Modulation of oxidative stress, inflammation, autophagy and expression of Nrf2 in hippocampus and frontal cortex of rats fed with açaí-enriched diets

Nutritional Neuroscience

Volumn 20, Issue 5, 2017, Pages 305-315

  Poulose, Shibu M ^a   Bielinski, Donna F ^a   Carey, Amanda ^a,b   Schauss, Alexander G ^c   Shukitt Hale, Barbara ^a  

^a TUFTS UNIVERSITY   (United States)

^b SIMMONS COLLEGE   (United States)

^c AIBMR Life Sciences Inc   (United States)

Author keywords

Antioxidants; Autophagy; A a ; Inflammation; Oxidative stress; Ubiquitin

Indexed keywords

BECLIN 1; GLUTATHIONE TRANSFERASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MAMMALIAN TARGET OF RAPAMYCIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; SEQUESTOSOME 1; SUPEROXIDE DISMUTASE; TRANSCRIPTION FACTOR NRF2; ANTIOXIDANT; CYBB PROTEIN, RAT; NFE2L2 PROTEIN, RAT; PLANT EXTRACT;

ANIMAL TISSUE; ARTICLE; AUTOPHAGY; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; EUTERPE; IMMUNOHISTOCHEMISTRY; MALE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; CHEMISTRY; COGNITION; DIET; DRUG EFFECTS; FISCHER 344 RAT; FRONTAL LOBE; FRUIT; GENETICS; HIPPOCAMPUS; INFLAMMATION; MEMORY; METABOLISM; OXIDATION REDUCTION REACTION; PHYSIOLOGY; PHYTOTHERAPY; SPECIES DIFFERENCE;

ANIMALS; ANTIOXIDANTS; AUTOPHAGY; COGNITION; DIET; EUTERPE; FRONTAL LOBE; FRUIT; HIPPOCAMPUS; INFLAMMATION; MALE; MEMORY; NADPH OXIDASE 2; NF-E2-RELATED FACTOR 2; NF-KAPPA B; OXIDATION-REDUCTION; OXIDATIVE STRESS; PHYTOTHERAPY; PLANT EXTRACTS; RATS; RATS, INBRED F344; SPECIES SPECIFICITY;

EID: 84971356065     PISSN: 1028415X     EISSN: 14768305     Source Type: Journal    
DOI: 10.1080/1028415X.2015.1125654     Document Type: Article

References (50)

