Urolithin A attenuates memory impairment and neuroinflammation in APP/PS1 mice

Journal of Neuroinflammation

Volumn 16, Issue 1, 2019, Pages

  Gong, Zhuo ^a   Huang, Jingyi ^a   Xu, Biao ^a   Ou, Zhenri ^a   Zhang, Le ^a   Lin, Xiaohong ^a   Ye, Xiujuan ^a   Kong, Xuejian ^a   Long, Dahong ^a   Sun, Xiangdong ^a   He, Xiaosong ^a   Xu, Liping ^a   Li, Qingqing ^a   Xuan, Aiguo ^a  

^a GUANGZHOU MEDICAL UNIVERSITY   (China)

Author keywords

Alzheimer's disease; Memory impairment; Neurogenesis; Neuroinflammation; Urolithin A

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; BETA SECRETASE 1; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; INTERLEUKIN 1BETA; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE P38; NEUROPROTECTIVE AGENT; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; UROLITHIN A; 3,8-DIHYDROXY-6H-DIBENZO(B,D)PYRAN-6-ONE; ANTIINFLAMMATORY AGENT; COUMARIN DERIVATIVE; CYTOKINE; NERVE PROTEIN; PRESENILIN 1; PSEN1 PROTEIN, HUMAN;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; ARTICLE; ASTROCYTOSIS; BRAIN CORTEX; COGNITIVE DEFECT; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GLIOSIS; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; INTRACELLULAR SIGNALING; MEMORY DISORDER; MORRIS WATER MAZE TEST; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NERVOUS SYSTEM INFLAMMATION; NEUROPROTECTION; NEWBORN; NONHUMAN; PROTEIN DEGRADATION; PROTEIN EXPRESSION LEVEL; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; TRANSGENIC MOUSE; TUNEL ASSAY; WESTERN BLOTTING; AMYLOID PLAQUE; ANIMAL; BRAIN; C57BL MOUSE; COMPLICATION; DISEASE MODEL; DRUG EFFECT; ENCEPHALITIS; GENE EXPRESSION REGULATION; GENETICS; MAZE TEST; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; ANTI-INFLAMMATORY AGENTS; BRAIN; COUMARINS; CYTOKINES; DISEASE MODELS, ANIMAL; ENCEPHALITIS; FEMALE; GENE EXPRESSION REGULATION; GLIOSIS; MAZE LEARNING; MEMORY DISORDERS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; NEUROGENESIS; PLAQUE, AMYLOID; PRESENILIN-1; SIGNAL TRANSDUCTION;

EID: 85062993716     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/s12974-019-1450-3     Document Type: Article

References (58)

