stress and apoptosis in adult male rats. Andrologia 49(1):e12593.  https://doi.org/10.1111/and.12593 Google Scholar
  5. Alias Y, Awang K, Hadi AH, Thoison O, Sévenet T, Païs M (1995) An antimitotic and cytotoxic chalcone from Fissistigma lanuginosum. J Nat Prod 58(8):1160–1166Google Scholar
  6. Aloud AA, Veeramani C, Govindasamy C, Alsaif MA, Al-Numair KS (2018) Galangin, a natural flavonoid reduces mitochondrial oxidative damage in streptozotocin-induced diabetic rats. Redox Rep 23(1):29–34.  https://doi.org/10.1080/13510002.2017.1365224 Google Scholar
  7. Ames BN (1983) Dietary carcinogens and anticarcinogens: oxygen radicals and degenerative diseases. Science 221:1256–1263.  https://doi.org/10.1126/science.6351251 Google Scholar
  8. Ames BN, Durston WE, Yamasaki E, Lee FD (1973) Carcinogens are mutagens: a simple test system combining liver homogenates for activation and bacteria for detection. PNAS 70(8):2281–2285.  https://doi.org/10.1073/pnas.70.8.2281 Google Scholar
  9. Arroo RRJ, Beresford KJM, Bhambra AS, Boarder MR, Budriesi R, Cheng Z, Micucci M, Ruparelia KC, Surichan S, Androutsopoulos V (2014) Phytoestrogens as natural prodrugs in cancer prevention: towards a mechanistic model. Phytochem Rev 13(4):853–866.  https://doi.org/10.1007/s11101-014-9355-3 Google Scholar
  10. Balunas MJ, Su B, Brueggemeier RJ, Kinghorn AD (2008) Natural products as aromatase inhibitors. Anticancer Agents Med Chem 8(6):646–682.  https://doi.org/10.2174/187152008785133092 Google Scholar
  11. Bansal Y, Singh R, Saroj P, Sodhi RK, Kuhad A (2018) Naringenin protects against oxido-inflammatory aberrations and altered tryptophan metabolism in olfactory bulbectomized-mice model of depression. Toxicol Appl Pharmacol 355:257–268.  https://doi.org/10.1016/J.TAAP.2018.07.010 Google Scholar
  12. Bauer ME, De la Fuente M (2016) The role of oxidative and inflammatory stress and persistent viral infections in immunosenescence. Mech Ageing Dev 158:27–37.  https://doi.org/10.1016/j.mad.2016.01.001 Google Scholar
  13. Benetou V, Trichopoulou A, Orfanos P, Naska A, Lagiou P, Boffetta P, Trichopoulos D (2008) Conformity to traditional Mediterranean diet and cancer incidence: the Greek EPIC cohort. Br J Cancer 99(1):191–195.  https://doi.org/10.1038/sj.bjc.6604418 Google Scholar
  14. Benzie IFF, Strain JJ (1999) Ferric reducing antioxidant power assay: direct measure of total antioxidant activity of biological fluids and modified version for simultaneous measurement of total antioxidant power and ascorbic acid concentration. Methods Enzymol 299:15–27.  https://doi.org/10.1016/S0076-6879(99)99005-5 Google Scholar
  15. Bonaccio M, Di Castelnuovo A, Costanzo S, Gialluisi A, Persichillo M, Cerletti C, Donati MB, de Gaetano G, Iacoviello L (2018) Mediterranean diet and mortality in the elderly: a prospective cohort study and a meta-analysis. Br J Nutr 120(8):841–854.  https://doi.org/10.1017/s0007114518002179 Google Scholar
  16. Cameron E, Pauling L (1979) Cancer and vitamin C: a discussion of the nature, causes, prevention and treatment of cancer with special reference to the value of vitamin C (2nd extended edition 1993). Camino Books, Philadelphia. ISBN: 0-940159-21-XGoogle Scholar
  17. Cano A, Acosta M, Arnaro MB (2000) A method to measure antioxidant activity in organic media: application to lipophilic vitamins. Redox Rep 5:365–370.  https://doi.org/10.1179/135100000101535933 Google Scholar
