Supplementation of lycopene attenuates oxidative stress induced neuroinflammation and cognitive impairment via Nrf2/NF-κB transcriptional pathway

Food and Chemical Toxicology

Volumn 109, Issue , 2017, Pages 505-516

  Zhao, Beita ^a   Ren, Bo ^a   Guo, Rui ^a   Zhang, Wentong ^a   Ma, Shaobo ^a   Yao, Yuchen ^a   Yuan, Tian ^a   Liu, Zhigang ^a   Liu, Xuebo ^a  

^a NORTHWEST A F UNIVERSITY   (China)

Author keywords

Cognitive impairment; Lycopene; Neuroinflammation; Nrf2 NF B transcriptional pathway; Oxidative stress

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CALCIUM ION; CELL MARKER; CYTOKINE; GALACTOSE; GLIAL FIBRILLARY ACIDIC PROTEIN; HEME OXYGENASE 1; HYDROGEN PEROXIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; IONIZED CALCIUM BINDING ADAPTOR MOLECULE 1; LYCOPENE; MESSENGER RNA; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE); REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE) 1; TRANSCRIPTION FACTOR NRF2; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; CAROTENOID; NEUROPROTECTIVE AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; CD-1 MOUSE; CELL DAMAGE; CHRONIC DISEASE; COGNITIVE DEFECT; CONTROLLED STUDY; DOWN REGULATION; DRUG MECHANISM; ENZYME ACTIVATION; ENZYME ACTIVITY; GLIA CELL; HIPPOCAMPUS; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; LOCOMOTION; MALE; MORRIS WATER MAZE TEST; MOUSE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; OXIDATIVE STRESS; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; SH-SY5Y CELL LINE; SIGNAL TRANSDUCTION; VITAMIN SUPPLEMENTATION; Y-MAZE TEST; ANIMAL; DRUG EFFECTS; GENETICS; HUMAN; MAZE TEST; METABOLISM; NERVE CELL; PSYCHOLOGY;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CAROTENOIDS; COGNITIVE DYSFUNCTION; HIPPOCAMPUS; HUMANS; INTERLEUKIN-1BETA; MALE; MAZE LEARNING; MICE; NEURONS; NEUROPROTECTIVE AGENTS; NF-E2-RELATED FACTOR 2; NF-KAPPA B; OXIDATIVE STRESS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 85030674525     PISSN: 02786915     EISSN: 18736351     Source Type: Journal    
DOI: 10.1016/j.fct.2017.09.050     Document Type: Article

References (54)

