Pelargonidin improves memory deficit in amyloid β25-35 rat model of Alzheimer's disease by inhibition of glial activation, cholinesterase, and oxidative stress

Biomedicine and Pharmacotherapy

Volumn 83, Issue , 2016, Pages 85-91

  Sohanaki, Hamid ^a   Baluchnejadmojarad, Tourandokht ^b   Nikbakht, Farnaz ^b   Roghani, Mehrdad ^c  

^a TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b IRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^c SHAHED UNIVERSITY   (Iran)

Author keywords

Acetylcholinesterase; Glial fibrillary acidic protein; Inducible nitric oxide synthase; Oxidative stress; Pelargonidin; amyloid

Indexed keywords

ACETYLCHOLINESTERASE; AMYLOID BETA PROTEIN[25-35]; CATALASE; GLIAL FIBRILLARY ACIDIC PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; MALONALDEHYDE; NITRITE; PELARGONIDIN; AMYLOID BETA PROTEIN; AMYLOID BETA-PROTEIN (25-35); ANTHOCYANIN; CHOLINESTERASE; PEPTIDE FRAGMENT;

ALZHEIMER DISEASE; AMNESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CHOLINESTERASE INHIBITION; CONTROLLED STUDY; DORSAL HIPPOCAMPUS; DRUG MECHANISM; ENZYME ACTIVITY; ESCAPE BEHAVIOR; LATENT PERIOD; LOCOMOTION; MALE; MENTAL PERFORMANCE; MORRIS WATER MAZE TEST; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; POST HOC ANALYSIS; PRIORITY JOURNAL; RAT; RAT MODEL; SPATIAL MEMORY; ANIMAL; COMPLICATION; DISEASE MODEL; DRUG EFFECTS; GLIA; HIPPOCAMPUS; MEMORY DISORDERS; METABOLISM; PATHOLOGY; REACTION TIME; WISTAR RAT;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; ANTHOCYANINS; CATALASE; CHOLINESTERASES; DISEASE MODELS, ANIMAL; GLIAL FIBRILLARY ACIDIC PROTEIN; HIPPOCAMPUS; MALE; MALONDIALDEHYDE; MEMORY DISORDERS; NEUROGLIA; NITRIC OXIDE SYNTHASE TYPE II; NITRITES; OXIDATIVE STRESS; PEPTIDE FRAGMENTS; RATS, WISTAR; REACTION TIME;

EID: 84975885884     PISSN: 07533322     EISSN: 19506007     Source Type: Journal    
DOI: 10.1016/j.biopha.2016.06.021     Document Type: Article

References (60)