  18. Cao GH, Prior RL (1999) Measurement of oxygen radical absorbance capacity in biological samples. Methods Enzymol 299:50–62.  https://doi.org/10.1016/S0076-6879(99)99008-0 Google Scholar
  19. Chen S, Ruan Q, Bedner E, Deptala A, Wang X, Hsieh TC, Traganos F, Darzynkiewicz Z (2001) Effects of the flavonoid baicalin and its metabolite baicalein on androgen receptor expression, cell cycle progression and apoptosis of prostate cancer cell lines. Cell Prolif 34:293–304.  https://doi.org/10.1046/j.0960-7722.2001.00213.x Google Scholar
  20. Chen H, Lu C, Liu H, Wang M, Zhao H, Yan Y, Han L (2017) Quercetin ameliorates imiquimod-induced psoriasis-like skin inflammation in mice via the NF-κB pathway. Int Immunopharmacol 48:110–117.  https://doi.org/10.1016/J.INTIMP.2017.04.022 Google Scholar
  21. Chen Y, Luo HQ, Sun LL, Xu MT, Yu J, Liu LL, Zhang JY, Wang YQ, Wang HX, Bao XF, Meng GL (2018) Dihydromyricetin attenuates myocardial hypertrophy induced by transverse aortic constriction via oxidative stress inhibition and SIRT3 pathway enhancement. Int J Mol Sci 19(9):e2592.  https://doi.org/10.3390/ijms19092592 Google Scholar
  22. Dong HQ, Lin WW, Wu J, Chen TS (2010) Flavonoids activate activate pregnane x receptor-mediated CYP3A4 gene expression by inhibiting cyclin-dependent kinases in HepG2 liver carcinoma cells. BMC Biochem 11:23.  https://doi.org/10.1186/1471-2091-11-23 Google Scholar
  23. Du W, An Y, He X, Zhang D, He W (2018) Protection of kaempferol on oxidative stress-induced retinal pigment epithelial cell damage. Oxidative Med Cell Longev 2018:1–14.  https://doi.org/10.1155/2018/1610751 Google Scholar
  24. Ekinci-Akdemir FN et al (2018) The effects of casticin and myricetin on liver damage induced by methotrexate in rats. Mashhad Univ Med Sci 21(12):1281–1288.  https://doi.org/10.22038/IJBMS.2018.29922.7217 Google Scholar
  25. Eldutar E et al (2017) Restorative effects of Chrysin pretreatment on oxidant-antioxidant status, inflammatory cytokine production, and apoptotic and autophagic markers in acute paracetamol-induced hepatotoxicity in rats: an experimental and biochemical study. J Biochem Mol Toxicol 31(11):e21960.  https://doi.org/10.1002/jbt.21960 Google Scholar
  26. Evelson P, Travacio M, Repetto M (2001) Evaluation of total reactive antioxidant potential (TRAP) of tissue homogenates and their cytosols. Arch Biochem Biophys 388:261–266.  https://doi.org/10.1006/abbi.2001.2292 Google Scholar
  27. Fan X et al (2018) Isoorientin ameliorates APAP-induced hepatotoxicity via activation Nrf2 antioxidative pathway: the involvement of AMPK/Akt/GSK3β. Front Pharmacol 9:1334.  https://doi.org/10.3389/fphar.2018.01334 Google Scholar
  28. Fikry EM, Hasan WA, Mohamed EG (2018) Rutin and meloxicam attenuate paw inflammation in mice: affecting sorbitol dehydrogenase activity. J Biochem Mol Toxicol 32(2):e22029.  https://doi.org/10.1002/jbt.22029 Google Scholar
  29. Finley JW, Kong AN, Hintze KJ, Jeffery EH, Ji LL, Lei XG (2011) Antioxidants in foods: state of the science important to the food industry. J Agric Food Chem 59(13):6837–6846.  https://doi.org/10.1021/jf2013875 Google Scholar