1. Katsouri L, Lim YM, Blondrath K, Eleftheriadou I, Lombardero L, Birch AM, Mirzaei N, Irvine EE, Mazarakis ND, Sastre M. PPARγ-coactivator-1α gene transfer reduces neuronal loss and amyloid-β generation by reducing β-secretase in an Alzheimer's disease model. Proc Natl Acad Sci U S A. 2016;113:12292-7.
2. Gold M, El Khoury J. β-amyloid, microglia, and the inflammasome in Alzheimer's disease. Semin Immunopathol. 2015;37:607-11.
3. Hanzel CE, Pichet-Binette A, Pimentel LS, Iulita MF, Allard S, Ducatenzeiler A, Do Carmo S, Cuello AC. Neuronal driven pre-plaque inflammation in a transgenic rat model of Alzheimer's disease. Neurobiol Aging. 2014;35:2249-62.
4. Hoeijmakers L, Ruigrok SR, Amelianchik A, Ivan D, van Dam AM, Lucassen PJ, Korosi A. Early-life stress lastingly alters the neuroinflammatory response to amyloid pathology in an Alzheimer's disease mouse model. Brain Behav Immun. 2017;63:160-75.
5. Ries M, Sastre M. Mechanisms of Aβ clearance and degradation by glial cells. Front Aging Neurosci. 2016;8:160.
6. in t' Veld BA, Ruitenberg A, Hofman A, Launer LJ, van Duijn CM, Stijnen T, Breteler MM, Stricker BH. Nonsteroidal antiinflammatory drugs and the risk of Alzheimer's disease. N Engl J Med. 2001;345:1515-21.
7. Stewart WF, Kawas C, Corrada M, Metter EJ. Risk of Alzheimer's disease and duration of NSAID use. Neurology. 1997;48:626-32.
8. Larrosa M, González-Sarrías A, García-Conesa MT, Tomás-Barberán FA, Espín JC. Urolithins, ellagic acid-derived metabolites produced by human colonic microflora, exhibit estrogenic and antiestrogenic activities. J Agric Food Chem. 2006;54:1611-20.
9. Tomás-Barberán FA, García-Villalba R, González-Sarrías A, Selma MV, Espín JC. Ellagic acid metabolism by human gut microbiota: consistent observation of three urolithin phenotypes in intervention trials, independent of food source, age, and health status. J Agric Food Chem. 2014;62:6535-8.
10. Larrosa M, González-Sarrías A, Yáñez-Gascón MJ, Selma MV, Azorín-Ortuño M, Toti S, Tomás-Barberán F, Dolara P, Espín JC. Anti-inflammatory properties of a pomegranate extract and its metabolite urolithin-A in a colitis rat model and the effect of colon inflammation on phenolic metabolism. J Nutr Biochem. 2010;21:717-25.
11. Ishimoto H, Shibata M, Myojin Y, Ito H, Sugimoto Y, Tai A, Hatano T. In vivo anti-inflammatory and antioxidant properties of ellagitannin metabolite urolithin A. Bioorg Med Chem Lett. 2011;21(19):5901-4.
12. Giménez-Bastida JA, González-Sarrías A, Larrosa M, Tomás-Barberán F, Espín JC, García-Conesa MT. Ellagitannin metabolites, urolithin A glucuronide and its aglycone urolithin A, ameliorate TNF-α-induced inflammation and associated molecular markers in human aortic endothelial cells. Mol Nutr Food Res. 2012;56:784-96.
13. Giménez-Bastida JA, Larrosa M, González-Sarrías A, Tomás-Barberán F, Espín JC, García-Conesa MT. Intestinal ellagitannin metabolites ameliorate cytokine-induced inflammation and associated molecular markers in human colon fibroblasts. J Agric Food Chem. 2012;60:8866-76.
14. González-Sarrías A, Larrosa M, Tomás-Barberán FA, Dolara P, Espín JC. NF-kappaB-dependent anti-inflammatory activity of urolithins, gut microbiota ellagic acid-derived metabolites, in human colonic fibroblasts. Br J Nutr. 2010;104:503-12.