1. [1] Fan, L.Y., Chiu, M.J., Combotherapy and current concepts as well as future strategies for the treatment of Alzheimer's disease. Neuropsychiatr. Dis. Treat. 10 (2014), 439–451.
2. [2] Bernal-Mondragon, C., Rivas-Arancibia, S., Kendrick, K.M., Guevara-Guzman, R., Estradiol prevents olfactory dysfunction induced by A-beta 25-35 injection in hippocampus. BMC Neurosci., 14, 2013, 104.
3. [3] Li, H., Zhang, H., Huang, H., Wang, Y., Huang, H., Caring burden and associated factors of care providers for senile dementia patients in an urban-rural fringe of Fuzhou City, China. Aging Clin. Exp. Res. 24:6 (2012), 707–713.
4. [4] Hardy, J., The amyloid hypothesis for Alzheimer's disease: a critical reappraisal. J. Neurochem. 110:4 (2009), 1129–1134.
5. [5] Wyss-Coray, T., Rogers, J., Inflammation in Alzheimer disease—a brief review of the basic science and clinical literature. Cold Spring Harb. Perspect. Med., 2(1), 2012, a006346.
6. [6] Querfurth, H.W., LaFerla, F.M., Alzheimer's disease. N. Engl. J. Med. 362:4 (2010), 329–344.
7. [7] Anand, R., Gill, K.D., Mahdi, A.A., Therapeutics of Alzheimer's disease: past, present and future. Neuropharmacology 76 (2014), 27–50.
8. [8] Blennow, K., de Leon, M.J., Zetterberg, H., Alzheimer's disease. Lancet 368:9533 (2006), 387–403.
9. [9] Karran, E., Hardy, J., A critique of the drug discovery and phase 3 clinical programs targeting the amyloid hypothesis for Alzheimer disease. Ann. Neurol. 76:2 (2014), 185–205.
10. [10] Krstic, D., Knuesel, I., The airbag problem—a potential culprit for bench-to-bedside translational efforts: relevance for Alzheimer's disease. Acta Neuropathol. Commun., 1, 2013, 62.
11. [11] Shah, R.S., Lee, H.G., Xiongwei, Z., Perry, G., Smith, M.A., Castellani, R.J., Current approaches in the treatment of Alzheimer's disease. Biomed. Pharmacother. 62:4 (2008), 199–207.
12. [12] Dreiseitel, A., Schreier, P., Oehme, A., Locher, S., Rogler, G., Piberger, H., et al. Inhibition of proteasome activity by anthocyanins and anthocyanidins. Biochem. Biophys. Res. Commun. 372:1 (2008), 57–61.
13. [13] Paixão, J., Dinis, T.C., Almeida, L.M., Dietary anthocyanins protect endothelial cells against peroxynitrite-induced mitochondrial apoptosis pathway and Bax nuclear translocation: an in vitro approach. Apoptosis 16:10 (2011), 976–989.
14. [14] Roy, M., Sen, S., Chakraborti, A.S., Action of pelargonidin on hyperglycemia and oxidative damage in diabetic rats: implication for glycation-induced hemoglobin modification. Life Sci. 82:21 (2008), 1102–1110.
15. [15] Carkeet, C., Clevidence, B.A., Novotny, J.A., Anthocyanin excretion by humans increases linearly with increasing strawberry dose. J. Nutr. 138:5 (2008), 897–902.
16. [16] Tsuda, T., Kato, Y., Osawa, T., Mechanism for the peroxynitrite scavenging activity by anthocyanins. FEBS Lett. 484:3 (2000), 207–210.
17. [17] Youdim, K.A., Dobbie, M.S., Kuhnle, G., Proteggente, A.R., Abbott, N.J., Rice-Evans, C., Interaction between flavonoids and the blood-brain barrier: in vitro studies. J. Neurochem. 85:1 (2003), 180–192.
18. [18] Abraham, S.K., Schupp, N., Schmid, U., Stopper, H., Antigenotoxic effects of the phytoestrogen pelargonidin chloride and the polyphenol chlorogenic acid. Mol. Nutr. Food Res. 51:7 (2007), 880–887.
19. [19] Dhivya, S., Khandelwal, N., Abraham, S.K., Premkumar, K., Impact of anthocyanidins on mitoxantrone-induced cytotoxicity and genotoxicity: an in vitro and In vivo analysis. Integr. Cancer Ther., 2016.
20. [20] Roghani, M., Niknam, A., Jalali-Nadoushan, M.R., Kiasalari, Z., Khalili, M., Baluchnejadmojarad, T., Oral pelargonidin exerts dose-dependent neuroprotection in 6-hydroxydopamine rat model of hemi-parkinsonism. Brain Res. Bull. 82:5 (2010), 279–283.
21. [21] Roghani, M., Niknam, A., Jalali-Nadoushan, M.-R., Kiasalari, Z., Khalili, M., Baluchnejadmojarad, T., Oral pelargonidin exerts dose-dependent neuroprotection in 6-hydroxydopamine rat model of hemi-parkinsonism. Brain Res. Bull. 82:5 (2010), 279–283.
22. [22] Mirshekar, M., Roghani, M., Khalili, M., Baluchnejadmojarad, T., Moazzen, S.A., Chronic oral pelargonidin alleviates streptozotocin-induced diabetic neuropathic hyperalgesia in rat: involvement of oxidative stress. Iran Biom J, 14(1–2), 2010, 33.
23. [23] Lin, Y.C., Tsai, P.F., Wu, J.S., Protective effect of anthocyanidins against sodium dithionite-induced hypoxia injury in C6 glial cells. J. Agric. Food Chem. 62:24 (2014), 5603–5608.
24. [24] Roghani, M., Niknam, A., Jalali-Nadoushan, M.R., Kiasalari, Z., Khalili, M., Baluchnejadmojarad, T., Oral pelargonidin exerts dose-dependent neuroprotection in 6-hydroxydopamine rat model of hemi-parkinsonism. Brain Res. Bull. 82:5–6 (2010), 279–283.