  30. Franceschi C, Campisi J (2014) Chronic inflammation (inflammaging) and its potential contribution to age-associated diseases. J Gerontol A Biol Sci Med Sci 69(Suppl 1):S4–S9.  https://doi.org/10.1093/gerona/glu057 Google Scholar
  31. Fu Y, Hsieh TC, Guo J, Kunicki J, Lee MY, Darzynkiewicz Z, Wu JM (2004) Licochalcone-A, a novel flavonoid isolated from licorice root (Glycyrrhiza glabra), causes G2 and late-G1 arrests in androgen-independent PC-3 prostate cancer cells. Biochem Biophys Res Commun 322(1):263–270.  https://doi.org/10.1016/j.bbrc.2004.07.094 Google Scholar
  32. GISSI-Prevenzione Investigators (1999) Dietary supplementation with n-3 polyunsaturated fatty acids and vitamin E after myocardial infarction: results of the GISSI-Prevenzione trial. Lancet 354:447–455.  https://doi.org/10.1016/S0140-6736(99)07072-5 Google Scholar
  33. Grosso G, Micek A, Godos J, Pajak A, Sciacca S, Galvano F, Giovannucci EL (2017) Dietary flavonoid and lignan intake and mortality in prospective cohort studies: systematic review and dose-response meta-analysis. Am J Epidemiol 185(12):1304–1316.  https://doi.org/10.1093/aje/kww207 Google Scholar
  34. Guo D et al (2018) Orientin and neuropathic pain in rats with spinal nerve ligation. Int Immunopharmacol 58:72–79.  https://doi.org/10.1016/J.INTIMP.2018.03.013 Google Scholar
  35. Guo H, Li M, Xu L-J (2019) Apigetrin treatment attenuates LPS-induced acute otitis media though suppressing inflammation and oxidative stress. Biomed Pharmacother 109:1978–1987.  https://doi.org/10.1016/J.BIOPHA.2018.07.022 Google Scholar
  36. Halliwell B (2000) The antioxidant paradox. Lancet 355:1179–1180.  https://doi.org/10.1016/S0140-6736(00)02075-4 Google Scholar
  37. Halliwell B (2013) The antioxidant paradox: less paradoxical now? Br J Clin Pharmacol 75(3):637–644.  https://doi.org/10.1111/j.1365-2125.2012.04272.x Google Scholar
  38. Han XX, Jiang YP, Liu N, Wu J, Yang JM, Li YX, Sun M, Sun T, Zheng P, Yu JQ (2019) Protective effects of Astragalin on spermatogenesis in streptozotocin induced diabetes in male mice by improving antioxidant activity and inhibiting inflammation. Biomed Pharmacother 110:561–570.  https://doi.org/10.1016/j.biopha.2018.12.012 Google Scholar
  39. Harborne JB, Williams CA (2000) Advances in flavonoid research since 1992. Phytochemistry 55:481–504.  https://doi.org/10.1016/S0031-9422(00)00235-1 Google Scholar
  40. Harman D (1981) The aging process (free radicals/evolution/antioxidants/degenerative diseases/longevity). Proc Natl Acad Sci USA 78(11):7124–7128.  https://doi.org/10.1007/BF02432187 Google Scholar
  41. He Y, Xia Z, Yu D, Wang J, Jin L, Huang D, Ye X, Li X, Zhang B (2019) Hepatoprotective effects and structure-activity relationship of five flavonoids against lipopolysaccharide/d-galactosamine induced acute liver failure in mice. Int Immunopharmacol 68:171–178.  https://doi.org/10.1016/J.INTIMP.2018.12.059 Google Scholar
  42. Huang Y-C et al (2017) Galangin ameliorates cisplatin-induced nephrotoxicity by attenuating oxidative stress, inflammation and cell death in mice through inhibition of ERK and NF-κB signalling. Toxicol Appl Pharmacol 329:128–139.  https://doi.org/10.1016/J.TAAP.2017.05.034 Google Scholar
  43. Jacob RA, Aiello GM, Stephensen CB, Blumberg JB, Milbury PE, Wallock LM, Ames BN (2003) Moderate antioxidant supplementation has no effect on biomarkers of oxidant damage in healthy men with low fruit and vegetable intakes. J Nutr 133(3):740–743.  https://doi.org/10.1093/jn/133.3.740 Google Scholar