15. West MJ, Coleman PD, Flood DG, Troncoso JC. Differences in the pattern of hippocampal neuronal loss in normal ageing and Alzheimer's disease. Lancet. 1994;344:769-72.
16. Raefsky SM, Furman R, Milne G, Pollock E, Axelsen P, Mattson MP, Shchepinov MS. Deuterated polyunsaturated fatty acids reduce brain lipid peroxidation and hippocampal amyloid β-peptide levels, without discernable behavioral effects in an APP/PS1 mutant transgenic mouse model of Alzheimer's disease. Neurobiol Aging. 2018;66:165-76.
17. Shors TJ, Miesegaes G, Beylin A, Zhao M, Rydel T, Gould E. Neurogenesis in the adult is involved in the formation of trace memories. Nature. 2001;410:372-6.
18. Ou Z, Kong X, Sun X, He X, Zhang L, Gong Z, Huang J, Xu B, Long D, Li J, et al. Metformin treatment prevents amyloid plaque deposition and memory impairment in APP/PS1 mice. Brain Behav Immun. 2018;69:351-63.
19. Fu AK, Hung KW, Yuen MY, Zhou X, Mak DS, Chan IC, Cheung TH, Zhang B, Fu WY, Liew FY, et al. IL-33 ameliorates Alzheimer's disease-like pathology and cognitive decline. Proc Natl Acad Sci U S A. 2016;113:E2705-13.
20. Li S, Hou H, Mori T, Sawmiller D, Smith A, Tian J, Giunta B, Sanberg PR, Zhang S, et al. Swedish mutant APP-based BACE1 binding site peptide reduces APP β-cleavage and cerebral Aβ levels in Alzheimer's mice. Sci Rep. 2015;5:11322.
21. Chen Y, Zhou K, Wang R, Liu Y, Kwak YD, Ma T, Thompson RC, Zhao Y, Smith L, Gasparini L, et al. Antidiabetic drug metformin (GlucophageR) increases biogenesis of Alzheimer's amyloid peptides via up-regulating BACE1 transcription. Proc Natl Acad Sci U S A. 2009;106:3907-12.
22. Li W, Qiu X, Jiang H, Zhi Y, Fu J, Liu J. Ulinastatin inhibits the inflammation of LPS-induced acute lung injury in mice via regulation ofAMPK/NF-κB pathway. Int Immunopharmacol. 2015;29:560-7.
23. Chen S, Zhao L, Sherchan P, Ding Y, Yu J, Nowrangi D, Tang J, Xia Y, Zhang JH. Activation of melanocortin receptor 4 with RO27-3225 attenuates neuroinflammation through AMPK/JNK/p38 MAPK pathway after intracerebral hemorrhage in mice. J Neuroinflammation. 2018;15:106.
24. Hartman RE, Shah A, Fagan AM, Schwetye KE, Parsadanian M, Schulman RN, Finn MB, Holtzman DM. Pomegranate juice decreases amyloid load and improves behavior in a mouse model of Alzheimer's disease. Neurobiol Dis. 2006;24:506-15.
25. Subash S, Braidy N, Essa MM, Zayana AB, Ragini V, Al-Adawi S, Al-Asmi A, Guillemin GJ. Long-term (15 mo) dietary supplementation with pomegranates from Oman attenuates cognitive and behavioral deficits in a transgenic mice model of Alzheimer's disease. Nutrition. 2015;31:223-9.
26. Rojanathammanee L, Puig KL, Combs CK. Pomegranate polyphenols and extract inhibit nuclear factor of activated T-cell activity and microglial activation in vitro and in a transgenic mouse model of Alzheimer disease. J Nutr. 2013;143:597-605.
27. Ahmed AH, Subaiea GM, Eid A, Li L, Seeram NP, Zawia NH. Pomegranate extract modulates processing of amyloid-β precursor protein in an aged Alzheimer's disease animal model. Curr Alzheimer Res. 2014;11:834-43.
28. Drapeau E, Nora Abrous D. Stem cell review series: role of neurogenesis in age-related memory disorders. Aging Cell. 2008;7:569-89.
29. Chao F, Jiang L, Zhang Y, Zhou C, Zhang L, Tang J, Liang X, Qi Y, Zhu Y, Ma J, et al. Stereological investigation of the effects of treadmill running exercise on the hippocampal neurons in middle-aged APP/PS1 transgenic mice. J Alzheimers Dis. 2018;63:689-703.
