Naringenin, a dietary flavanone, enhances insulin-like growth factor 1 receptor-mediated antioxidant defense and attenuates methylglyoxal-induced neurite damage and apoptotic death

References

• Pham VM, Tu NH, Katano T, et al. Impaired peripheral nerve regeneration in type-2 diabetic mouse model. Eur J Neurosci. 2018;47(2):126–39. doi: 10.1111/ejn.13771
   PubMed Web of Science ®Google Scholar
• Athauda D, Foltynie T. Insulin resistance and Parkinson’s disease: a new target for disease modification? Prog Neurobiol. 2016;145-146:98–120. doi: 10.1016/j.pneurobio.2016.10.001
   PubMed Web of Science ®Google Scholar
• Allaman I, Belanger M, Magistretti PJ. Methylglyoxal, the dark side of glycolysis. Front Neurosci. 2015;9:23–35. doi: 10.3389/fnins.2015.00023
   PubMed Web of Science ®Google Scholar
• Di Loreto S, Zimmitti V, Sebastiani P, et al. Methylglyoxal causes strong weakening of detoxifying capacity and apoptotic cell death in rat hippocampal neurons. Int J Biochem Cell Biol. 2008;40(2):245–57. doi: 10.1016/j.biocel.2007.07.019
   PubMed Web of Science ®Google Scholar
• Di Loreto S, Caracciolo V, Colafarina S, et al. Methylglyoxal induces oxidative stress-dependent cell injury and up-regulation of interleukin-10 and nerve growth factor in cultured hippocampal neuronal cells. Brain Res. 2004;1006(2):157–67. doi: 10.1016/j.brainres.2004.01.066
   PubMed Web of Science ®Google Scholar
• Shinpo K, Kikuchi S, Sasaki H, et al. Selective vulnerability of spinal motor neurons to reactive dicarbonyl compounds, intermediate products of glycation, in vitro: implication of inefficient glutathione system in spinal motor neurons. Brain Res. 2000;861(1):151–9. doi: 10.1016/S0006-8993(00)02047-3
   PubMed Web of Science ®Google Scholar
• Fiory F, Lombardi A, Miele C, et al. Methylglyoxal impairs insulin signalling and insulin action on glucose-induced insulin secretion in the pancreatic beta cell line INS-1E. Diabetologia. 2011;54(11):2941–52. doi: 10.1007/s00125-011-2280-8
   PubMed Web of Science ®Google Scholar
• Navarro I, Leibush B, Moon TW, et al. Insulin, insulin-like growth factor-I (IGF-I) and glucagon: the evolution of their receptors. Comp Biochem Physiol B Biochem Mol Biol. 1999;122(2):137–53. doi: 10.1016/S0305-0491(98)10163-3
   PubMed Web of Science ®Google Scholar
• Bassil F, Fernagut PO, Bezard E, et al. Insulin, IGF-1 and GLP-1 signaling in neurodegenerative disorders: targets for disease modification? Prog Neurobiol. 2014;118:1–18. doi: 10.1016/j.pneurobio.2014.02.005
   PubMed Web of Science ®Google Scholar
• Tseng YH, Ueki K, Kriauciunas KM, et al. Differential roles of insulin receptor substrates in the anti-apoptotic function of insulin-like growth factor-1 and insulin. J Biol Chem. 2002;277(35):31601–11. doi: 10.1074/jbc.M202932200
   PubMed Web of Science ®Google Scholar
• Ozdinler P, Macklis J. IGF-I specifically enhances axon outgrowth of corticospinal motor neurons. Nat Neurosci. 2006;9(11):1371–81. doi: 10.1038/nn1789
   PubMed Web of Science ®Google Scholar
• Hsu YY, Tseng YT, Lo YC. Berberine, a natural antidiabetes drug, attenuates glucose neurotoxicity and promotes Nrf2-related neurite outgrowth. Toxicol Appl Pharmacol. 2013;272(3):787–96. doi: 10.1016/j.taap.2013.08.008
   PubMed Web of Science ®Google Scholar
• Assini JM, Mulvihill EE, Huff MW. Citrus flavonoids and lipid metabolism. Curr Opin Lipidol. 2013;24(1):34–40. doi: 10.1097/MOL.0b013e32835c07fd
   PubMed Web of Science ®Google Scholar
• Ren B, Qin W, Wu F, et al. Apigenin and naringenin regulate glucose and lipid metabolism, and ameliorate vascular dysfunction in type 2 diabetic rats. Eur J Pharmacol. 2016;773:13–23. doi: 10.1016/j.ejphar.2016.01.002
   PubMed Web of Science ®Google Scholar
• Wang K, Chen Z, Huang J, et al. Naringenin prevents ischaemic stroke damage via anti-apoptotic and anti-oxidant effects. Clin Exp Pharmacol Physiol. 2017;44(8):862–71. doi: 10.1111/1440-1681.12775