1. Akbaraly, T.N., Hamer, M., Ferrie, J.E., Lowe, G., Batty, G.D., Hagger-Johnson, G., Singh-Manoux, A., Shipley, M.J., Kivimäki, M., Chronic inflammation as a determinant of future aging phenotypes. Can. Med. Assoc. J. 185 (2013), E763–E770.
2. Akiyama, H., Barger, S., Barnum, S., Bradt, B., Bauer, J., Cole, G.M., Cooper, N.R., Eikelenboom, P., Emmerling, M., Fiebich, B.L., Inflammation and Alzheimer's disease. Neurobiol. Aging 21 (2000), 383–421.
3. Allison, D.J., Ditor, D.S., The common inflammatory etiology of depression and cognitive impairment: a therapeutic target. J. Neuroinflammation, 11, 2014, 151.
4. Banji, O.J., Banji, D., Ch, K., Curcumin and hesperidin improve cognition by suppressing mitochondrial dysfunction and apoptosis induced by D-galactose in rat brain. Food Chem. Toxicol. 74 (2014), 51–59.
5. Bao, Q., Pan, J., Qi, H., Wang, L., Qian, H., Jiang, F., Shao, Z., Xu, F., Tao, Z., Ma, Q., Aging and age-related diseases–from endocrine therapy to target therapy. Mol. Cell Endocrinol. 394 (2014), 115–118.
6. Buendia, I., Michalska, P., Navarro, E., Gameiro, I., Egea, J., León, R., Nrf2–ARE pathway: an emerging target against oxidative stress and neuroinflammation in neurodegenerative diseases. Pharmacol. Ther. 157 (2016), 84–104.
7. Calabrese, V., Cornelius, C., Cuzzocrea, S., Iavicoli, I., Rizzarelli, E., Calabrese, E.J., Hormesis, cellular stress response and vitagenes as critical determinants in aging and longevity. Mol. Asp. Med. 32 (2011), 279–304.
8. Christen, Y., Oxidative stress and Alzheimer disease. Am. J. Clin. Nutr., 71, 2000 621s-629s.
9. Chung, H.Y., Sung, B., Jung, K.J., Zou, Y., Yu, B.P., The molecular inflammatory process in aging. Antioxid. Redox Signal 8 (2006), 572–581.
10. Cui, X., Zuo, P., Zhang, Q., Li, X., Hu, Y., Long, J., Packer, L., Liu, J., Chronic systemic D-galactose exposure induces memory loss, neurodegeneration, and oxidative damage in mice: protective effects of R-α-lipoic acid. J. Neurosci. Res. 83 (2006), 1584–1590.
11. Dai, J.-N., Zong, Y., Zhong, L.-M., Li, Y.-M., Zhang, W., Bian, L.-G., Ai, Q.-L., Liu, Y.-D., Sun, J., Lu, D., Gastrodin inhibits expression of inducible NO synthase, cyclooxygenase-2 and proinflammatory cytokines in cultured LPS-stimulated microglia via MAPK pathways. PLoS One, 6, 2011, e21891.
12. Greilberger, J., Koidl, C., Greilberger, M., Lamprecht, M., Schroecksnadel, K., Leblhuber, F., Fuchs, D., Oettl, K., Malondialdehyde, carbonyl proteins and albumin-disulphide as useful oxidative markers in mild cognitive impairment and Alzheimer's disease. Free Radic. Res. 42 (2008), 633–638.
13. Gropper, S.S., Weese, S.J.O., West, P.A., Gross, K.C., Free galactose content of fresh fruits and strained fruit and vegetable baby foods: more foods to consider for the galactose-restricted diet. J. Am. Diet. Assoc. 100 (2000), 573–575.
14. Harper, M.E., Bevilacqua, L., Hagopian, K., Weindruch, R., Ramsey, J.J., Ageing, oxidative stress, and mitochondrial uncoupling. Acta Physiol. Scand. 182 (2004), 321–331.
15. Heneka, M.T., Carson, M.J., El Khoury, J., Landreth, G.E., Brosseron, F., Feinstein, D.L., Jacobs, A.H., Wyss-Coray, T., Vitorica, J., Ransohoff, R.M., Neuroinflammation in Alzheimer's disease. Lancet Neurol. 14 (2015), 388–405.
16. Hock, C., Heese, K., Hulette, C., Rosenberg, C., Otten, U., Region-specific neurotrophin imbalances in Alzheimer disease: decreased levels of brain-derived neurotrophic factor and increased levels of nerve growth factor in hippocampus and cortical areas. Arch. Neurol. 57 (2000), 846–851.
17. Hsieh, H.-M., Wu, W.-M., Hu, M.-L., Soy isoflavones attenuate oxidative stress and improve parameters related to aging and Alzheimer's disease in C57BL/6J mice treated with D-galactose. Food Chem. Toxicol. 47 (2009), 625–632.