30. Rupp NJ, Wegenast-Braun BM, Radde R, Calhoun ME, Jucker M. Early onset amyloid lesions lead to severe neuritic abnormalities and local, but not global neuron loss in APPPS1 transgenic mice. Neurobiol Aging. 2011;32:2324.
31. Takeuchi A, Irizarry MC, Duff K, Saido TC, Hsiao Ashe K, Hasegawa M, Mann DM, Hyman BT, Iwatsubo T. Age-related amyloid beta deposition in transgenic mice overexpressing both Alzheimer mutant presenilin 1 and amyloid beta precursor protein Swedish mutant is not associated with global neuronal loss. Am J Pathol. 2000;157(1):331-9.
32. Long Z, Zheng M, Zhao L, Xie P, Song C, Chu Y, Song W, He G. Valproic acid attenuates neuronal loss in the brain of APP/PS1 double transgenic Alzheimer's disease mice model. Curr Alzheimer Res. 2013;10(3):261-9.
33. Stygelbout V, Leroy K, Pouillon V, Ando K, D'Amico E, Jia Y, Luo HR, Duyckaerts C, Erneux C, Schurmans S, et al. Inositol trisphosphate 3-kinase B is increased in human Alzheimer brain and exacerbates mouse Alzheimer pathology. Brain. 2014;137:537-52.
34. Puzzo D, Loreto C, Giunta S, Musumeci G, Frasca G, Podda MV, Arancio O, Palmeri A. Effect of phosphodiesterase-5 inhibition on apoptosis and beta amyloid load in aged mice. Neurobiol Aging. 2014;35:520-31.
35. Gorji N, Moeini R, Memariani Z. Almond, hazelnut and walnut, three nuts for neuroprotection in Alzheimer's disease: a neuropharmacological review of their bioactive constituents. Pharmacol Res. 2018;129:115-27.
36. Shukitt-Hale B, Bielinski DF, Lau FC, Willis LM, Carey AN, Joseph JA. The beneficial effects of berries on cognition, motor behaviour and neuronal function in ageing. Br J Nutr. 2015;114:1542-9.
37. Holtzman DM, Morris JC, Goate AM. Alzheimer's disease: the challenge of the second century. Sci Transl Med. 2011;3:77sr1.
38. Yuan T, Ma H, Liu W, Niesen DB, Shah N, Crews R, Rose KN, Vattem DA, Seeram NP. Pomegranate's neuroprotective effects against Alzheimer's disease are mediated by urolithins, its ellagitannin-gut microbial derived metabolites. ACS Chem Neurosci. 2016;7:26-33.
39. Walker D, Lue LF. Anti-inflammatory and immune therapy for Alzheimer's disease: current status and future directions. Curr Neuropharmacol. 2007;5:232-43.
40. Piwowarski JP, Kiss AK, Granica S, Moeslinger T. Urolithins, gut microbiota-derived metabolites of ellagitannins, inhibit LPS-induced inflammation in RAW 264.7 murine macrophages. Mol Nutr Food Res. 2015;59:2168-77.
41. Itagaki S, McGeer PL, Akiyama H, Zhu S, Selkoe D. Relationship of microglia and astrocytes to amyloid deposits of Alzheimer disease. J Neuroimmunol. 1989;24:173-82.
42. Sun W, Yan C, Frost B, Wang X, Hou C, Zeng M, Gao H, Kang Y, Liu J. Pomegranate extract decreases oxidative stress and alleviates mitochondrial impairment by activating AMPK-Nrf2 in hypothalamic paraventricular nucleus of spontaneously hypertensive rats. Sci Rep. 2016;6:34246.
43. Ok E, Do GM, Lim Y, Park JE, Park YJ, Kwon O. Pomegranate vinegar attenuates adiposity in obese rats through coordinated control of AMPK signaling in the liver and adipose tissue. Lipids Health Dis. 2013;12:163.
44. Mo C, Wang L, Zhang J, Numazawa S, Tang H, Tang X, Han X, Li J, Yang M, Wang Z, et al. The crosstalk between Nrf2 and AMPK signal pathways is important for the anti-inflammatory effect of berberine in LPS-stimulated macrophages and endotoxin-shocked mice. Antioxid Redox Signal. 2014;20:574-88.