  44. Jagan K, Priya CS, Kalpana K, Vidhya R, Anuradha CV (2017) Apigenin attenuates hippocampal oxidative events, inflammation and pathological alterations in rats fed high fat, fructose diet. Biomed Pharmacother 89:323–331.  https://doi.org/10.1016/j.biopha.2017.01.162 Google Scholar
  45. Jones DP (2006) Redefining oxidative stress. Antioxid Redox Signal 8(9, 10):1865–1879.  https://doi.org/10.1089/ars.2006.8.1865 Google Scholar
  46. Kandemir FM et al (2017) Chrysin protects rat kidney from paracetamol-induced oxidative stress, inflammation, apoptosis, and autophagy: a multi-biomarker approach. Sci Pharm 85(1):4.  https://doi.org/10.3390/scipharm85010004 Google Scholar
  47. Kanimozhi S, Bhavani P, Subramanian P (2017) Influence of the flavonoid, quercetin on antioxidant status, lipid peroxidation and histopathological changes in hyperammonemic rats. Indian J Clin Biochem 32(3):275–284.  https://doi.org/10.1007/s12291-016-0603-8 Google Scholar
  48. Khan N, Asim M, Afaq F, Abu Zaid M, Mukhtar H (2008) A novel dietary flavonoid fisetin inhibits androgen receptor signaling and tumor growth in athymic nude mice. Cancer Res 68(20):8555–8563.  https://doi.org/10.1158/0008-5472.CAN-08-0240 Google Scholar
  49. Kheradmand E, Hajizadeh Moghaddam A, Zare M (2018) Neuroprotective effect of hesperetin and nano-hesperetin on recognition memory impairment and the elevated oxygen stress in rat model of Alzheimer’s disease. Biomed Pharmacother 97:1096–1101.  https://doi.org/10.1016/J.BIOPHA.2017.11.047 Google Scholar
  50. Khurana RK, Jain A, Jain A, Sharma T, Singh B, Kesharwani P (2018) Administration of antioxidants in cancer: debate of the decade. Drug Discovery Today 23(4):763–770.  https://doi.org/10.1016/j.drudis.2018.01.021 Google Scholar
  51. Knowles LM, Zigrossi DA, Tauber RA, Hightower C, Milner JA (2000) Flavonoids suppress androgen-independent human prostate tumor proliferation. Nutr Cancer 38(1):116–122.  https://doi.org/10.1207/S15327914NC381_16 Google Scholar
  52. Lei Y (2017) Myricitrin decreases traumatic injury of the spinal cord and exhibits antioxidant and anti-inflammatory activities in a rat model via inhibition of COX-2, TGF-β1, p53 and elevation of Bcl-2/Bax signaling pathway. Mol Med Rep 16(5):7699–7705.  https://doi.org/10.3892/mmr.2017.7567 Google Scholar
  53. Lei L, Yang Y, He HJ, Chen EF, Du L, Dong J, Yang J (2016) Flavan-3-ols consumption and cancer risk: a meta-analysis of epidemiologic studies. Oncotarget 7(45):73573–73592.  https://doi.org/10.18632/oncotarget.12017 Google Scholar
  54. Li S, Coa H, Shen D, Jia Q, Chen C, Xing SL (2018a) Quercetin protects against ox-LDL-induced injury via regulation of ABCAl, LXR-α and PCSK9 in RAW264.7 macrophages. Mol Med Rep 18(1):799–806.  https://doi.org/10.3892/mmr.2018.9048 Google Scholar
  55. Li Y, Ton L, Zhang J, Zhang Y, Zhang F (2018b) Galangin alleviates liver ischemia-reperfusion injury in a rat model by mediating the PI3K/AKT pathway. Cell Physiol Biochem 51(3):1354–1363.  https://doi.org/10.1159/000495553 Google Scholar