1. United Nations-Department of Economic and Social Affairs Population Divisions. World population aging. 2013. ST/ESA/SER A/348.
2. Marx J., Neurodegenerative diseases. Picking apart the causes of mysterious dementias. Science 2006;314:42–3. doi:10.1126/science.314.5796.42
3. Pierpaoli W., Neurodegenerative diseases:a common etiology and a common therapy. Ann N Y Acad Sci 2005;1057:319–26. doi:10.1196/annals.1356.024
4. Chen Y, Dube CM, Rice CJ, Baram TZ., Rapid loss of dendritic spines after stress involves derangement of spine dynamics by corticotropin-releasing hormone. J Neurosci 2008;28:2903–11. doi:10.1523/JNEUROSCI.0225-08.2008
5. Lee J, Giordano S, Zhang J., Autophagy, mitochondria and oxidative stress:cross-talk and redox signalling. Biochem J 2012;441:523–40. doi:10.1042/BJ20111451
6. Friedman LG, Lachenmayer ML, Wang J, He L, Poulose SM, Komatsu M, et al. Disrupted autophagy leads to dopaminergic axon and dendrite degeneration and promotes presynaptic accumulation of alpha-synuclein and LRRK2 in the brain. J Neurosci 2012;32:7585–93. doi:10.1523/JNEUROSCI.5809-11.2012
7. Ulbricht C, Brigham A, Burke D, Costa D, Giese N, Iovin R, et al. An evidence-based systematic review of acai (Euterpe oleracea) by the Natural Standard Research Collaboration. J Diet Suppl 2012;9:128–47. doi:10.3109/19390211.2012.686347
8. Kang J, Xie C, Li Z, Nagarajan S, Schauss AG, Wu T, et al. Flavonoids from acai (Euterpe oleracea Mart.) pulp and their antioxidant and anti-inflammatory activities. Food Chem 2011;128:152–7. doi:10.1016/j.foodchem.2011.03.011
9. Schauss AG, Wu X, Prior RL, Ou B, Patel D, Huang D, et al. Phytochemical and nutrient composition of the freeze-dried Amazonian palm berry, Euterpe oleraceae mart. (acai). J Agric Food Chem 2006;54:8598–603. doi:10.1021/jf060976g
10. Poulose S, Shukitt-Hale B., Functional role of walnuts and acai fruits on brain health. In:Patil BS, Jayaprakasha GK, Rao CO, Mahattanatawee K, editors. Tropical and subtropical fruits. Washington, DC:American Chemical Society Publications; p. 171–87.
11. Odendaal AY, Schauss AG., Potent antioxidant and anti-inflammatory flavonoids in the nutrient-rich Amazonian palm fruit, açaí (Euterpe spp.). In:Watson RR, Reedy VR, Zibadi S, editors. Polyphenols in human health and disease. San Diego:Academic Press; 2014. p. 219–39.
12. Poulose SM, Fisher DR, Bielinski DF, Gomes SM, Rimando AM, Schauss AG, et al. Restoration of stressor-induced calcium dysregulation and autophagy inhibition by polyphenol-rich açaí (Euterpe spp.) fruit pulp extracts in rodent brain cells in vitro. Nutrition 2014;30:853–62. doi:10.1016/j.nut.2013.11.011
13. Xie C, Kang J, Li Z, Schauss AG, Badger TM, Nagarajan S, et al. The acai flavonoid velutin is a potent anti-inflammatory agent:blockade of LPS-mediated TNF-alpha and IL-6 production through inhibiting NF-kappaB activation and MAPK pathway. J Nutr Biochem 2012;23:1184–91. doi:10.1016/j.jnutbio.2011.06.013
14. Jensen GS, Ager DM, Redman KA, Mitzner MA, Benson KF, Schauss AG., Pain reduction and improvement in range of motion after daily consumption of an acai (Euterpe oleracea Mart.) pulp-fortified polyphenolic-rich fruit and berry juice blend. J Med Food 2011;14:702–11. doi:10.1089/jmf.2010.0150
15. Xie C, Kang J, Burris R, Ferguson ME, Schauss AG, Nagarajan S, et al. Acai juice attenuates atherosclerosis in ApoE deficient mice through antioxidant and anti-inflammatory activities. Atherosclerosis 2011;216:327–33. doi:10.1016/j.atherosclerosis.2011.02.035
16. Schauss AG, Wu X, Prior RL, Ou B, Huang D, Owens J, et al. Antioxidant capacity and other bioactivities of the freeze-dried Amazonian palm berry, Euterpe oleraceae mart. (acai). J Agric Food Chem 2006;54:8604–10. doi:10.1021/jf0609779