45. Kang I, Kim Y, Tomás-Barberán FA, Espín JC, Chung S. Urolithin A, C, and D, but not iso-urolithin A and urolithin B, attenuate triglyceride accumulation in human cultures of adipocytes and hepatocytes. Mol Nutr Food Res. 2016;60:1129-38.
46. Vingtdeux V, Giliberto L, Zhao H, Chandakkar P, Wu Q, Simon JE, Janle EM, Lobo J, Ferruzzi MG, Davies P, et al. AMP-activated protein kinase signaling activation by resveratrol modulates amyloid-beta peptide metabolism. J Biol Chem. 2010;285:9100-13.
47. Pei JJ, Hugon J. mTOR-dependent signalling in Alzheimer's disease. J Cell Mol Med. 2008;12:2525-32.
48. Zhang J, Zhang Y, Xiao F, Liu Y, Wang J, Gao H, Rong S, Yao Y, Li J, Xu G. The peroxisome proliferator-activated receptor γ agonist pioglitazone prevents NF-κB activation in cisplatin nephrotoxicity through the reduction of p65 acetylation via the AMPK-SIRT1/p300 pathway. Biochem Pharmacol. 2016;101:100-11.
49. Kauppinen A, Suuronen T, Ojala J, Kaarniranta K, Salminen A. Antagonistic crosstalk between NF-κB and SIRT1 in the regulation of inflammation and metabolic disorders. Cell Signal. 2013;25:1939-48.
50. Salvadó L, Coll T, Gómez-Foix AM, Salmerón E, Barroso E, Palomer X, Vázquez-Carrera M. Oleate prevents saturated-fatty-acid-induced ER stress, inflammation and insulin resistance in skeletal muscle cells through an AMPK-dependent mechanism. Diabetologia. 2013;56:1372-82.
51. Boakye YD, Groyer L, Heiss EH. An increased autophagic flux contributes to the anti-inflammatory potential of urolithin A in macrophages. Biochim Biophys Acta. 1862;2018:61-70.
52. Xu J, Yuan C, Wang G, Luo J, Ma H, Xu L, Mu Y, Li Y, Seeram NP, Huang X, et al. Urolithins attenuate LPS-induced neuroinflammation in BV2Microglia via MAPK, Akt, and NF-κB signaling pathways. J Agric Food Chem. 2018;66:571-80.
53. Munoz L, Ammit AJ. Targeting p38 MAPK pathway for the treatment of Alzheimer's disease. Neuropharmacology. 2010;58:561-8.
54. Pei JJ, Braak E, Braak H, Grundke-Iqbal I, Iqbal K, Winblad B, Cowburn RF. Localization of active forms of C-jun kinase (JNK) and p38 kinase in Alzheimer's disease brains at different stages of neurofibrillary degeneration. J Alzheimers Dis. 2001;3:1-48.
55. Sabogal-Guáqueta AM, Osorio E, Cardona-Gómez GP. Linalool reverses neuropathological and behavioral impairments in old triple transgenic Alzheimer's mice. Neuropharmacology. 2016;102:111-20.
56. Kim TI, Lee YK, Park SG, Choi IS, Ban JO, Park HK, Nam SY, Yun YW, Han SB, Oh KW, et al. l-Theanine, an amino acid in green tea, attenuates beta-amyloid-induced cognitive dysfunction and neurotoxicity: reduction in oxidative damage and inactivation of ERK/p38 kinase and NF-kappaB pathways. Free Radic Biol Med. 2009;47:1601-10.
57. Wang Y, Qiu Z, Zhou B, Liu C, Ruan J, Yan Q, Liao J, Zhu F. In vitro antiproliferative and antioxidant effects of urolithin A, the colonic metabolite of ellagic acid, on hepatocellular carcinomas HepG2 cells. Toxicol in Vitro. 2015;29:1107-15.
58. Qiu Z, Zhou B, Jin L, Yu H, Liu L, Liu Y, Qin C, Xie S, Zhu F. In vitro antioxidant and antiproliferative effects of ellagic acid and its colonic metabolite, urolithins, on human bladder cancer T24 cells. Food Chem Toxicol. 2013;59:428-37.