  56. Lorenz P, Roychowdhury S, Engelmann M, Wolf G, Horn TFW (2003) Oxyresveratrol and resveratrol are potent antioxidants and free radical scavengers: effect on nitrosative and oxidative stress derived from microglial cells. Nitric Oxide Biol Chem 9(2):64–76.  https://doi.org/10.1016/j.niox.2003.09.005 Google Scholar
  57. Lv P et al (2019) Eriodictyol inhibits high glucose-induced oxidative stress and inflammation in retinal ganglial cells. J Cell Biochem 120(4):5644–5651.  https://doi.org/10.1002/jcb.27848 Google Scholar
  58. Manach C, Williamson G, Morand C, Scalbert A, Rémésy C (2005) Bioavailability and bioefficacy of polyphenols in humans. I. Review of 97 bioavailability studies. Am J Clin Nutr 81(suppl):230S–242S.  https://doi.org/10.1093/ajcn/81.1.230s Google Scholar
  59. Mohana Kumara P, Soujanya KN, Ravikanth G, Vasudeva R, Ganeshaiah KN, Uma Shaanker R (2014) Rohitukine, a chromone alkaloid and a precursor of flavopiridol, isproduced by endophytic fungi isolated from Dysoxylum binectariferum Hook.f and Amoora rohituka (Roxb).Wight & Arn. Phytomedicine 21(4):541–546.  https://doi.org/10.1016/j.phymed.2013.09.019 Google Scholar
  60. Nkpaa KW, Onyeso GI (2018) Rutin attenuates neurobehavioral deficits, oxidative stress, neuro-inflammation and apoptosis in fluoride treated rats. Neurosci Lett 682:92–99.  https://doi.org/10.1016/J.NEULET.2018.06.023 Google Scholar
  61. Ou B, Huang D, Hampsch-Woodill M, Flanagan JA, Deemer EK (2002) Analysis of antioxidant activities of common vegetables employing oxygen radical absorbance capacity (ORAC) and ferric reducing antioxidant power (FRAP) assays: a comparative study. J Agric Food Chem 50:3122–3128.  https://doi.org/10.1021/jf0116606 Google Scholar
  62. Pauling L (1970) Vitamin C and the common cold, 1st edn. WH Freeman, San FranciscoGoogle Scholar
  63. Pauling L (1986) How to live longer and feel better. WH Freeman, New YorkGoogle Scholar
  64. Priyadarsini RV, Nagini S (2012) Quercetin suppresses cytochrome P450 mediated ROS generation and NF-κB activation to inhibit the development of 7,12-dimethylbenz[a]anthracene (DMBA) induced hamster buccal pouch carcinomas. Free Radic Res 46(1):41–49.  https://doi.org/10.3109/10715762.2011.637204 Google Scholar
  65. Rezabakhsh A et al (2019) Quercetin alleviates high glucose-induced damage on human umbilical vein endothelial cells by promoting autophagy. Phytomedicine 56:183–193.  https://doi.org/10.1016/J.PHYMED.2018.11.008 Google Scholar
  66. Rozmer Z, Perjési P (2016) Naturally occurring chalcones and their biological activities. Phytochem Rev 15:87–120.  https://doi.org/10.1007/s11101-014-9387-8 Google Scholar
  67. Safia Kamil M, Jadiya P, Sheikh S, Haque E, Nazir A, Lakshmi V, Mir SS (2015) The chromone alkaloid, rohitukine, affords anti-cancer activity via modulating apoptosis pathways in A549 cell line and yeast mitogen activated protein kinase (MAPK) pathway. PLoS ONE 10(9):e0137991.  https://doi.org/10.1371/journal.pone.0137991 Google Scholar
  68. Samie A, Sedaghar R, Baluchnejadmojarad T, Roghani M (2018) Hesperetin, a citrus flavonoid, attenuates testicular damage in diabetic rats via inhibition of oxidative stress, inflammation, and apoptosis. Life Sci 210:132–139.  https://doi.org/10.1016/J.LFS.2018.08.074 Google Scholar
  69. Sanada F, Taniyama Y, Muratsu J, Otsu R, Shimizu H, Rakugi H, Morishita R (2018) Source of chronic inflammation in aging. Front Cardiovasc Med 5:12.  https://doi.org/10.3389/fcvm.2018.00012 Google Scholar