   PubMed Web of Science ®Google Scholar
• Wang K, Chen Z, Huang L, et al. Naringenin reduces oxidative stress and improves mitochondrial dysfunction via activation of the Nrf2/ARE signaling pathway in neurons. Int J Mol Med. 2017;40(5):1582–90. doi: 10.3892/ijmm.2017.3134
   PubMed Web of Science ®Google Scholar
• Al-Dosari DI, Ahmed MM, Al-Rejaie SS, et al. Flavonoid naringenin attenuates oxidative stress, apoptosis and Improves neurotrophic effects in the diabetic Rat Retina. Nutrients. 2017;9(10):1161–1174. doi: 10.3390/nu9101161
   PubMed Web of Science ®Google Scholar
• Singh AK, Raj V, Keshari AK, et al. Isolated mangiferin and naringenin exert antidiabetic effect via PPARgamma/GLUT4 dual agonistic action with strong metabolic regulation. Chem Biol Interact. 2018;280:33–44. doi: 10.1016/j.cbi.2017.12.007
   PubMed Web of Science ®Google Scholar
• Lou H, Jing X, Wei X, et al. Naringenin protects against 6-OHDA-induced neurotoxicity via activation of the Nrf2/ARE signaling pathway. Neuropharmacology. 2014;79:380–8. doi: 10.1016/j.neuropharm.2013.11.026
   PubMed Web of Science ®Google Scholar
• M SS, C, DN. Influence of quercetin, naringenin and berberine on glucose transporters and insulin signalling molecules in brain of streptozotocin-induced diabetic rats. Biomed Pharmacother. 2017;94:605–11. doi: 10.1016/j.biopha.2017.07.142
   PubMed Web of Science ®Google Scholar
• Hsu YY, Jong YJ, Tsai HH, et al. Triptolide increases transcript and protein levels of survival motor neurons in human SMA fibroblasts and improves survival in SMA-like mice. Br J Pharmacol. 2012;166(3):1114–26. doi: 10.1111/j.1476-5381.2012.01829.x
   PubMed Web of Science ®Google Scholar
• Wang J, Chang T. Methylglyoxal content in drinking coffee as a cytotoxic factor. J Food Sci. 2010;75(6):H167–71. doi: 10.1111/j.1750-3841.2010.01658.x
   PubMed Web of Science ®Google Scholar
• Arribas-Lorenzo G, Morales FJ. Analysis, distribution, and dietary exposure of glyoxal and methylglyoxal in cookies and their relationship with other heat-induced contaminants. J Agric Food Chem. 2010;58(5):2966–72. doi: 10.1021/jf902815p
   PubMed Web of Science ®Google Scholar
• Vafeiadou K, Vauzour D, Lee HY, et al. The citrus flavanone naringenin inhibits inflammatory signalling in glial cells and protects against neuroinflammatory injury. Arch Biochem Biophys. 2009;484(1):100–9. doi: 10.1016/j.abb.2009.01.016
   PubMed Web of Science ®Google Scholar
• Nyane NA, Tlaila TB, Malefane TG, et al. Metformin-like antidiabetic, cardio-protective and non-glycemic effects of naringenin: molecular and pharmacological insights. Eur J Pharmacol. 2017;803:103–11. doi: 10.1016/j.ejphar.2017.03.042
   PubMed Web of Science ®Google Scholar
• Thilakarathna SH, Rupasinghe HP. Flavonoid bioavailability and attempts for bioavailability enhancement. Nutrients. 2013;5(9):3367–87. doi: 10.3390/nu5093367
   PubMed Web of Science ®Google Scholar
• Heo HJ, Kim D-O, Shin SC, et al. Effect of antioxidant flavanone, naringenin, from citrus junos on neuroprotection. J Agric Food Chem. 2004;52(6):1520–25. doi: 10.1021/jf035079g
   PubMed Web of Science ®Google Scholar
• Mercer LD, Kelly BL, Horne MK, et al. Dietary polyphenols protect dopamine neurons from oxidative insults and apoptosis: investigations in primary rat mesencephalic cultures. Biochem Pharmacol. 2005;69(2):339–45. doi: 10.1016/j.bcp.2004.09.018
   PubMed Web of Science ®Google Scholar
• Hua FZ, Ying J, Zhang J, et al. Naringenin pre-treatment inhibits neuroapoptosis and ameliorates cognitive impairment in rats exposed to isoflurane anesthesia by regulating the PI3/Akt/PTEN signalling pathway and suppressing NF-kappaB-mediated inflammation. Int J Mol Med. 2016;38(4):1271–80. doi: 10.3892/ijmm.2016.2715
   PubMed Web of Science ®Google Scholar