17. Poulose SM, Fisher DR, Larson J, Bielinski DF, Rimando AM, Carey AN, et al. Anthocyanin-rich acai (Euterpe oleracea Mart.) fruit pulp fractions attenuate inflammatory stress signaling in mouse brain BV-2 microglial cells. J Agric Food Chem 2012;60:1084–93. doi:10.1021/jf203989k
18. Souza-Monteiro JR, Hamoy M, Santana-Coelho D, Arrifano GP, Paraense RS, Costa-Malaquias A, et al. Anticonvulsant properties of Euterpe oleracea in mice. Neurochem Int 2015. doi:10.1016/j.neuint.2015.06.014
19. Preston AR, Eichenbaum H., Interplay of hippocampus and prefrontal cortex in memory. Curr Biol 2013;23:R764–73. doi:10.1016/j.cub.2013.05.041
20. Gemma C, Vila J, Bachstetter A, Bickford PC., Oxidative stress and the aging brain:from theory to prevention. In:Riddle DR, editor. Brain aging:models, methods, and mechanisms. Boca Raton, FL:CRC Press/Taylor & Francis; 2007.
21. Park HR, Kong KH, Yu BP, Mattson MP, Lee J., Resveratrol inhibits the proliferation of neural progenitor cells and hippocampal neurogenesis. J Biol Chem 2012;287:42588–600. doi:10.1074/jbc.M112.406413
22. Hicyilmaz H, Vural H, Delibas N, Sutcu R, Gultekin F, Yilmaz N., The effects of walnut supplementation on hippocampal NMDA receptor subunits NR2A and NR2B of rats. Nutr Neurosci 2014. doi:10.1179/1476830514Y.0000000166
23. Poulose SM, Bielinski DF, Carrihill-Knoll KL, Rabin BM, Shukitt-Hale B., Protective effects of blueberry-and strawberry diets on neuronal stress following exposure to 56 Fe particles. Brain Res 2014;1593:9–18. doi:10.1016/j.brainres.2014.10.028
24. Hensley K, Harris-White ME., Redox regulation of autophagy in healthy brain and neurodegeneration. Neurobiol Dis 2015;84:50–9. doi:10.1016/j.nbd.2015.03.002
25. Shah ZA, Li RC, Thimmulappa RK, Kensler TW, Yamamoto M, Biswal S, et al. Role of reactive oxygen species in modulation of Nrf2 following ischemic reperfusion injury. Neuroscience 2007;147:53–9. doi:10.1016/j.neuroscience.2007.02.066
26. Rojo AI, Innamorato NG, Martin-Moreno AM, De Ceballos ML, Yamamoto M, Cuadrado A., Nrf2 regulates microglial dynamics and neuroinflammation in experimental Parkinson's disease. Glia 2010;58:588–98. doi:10.1002/glia.20947
27. Vargas MR, Johnson JA., The Nrf2-ARE cytoprotective pathway in astrocytes. Expert Rev Mol Med 2009;11:e17. doi:10.1017/S1462399409001094
28. Carey AN, Miller MG, Fisher DR, Bielinski DF, Gilman CK, Poulose SM, Shukitt-Hale B., Dietary supplementation with the polyphenol-rich açaí pulps (Euterpe oleracea Mart. and Euterpe precatoria Mart.) improves cognition in aged rats and attenuates inflammatory signaling in BV-2 microglial cells. Nutr Neurosci 2015. doi:10.1080/1028415X.2015.1115213
29. Shukitt-Hale B, Mouzakis G, Joseph JA., Psychomotor and spatial memory performance in aging male Fischer 344 rats. Expl Gerontol 1998;33:615–24. doi:10.1016/S0531-5565(98)00024-2
30. Mizushima N, Yoshimori T., How to interpret LC3 immunoblotting. Autophagy 2007;3:542–5. doi:10.4161/auto.4600
31. Miller MG, Shukitt-Hale B., Berry fruit enhances beneficial signaling in the brain. J Agric Food Chem 2012;60:5709–15. doi:10.1021/jf2036033
32. Poulose SM, Carey AN, Shukitt-Hale B., Improving brain signaling in aging:could berries be the answer? Expert Rev Neurother 2012;12:887–9. doi:10.1586/ern.12.86
33. Lamport DJ, Saunders C, Butler LT, Spencer JP., Fruits, vegetables, 100% juices, and cognitive function. Nutr Rev 2014;72:774–89. doi:10.1111/nure.12149