18. Jain, C.K., Agarwal, S., Rao, A.V., The effect of dietary lycopene on bioavailability, tissue distribution, in vivo antioxidant properties and colonic preneoplasia in rats. Nutr. Res. 19 (1999), 1383–1391.
19. Kaminska, B., MAPK signalling pathways as molecular targets for anti-inflammatory therapy-from molecular mechanisms to therapeutic benefits. Biochim. Biophys. Acta 1754 (2005), 253–262.
20. Karasek, M., Melatonin, human aging, and age-related diseases. Exp. Gerontol. 39 (2004), 1723–1729.
21. Lee, W., Ku, S.-K., Bae, J.W., Bae, J.-S., Inhibitory effects of lycopene on HMGB1-mediated pro-inflammatory responses in both cellular and animal models. Food Chem. Toxicol. 50 (2012), 1826–1833.
22. Lei, M., Su, Y., Hua, X., Ding, J., Han, Q., Hu, G., Xiao, M., Chronic systemic injection of D-galactose impairs the septohippocampal cholinergic system in rats. Neuroreport 19 (2008), 1611–1615.
23. Lei, X., Lei, L., Zhang, Z., Cheng, Y., Neuroprotective effects of lycopene pretreatment on transient global cerebral ischemia-reperfusion in rats: the role of the Nrf2/HO-1 signaling pathway. Mol. Med. Rep. 13 (2016), 412–418.
24. Li, W., Nie, S., Peng, X., Liu, X., Li, C., Chen, Y., Li, J., Song, W., Xie, M., Ganoderma atrum polysaccharide improves age-related oxidative stress and immune impairment in mice. J. Agric. Food Chem. 60 (2012), 1413–1418.
25. Li, W., Nie, S., Xie, M., Yu, Q., Chen, Y., He, M., Ganoderma atrum polysaccharide attenuates oxidative stress induced by D-galactose in mouse brain. Life Sci. 88 (2011), 713–718.
26. Li, Z., Zhang, Z., Zhang, J., Jia, J., Ding, J., Luo, R., Liu, Z., Cordyceps militaris extract attenuates D-galactose-induced memory impairment in mice. J. Med. Food 15 (2012), 1057–1063.
27. Lin, M.T., Beal, M.F., Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 443 (2006), 787–795.
28. Liu, Z., Chen, Y., Qiao, Q., Sun, Y., Liu, Q., Ren, B., Liu, X., Sesamol supplementation prevents systemic inflammation-induced memory impairment and amyloidogenesis via inhibition of nuclear factor kappaB. Mol. Nutr. Food Res., 2016, 10.1002/mnfr.201600734.
29. Lu, J., Wu, D., Zheng, Y., Hu, B., Zhang, Z., Ye, Q., Liu, C., Shan, Q., Wang, Y., Ursolic acid attenuates D-galactose-induced inflammatory response in mouse prefrontal cortex through inhibiting AGEs/RAGE/NF-κB pathway activation. Cereb. Cortex 20 (2010), 2540–2548.
30. Marchesi, V.T., Alzheimer's dementia begins as a disease of small blood vessels, damaged by oxidative-induced inflammation and dysregulated amyloid metabolism: implications for early detection and therapy. FASEB J. 25 (2011), 5–13.
31. Marcotorchino, J., Romier, B., Gouranton, E., Riollet, C., Gleize, B., Malezet-Desmoulins, C., Landrier, J.F., Lycopene attenuates LPS-induced TNF-α secretion in macrophages and inflammatory markers in adipocytes exposed to macrophage-conditioned media. Mol. Nutr. Food Res. 56 (2012), 725–732.
32. Min, J.-y., Min, K.-b., Serum lycopene, lutein and zeaxanthin, and the risk of Alzheimer's disease mortality in older adults. Dement. Geriatr. Cogn. Disord. 37 (2013), 246–256.
33. Mortensen, A., Carotenoids and other pigments as natural colorants. Pure Appl. Chem. 78 (2006), 1477–1491.
34. Nagahara, A.H., Merrill, D.A., Coppola, G., Tsukada, S., Schroeder, B.E., Shaked, G.M., Wang, L., Blesch, A., Kim, A., Conner, J.M., Neuroprotective effects of brain-derived neurotrophic factor in rodent and primate models of Alzheimer's disease. Nat. Med. 15 (2009), 331–337.
35. Palozza, P., Simone, R., Catalano, A., Monego, G., Barini, A., Mele, M.C., Parrone, N., Trombino, S., Picci, N., Ranelletti, F.O., Lycopene prevention of oxysterol-induced proinflammatory cytokine cascade in human macrophages: inhibition of NF-κB nuclear binding and increase in PPARγ expression. J. Nutr. Biochem. 22 (2011), 259–268.