  70. Sharifzadeh M, Ranjbar A, Hosseini A, Khanavi M (2017) The effect of green tea extract on oxidative stress and spatial learning in streptozotocin-diabetic rats. Iranian J Pharm Res 16(1):201–209Google Scholar
  71. Sharma OP, Bhat TK (2009) DPPH antioxidant assay revisited. Food Chem 113:1202–1205.  https://doi.org/10.1016/j.foodchem.2008.08.008 Google Scholar
  72. Sherif IO (2018) Uroprotective mechanism of quercetin against cyclophosphamide-induced urotoxicity: effect on oxidative stress and inflammatory markers. J Cell Biochem 119(9):7441–7448.  https://doi.org/10.1002/jcb.27053 Google Scholar
  73. Singh S et al (2018) Rutin restricts hydrogen peroxide-induced alterations by up-regulating the redox-system: an in vitro, in vivo and in silico study. Eur J Pharmacol 835:115–125.  https://doi.org/10.1016/J.EJPHAR.2018.07.055 Google Scholar
  74. Singh S et al (2019) Rutin protects t-butyl hydroperoxide-induced oxidative impairment via modulating the Nrf2 and iNOS activity. Phytomedicine 55:92–104.  https://doi.org/10.1016/J.PHYMED.2018.07.009 Google Scholar
  75. Sreerama YN, Sashikala VB, Pratape VM (2010) Variability in the distribution of phenolic compounds in milled fractions of chickpea and horse gram: evaluation of their antioxidant properties. J Agric Food Chem 58:8322–8330.  https://doi.org/10.1021/jf101335r Google Scholar
  76. Stahl W, Sies H (2003) Antioxidant activity of carotenoids. Mol Aspects Med 24:345–351.  https://doi.org/10.1016/S0098-2997(03)00030-X Google Scholar
  77. Sun C, Wei J, Bi L (2017a) Rutin attenuates oxidative stress and proinflammatory cytokine level in adjuvant induced rheumatoid arthritis via inhibition of NF-κB. Pharmacology 100(1–2):40–49.  https://doi.org/10.1159/000451027 Google Scholar
  78. Sun L et al (2017b) Myricetin against ischemic cerebral injury in rat middle cerebral artery occlusion model. Mol Med Rep 17(2):3274–3280.  https://doi.org/10.3892/mmr.2017.8212 Google Scholar
  79. Taha H, Arya A, Paydar M, Looi CY, Wong WF, Vasudeva Murthy CR, Noordin MI, Ali HM, Mustafa AM, Hadi AH (2014) Upregulation of insulin secretion and downregulation of pro-inflammatory cytokines, oxidative stress and hyperglycemia in STZ-nicotinamide-induced type 2 diabetic rats by Pseuduvaria monticola bark extract. Food Chem Toxicol 66:295–306.  https://doi.org/10.1016/j.fct.2014.01.054 Google Scholar
  80. Thangaiyan R, Robert BM, Arjunan S, Govindasamy K, Nagarajan RP (2018) Preventive effect of apigenin against isoproterenol-induced apoptosis in cardiomyoblasts. J Biochem Mol Toxicol 32(11):e22213.  https://doi.org/10.1002/jbt.22213 Google Scholar
  81. Treml J, Šmejkal K (2016) Flavonoids as potent scavengers of hydroxyl radicals. Compr Rev Food Sci Food Saf 15:720–738.  https://doi.org/10.1111/1541-4337.12204 Google Scholar
  82. Tsai M-S et al (2018) Kaempferol protects against propacetamol-induced acute liver injury through CYP2E1 inactivation, UGT1A1 activation, and attenuation of oxidative stress, inflammation and apoptosis in mice. Toxicol Lett 290:97–109.  https://doi.org/10.1016/J.TOXLET.2018.03.024 Google Scholar