• Tseng YT, Chen CS, Jong YJ, et al. Loganin possesses neuroprotective properties, restores SMN protein and activates protein synthesis positive regulator Akt/mTOR in experimental models of spinal muscular atrophy. Pharmacol Res. 2016;111:58–75. doi: 10.1016/j.phrs.2016.05.023
   PubMed Web of Science ®Google Scholar
• Gao QG, Xie JX, Wong MS, et al. IGF-I receptor signaling pathway is involved in the neuroprotective effect of genistein in the neuroblastoma SK-N-SH cells. Eur J Pharmacol. 2012;677(1-3):39–46. doi: 10.1016/j.ejphar.2011.12.032
   PubMed Web of Science ®Google Scholar
• Xue M, Rabbani N, Momiji H, et al. Transcriptional control of glyoxalase 1 by Nrf2 provides a stress-responsive defence against dicarbonyl glycation. Biochem J. 2012;443(1):213–22. doi: 10.1042/BJ20111648
   PubMed Web of Science ®Google Scholar
• Prathapan A, Varghese MV, Abhilash S, et al. Polyphenol rich ethanolic extract from Boerhavia diffusa L. mitigates angiotensin II induced cardiac hypertrophy and fibrosis in rats. Biomed Pharmacother. 2017;87:427–36. doi: 10.1016/j.biopha.2016.12.114
   PubMed Web of Science ®Google Scholar
• Poulose SM, Bielinski DF, Carey A, et al. Modulation of oxidative stress, inflammation, autophagy and expression of Nrf2 in hippocampus and frontal cortex of rats fed with acai-enriched diets. Nutr Neurosci. 2017;20(5):305–15. doi: 10.1080/1028415X.2015.1125654
   PubMed Web of Science ®Google Scholar
• Yu ZW, Li D, Ling WH, et al. Role of nuclear factor (erythroid-derived 2)-like 2 in metabolic homeostasis and insulin action: a novel opportunity for diabetes treatment? World J Diabetes. 2012;3(1):19–28. doi: 10.4239/wjd.v3.i1.19
   PubMedGoogle Scholar
• Koike S, Nishimoto S, Ogasawara Y. Cysteine persulfides and polysulfides produced by exchange reactions with H2S protect SH-SY5Y cells from methylglyoxal-induced toxicity through Nrf2 activation. Redox Biol. 2017;12:530–9. doi: 10.1016/j.redox.2017.03.020
   PubMed Web of Science ®Google Scholar
• de Oliveira MR, Ferreira GC, Schuck PF, et al. Role for the PI3 K/Akt/Nrf2 signaling pathway in the protective effects of carnosic acid against methylglyoxal-induced neurotoxicity in SH-SY5Y neuroblastoma cells. Chem Biol Interact. 2015;242:396–406. doi: 10.1016/j.cbi.2015.11.003
   PubMed Web of Science ®Google Scholar
• Wang Z, Xiong L, Wang G, et al. Insulin-like growth factor-1 protects SH-SY5Y cells against beta-amyloid-induced apoptosis via the PI3K/Akt-Nrf2 pathway. Exp Gerontol. 2017;87(Pt A):23–32. doi: 10.1016/j.exger.2016.11.009
   PubMedGoogle Scholar
• Nishimoto S, Koike S, Inoue N, et al. Activation of Nrf2 attenuates carbonyl stress induced by methylglyoxal in human neuroblastoma cells: increase in GSH levels is a critical event for the detoxification mechanism. Biochem Biophys Res Commun. 2017;483(2):874–9. doi: 10.1016/j.bbrc.2017.01.024
   PubMed Web of Science ®Google Scholar
• Gu F, Chauhan V, Chauhan A. Glutathione redox imbalance in brain disorders. Curr Opin Clin Nutr Metab Care. 2015;18(1):89–95. doi: 10.1097/MCO.0000000000000134
   PubMed Web of Science ®Google Scholar
• Chang T, Wang R, Wu L. Methylglyoxal-induced nitric oxide and peroxynitrite production in vascular smooth muscle cells. Free Radic Biol Med. 2005;38(2):286–93. doi: 10.1016/j.freeradbiomed.2004.10.034
   PubMed Web of Science ®Google Scholar
• Orrego-Lagaron N, Martinez-Huelamo M, Vallverdu-Queralt A, et al. High gastrointestinal permeability and local metabolism of naringenin: influence of antibiotic treatment on absorption and metabolism. Br J Nutr. 2015;114(2):169–80. doi: 10.1017/S0007114515001671
   PubMed Web of Science ®Google Scholar
• Orrego-Lagaron N, Martinez-Huelamo M, Quifer-Rada P, et al. Absorption and disposition of naringenin and quercetin after simultaneous administration via intestinal perfusion in mice. Food Funct. 2016;7(9):3880–9. doi: 10.1039/C6FO00633G
   PubMed Web of Science ®Google Scholar