36. Peng, S., Garzon, D.J., Marchese, M., Klein, W., Ginsberg, S.D., Francis, B.M., Mount, H.T., Mufson, E.J., Salehi, A., Fahnestock, M., Decreased brain-derived neurotrophic factor depends on amyloid aggregation state in transgenic mouse models of Alzheimer's disease. J. Neurosci. 29 (2009), 9321–9329.
37. Poulose, S.M., Fisher, D.R., Larson, J., Bielinski, D.F., Rimando, A.M., Carey, A.N., Schauss, A.G., Shukitt-Hale, B., Anthocyanin-rich açai (Euterpe oleracea Mart.) fruit pulp fractions attenuate inflammatory stress signaling in mouse brain BV-2 microglial cells. J. Agr. Food Chem. 60 (2012), 1084–1093.
38. Prakash, A., Kumar, A., Lycopene protects against memory impairment and mito-oxidative damage induced by colchicine in rats: an evidence of nitric oxide signaling. Eur. J. Pharmacol. 721 (2013), 373–381.
39. Prakash, A., Kumar, A., Implicating the role of lycopene in restoration of mitochondrial enzymes and BDNF levels in β-amyloid induced Alzheimer′ s disease. Eur. J. Pharmacol. 741 (2014), 104–111.
40. Rao, A.V., Rao, L.G., Carotenoids and human health. Pharmacol. Res. 55 (2007), 207–216.
41. Sachdeva, A.K., Chopra, K., Lycopene abrogates Aβ (1-42)-mediated neuroinflammatory cascade in an experimental model of Alzheimer's disease. J. Nutr. Biochem. 26 (2015), 736–744.
42. Song, X., Bao, M., Li, D., Li, Y., Advanced glycation in D-galactose induced mouse aging model. Mech. Ageing. Dev. 108 (1999), 239–251.
43. Tapia-Arancibia, L., Aliaga, E., Silhol, M., Arancibia, S., New insights into brain BDNF function in normal aging and Alzheimer disease. Brain Res. Rev. 59 (2008), 201–220.
44. Thorpe, S., Baynes, J., Maillard reaction products in tissue proteins: new products and new perspectives. Amino acids 25 (2003), 275–281.
45. Tsai, S., Chiu, C., Yang, H., Yin, M., s-Allyl cysteine, s-ethyl cysteine, and s-propyl cysteine alleviate β-amyloid, glycative, and oxidative injury in brain of mice treated by D-galactose. J. Agr. Food Chem. 59 (2011), 6319–6326.
46. Ullah, F., Ali, T., Ullah, N., Kim, M.O., Caffeine prevents d-galactose-induced cognitive deficits, oxidative stress, neuroinflammation and neurodegeneration in the adult rat brain. Neurochem. Int. 90 (2015), 114–124.
47. Wu, W., Wang, X., Xiang, Q., Meng, X., Peng, Y., Du, N., Liu, Z., Sun, Q., Wang, C., Liu, X., Astaxanthin alleviates brain aging in rats by attenuating oxidative stress and increasing BDNF levels. Food Funct. 5 (2014), 158–166.
48. Xian, Y., Su, Z., Chen, J., Lai, X., Mao, Q., Cheng, C., Ip, S., Lin, Z., Isorhynchophylline improves learning and memory impairments induced by D-galactose in mice. Neurochem. Int. 76 (2014), 42–49.
49. Yu, L., Wang, W., Pang, W., Xiao, Z., Jiang, Y., Hong, Y., Dietary lycopene supplementation improves cognitive performances in tau transgenic mice expressing P301L mutation via inhibiting oxidative stress and tau hyperphosphorylation. J Alzheimers Dis. 57 (2017), 475–482.
50. 2 induced memory impairment in mice. J. Ethnopharmacol. 104 (2006), 250–256.
51. Zhang, Y., Chen, H., Zhu, W., Li, C., Comparison of the carotenoid compositions and protection of in-season and anti-season tomato extracts against d-galactose-induced cognition deficits and oxidative damage in mice. Int. J. Food Sci. Nutr. 67 (2016), 983–994.
52. Zhen, Y.Z., Lin, Y.J., Li, K.J., Zhang, G.L., Zhao, Y.F., Wang, M.M., Wei, J.B., Wei, J., Hu, G., Effects of rhein lysinate on D-galactose-induced aging mice. Exp. Ther. Med. 11 (2016), 303–308.
53. Zhong, S., Ge, Q., Qu, R., Li, Q., Ma, S., Paeonol attenuates neurotoxicity and ameliorates cognitive impairment induced by d-galactose in ICR mice. J. Neurol. Sci. 277 (2009), 58–64.
54. Zhou, Y., Dong, Y., Xu, Q., He, Y., Tian, S., Zhu, S., Zhu, Y., Dong, X., Mussel oligopeptides ameliorate cognition deficit and attenuate brain senescence in D-galactose-induced aging mice. Food Chem. Toxicol. 59 (2013), 412–420.