34. Hernandes MS, D'Avila JC, Trevelin SC, Reis PA, Kinjo ER, Lopes LR, et al. The role of Nox2-derived ROS in the development of cognitive impairment after sepsis. J Neuroinflamm 2014;11:36. doi:10.1186/1742-2094-11-36
35. Park J, Choi H, Min JS, Park SJ, Kim JH, Park HJ, et al. Mitochondrial dynamics modulate the expression of pro-inflammatory mediators in microglial cells. J Neurochem 2013;127:221–32. doi:10.1111/jnc.12361
36. Marklund SL, Westman NG, Lundgren E, Roos G., Copper- and zinc-containing superoxide dismutase, manganese-containing superoxide dismutase, catalase, and glutathione peroxidase in normal and neoplastic human cell lines and normal human tissues. Cancer Res1982;42:1955–61.
37. Andres-Lacueva C, Shukitt-Hale B, Galli RL, Jauregui O, Lamuela-Raventos RM, Joseph JA., Anthocyanins in aged blueberry-fed rats are found centrally and may enhance memory. Nutr Neurosci 2005;8:111–20. doi:10.1080/10284150500078117
38. Rendeiro C, Guerreiro JD, Williams CM, Spencer JP., Flavonoids as modulators of memory and learning:molecular interactions resulting in behavioural effects. Proc Nutr Soc 2012;71:246–62. doi:10.1017/S0029665112000146
39. Zhu H, Itoh K, Yamamoto M, Zweier JL, Li Y., Role of Nrf2 signaling in regulation of antioxidants and phase 2 enzymes in cardiac fibroblasts:protection against reactive oxygen and nitrogen species-induced cell injury. FEBS Lett 2005;579:3029–36. doi:10.1016/j.febslet.2005.04.058
40. Leonardo CC, Doré S., Dietary flavonoids are neuroprotective through Nrf2-coordinated induction of endogenous cytoprotective proteins. Nutr Neurosci 2011;14:226–36. doi:10.1179/1476830511Y.0000000013
41. Singh N, Agrawal M, Dore S., Neuroprotective properties and mechanisms of resveratrol in in vitro and in vivo experimental cerebral stroke models. ACS Chem Neurosci 2013;4:1151–1162. doi:10.1021/cn400094w
42. Ichimura Y, Waguri S, Sou YS, Kageyama S, Hasegawa J, Ishimura R, et al. Phosphorylation of p62 activates the Keap1-Nrf2 pathway during selective autophagy. Mol Cell 2013;51:618–31. doi:10.1016/j.molcel.2013.08.003
43. Cuervo AM., Autophagy:in sickness and in health. Trends Cell Biol 2004;14:70–7. doi:10.1016/j.tcb.2003.12.002
44. Filomeni G, Graziani I, De Zio D, Dini L, Centonze D, Rotilio G, et al. Neuroprotection of kaempferol by autophagy in models of rotenone-mediated acute toxicity:possible implications for Parkinson's disease. Neurobiol Aging 2012;33:767–85. doi:10.1016/j.neurobiolaging.2010.05.021
45. Klappan AK, Hones S, Mylonas I, Bruning A., Proteasome inhibition by quercetin triggers macroautophagy and blocks mTOR activity. Histochem Cell Biol 2012;137:25–36. doi:10.1007/s00418-011-0869-0
46. Poulose SM, Bielinski DF, Shukitt-Hale B., Walnut diet reduces accumulation of polyubiquitinated proteins and inflammation in the brain of aged rats. J Nutr Biochem 2013;24:912–9. doi:10.1016/j.jnutbio.2012.06.009
47. Komatsu M, Kurokawa H, Waguri S, Taguchi K, Kobayashi A, Ichimura Y, et al. The selective autophagy substrate p62 activates the stress responsive transcription factor Nrf2 through inactivation of Keap1. Nat Cell Biol 2010;12:213–23.
48. Nair S, Doh ST, Chan JY, Kong AN, Cai L., Regulatory potential for concerted modulation of Nrf2- and Nfkb1-mediated gene expression in inflammation and carcinogenesis. BrJ Cancer 2008;99:2070–82. doi:10.1038/sj.bjc.6604703
49. Kang R, Zeh HJ, Lotze MT, Tang D., The Beclin 1 network regulates autophagy and apoptosis. Cell Death Differ 2011;18:571–80. doi:10.1038/cdd.2010.191
50. Liu GH, Qu J, Shen X., NF-kappaB/p65 antagonizes Nrf2-ARE pathway by depriving CBP from Nrf2 and facilitating recruitment of HDAC3 to MafK. Biochimica Et biophysica Acta 2008;1783:713–27. doi:10.1016/j.bbamcr.2008.01.002