  83. Umukoro S, Kalejaye HA, Ben-Azu B, Ajayi AM (2018) Naringenin attenuates behavioral derangements induced by social defeat stress in mice via inhibition of acetylcholinesterase activity, oxidative stress and release of pro-inflammatory cytokines. Biomed Pharmacother 105:714–723.  https://doi.org/10.1016/J.BIOPHA.2018.06.016 Google Scholar
  84. Vance TM, Su J, Fontham ETH, Koo SI, Chun OK (2013) Dietary antioxidants and prostate cancer: a review. Nutr Cancer 65(6):793–801.  https://doi.org/10.1080/01635581.2013.806672 Google Scholar
  85. Wang J, Ferruzzi MG, Ho L, Blount J, Janle EM, Gong B, Pan Y, Nagana Gowda GA, Raftery D, Arrieta-Cruz I, Sharma V, Cooper B, Lobo J, Simon JE, Zhang C, Cheng A, Qian X, Ono K, Teplow DB, Pavlides C, Dixon RA, Pasinetti GM (2012) Brain-targeted proanthocyanidin metabolites for Alzheimer’s disease treatment. J Neurosci 32:5144–5150.  https://doi.org/10.1523/JNEUROSCI.6437-11.2012 Google Scholar
  86. Wang Z, Lan Y, Chen M, Wen C, Hu Y, Liu Z, Ye L (2017) Eriodictyol, not its glucuronide metabolites, attenuates acetaminophen-induced hepatotoxicity. Mol Pharm 14:2937–2951.  https://doi.org/10.1021/acs.molpharmaceut.7b00345 Google Scholar
  87. WCRF/AICR (2018) Diet, nutrition, physical activity and cancer: a global perspective. Continuous update project. Third expert report. www.dietandcancerreport.org. Accessed 12 July 2019
  88. Wei C-B, Tao K, Jiang R, Zhou L-D, Zhang Q-H, Yuan C-S (2017) Quercetin protects mouse liver against triptolide-induced hepatic injury by restoring Th17/Treg balance through Tim-3 and TLR4-MyD88-NF-κB pathway. Int Immunopharmacol 53:73–82Google Scholar
  89. Yao ZH, Yao XL, Zhang Y, Zhang SF, Hu JC (2018) Luteolin could improve cognitive dysfunction by inhibiting neuroinflammation. Neurochem Res 43:806–820.  https://doi.org/10.1007/s11064-018-2482-2 Google Scholar
  90. Zamora-Ros R, Touillaud M, Rothwell JA, Romieu I, Scalbert A (2014) Measuring exposure to the polyphenol metabolome in observational epidemiologic studies: current tools and applications and their limits. Am J Clin Nutr 100(1):11–26.  https://doi.org/10.3945/ajcn.113.077743 Google Scholar
  91. Zhang M, Wang K, Chen L, Yin B, Song Y (2016) Is phytoestrogen intake associated with decreased risk of prostate cancer? A systematic review of epidemiological studies based on 17,546 cases. Andrology 4(4):745–756.  https://doi.org/10.1111/andr.12196 Google Scholar
  92. Zhang R, Ai X, Duan Y, Xue M, He W, Wang C, Xu T, Xu M, Liu B, Li C, Wang Z, Zhang R, Wang G, Tian S, Liu H (2017) Kaempferol ameliorates H9N2 swine influenza virus-induced acute lung injury by inactivation of TLR4/MyD88-mediated NF-κB and MAPK signaling pathways. Biomed Pharmacother 89:660–672Google Scholar
  93. Zhao L, Zhang N, Yang D, Yang M, Guo X, He J, Wu W, Ji B, Cheng Q, Zhou F (2018) Protective effects of five structurally diverse flavonoid subgroups against chronic alcohol-induced hepatic damage in a mouse model. Nutrients 10:1754.  https://doi.org/10.3390/nu10111754 Google Scholar
  94. Zhu M, Zhou X, Zhao J (2017) Quercetin prevents alcohol-induced liver injury through targeting of PI3K/Akt/nuclear factor-κB and STAT3 signaling pathway. Exp Ther Med 14:6169–6175.  https://doi.org/10.3892/etm.2017.5329 Google Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Leicester School of PharmacyDe Montfort UniversityLeicesterUK
  2. 2.Faculty of Natural SciencesIBB UniversityLapaiNigeria

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