25. [25] Paxinos, G., Watson, C., The Rat Brain in Stereotaxic Coordinates: Hard Cover Edition. 2007, Elsevier Science & Technology Books.
26. [26] Liu, R.T., Zou, L.B., Fu, J.Y., Lu, Q.J., Effects of liquiritigenin treatment on the learning and memory deficits induced by amyloid beta-peptide (25–35) in rats. Behav. Brain Res. 210:1 (2010), 24–31.
27. [27] Vorhees, C.V., Williams, M.T., Morris water maze: procedures for assessing spatial and related forms of learning and memory. Nat. Protoc. 1:2 (2006), 848–858.
28. [28] Afshin-Majd, S., Khalili, M., Roghani, M., Mehranmehr, N., Baluchnejadmojarad, T., Carnosine exerts neuroprotective effect against 6-hydroxydopamine toxicity in hemiparkinsonian rat. Mol. Neurobiol. 51:3 (2015), 1064–1070.
29. [29] Bradford, M.M., A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976), 248–254.
30. [30] Claiborne, A., Catalase activity. Greenwald, R.A., (eds.) CRC Handbook of Methods for Oxygen Radical Research, 1985, CRC, Boca Raton, FL, 283–284.
31. [31] Ellman, G.L., Courtney, K.D., Andres, V. Jr., Feather-Stone, R.M., A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem. Pharmacol. 7 (1961), 88–95.
32. [32] Scuderi, C., Esposito, G., Blasio, A., Valenza, M., Arietti, P., Steardo, L. Jr., et al. Palmitoylethanolamide counteracts reactive astrogliosis induced by beta-amyloid peptide. J. Cell. Mol. Med. 15:12 (2011), 2664–2674.
33. [33] Lin, C., Lin, H.Y., Chen, J.H., Tseng, W.P., Ko, P.Y., Liu, Y.S., et al. Effects of paeonol on anti-neuroinflammatory responses in microglial cells. Int. J. Mol. Sci. 16:4 (2015), 8844–8860.
34. [34] Li, W.Z., Wu, W.Y., Huang, D.K., Yin, Y.Y., Kan, H.W., Wang, X., et al. Protective effects of astragalosides on dexamethasone and Abeta25-35 induced learning and memory impairments due to decrease amyloid precursor protein expression in 12-month male rats. Food Chem. Toxicol. 50:6 (2012), 1883–1890.
35. [35] Yin, Y., Ren, Y., Wu, W., Wang, Y., Cao, M., Zhu, Z., et al. Protective effects of bilobalide on Abeta(25–35) induced learning and memory impairments in male rats. Pharmacol. Biochem. Behav. 106 (2013), 77–84.
36. [36] Yang, H.J., Hwang, J.T., Kwon, D.Y., Kim, M.J., Kang, S., Moon, N.R., et al. Yuzu extract prevents cognitive decline and impaired glucose homeostasis in β-amyloid–infused rats. J. Nutr. 143:7 (2013), 1093–1099.
37. [37] Krstic, D., Knuesel, I., The airbag problem—a potential culprit for bench-to-bedside translational efforts: relevance for Alzheimer's disease. Acta Neuropathol. Commun., 1(1), 2013, 62.
38. [38] Yoon, J.H., Youn, K., Ho, C.T., Karwe, M.V., Jeong, W.S., Jun, M., p-Coumaric acid and ursolic acid from Corni fructus attenuated beta-amyloid(25-35)-induced toxicity through regulation of the NF-kappaB signaling pathway in PC12 cells. J. Agric. Food Chem. 62 (21 2014), 4911–4916.
39. [39] Wegiel, J., Wang, K.C., Imaki, H., Rubenstein, R., Wronska, A., Osuchowski, M., et al. The role of microglial cells and astrocytes in fibrillar plaque evolution in transgenic APP(SW) mice. Neurobiol. Aging 22:1 (2001), 49–61.
40. [40] Nagele, R.G., Wegiel, J., Venkataraman, V., Imaki, H., Wang, K.C., Wegiel, J., Contribution of glial cells to the development of amyloid plaques in Alzheimer's disease. Neurobiol. Aging 25:5 (2004), 663–674.
41. [41] Bagheri, M., Rezakhani, A., Nystrom, S., Turkina, M.V., Roghani, M., Hammarstrom, P., et al. Amyloid beta(1–40)-induced astrogliosis and the effect of genistein treatment in rat: a three-dimensional confocal morphometric and proteomic study. PLoS One, 8(10), 2013, e76526.
42. [42] Diaz, A., Mendieta, L., Zenteno, E., Guevara, J., Limon, I.D., The role of NOS in the impairment of spatial memory and damaged neurons in rats injected with amyloid beta 25–35 into the temporal cortex. Pharmacol. Biochem. Behav. 98:1 (2011), 67–75.
43. [43] Lee, S.H., Jeong, E., Paik, S.S., Jeon, J.H., Jung, S.W., Kim, H.B., et al. Cyanidin-3-glucoside extracted from mulberry fruit can reduce N-methyl-N-nitrosourea-induced retinal degeneration in rats. Curr. Eye Res. 39:1 (2014), 79–87.
44. [44] Wang, J., Ma, C., Rong, W., Jing, H., Hu, X., Liu, X., et al. Bog bilberry anthocyanin extract improves motor functional recovery by multifaceted effects in spinal cord injury. Neurochem. Res. 37:12 (2012), 2814–2825.
45. [45] Mufson, E.J., Presley, L.N., Kordower, J.H., Nerve growth factor receptor immunoreactivity within the nucleus basalis (Ch4) in Parkinson's disease: reduced cell numbers and co-localization with cholinergic neurons. Brain Res. 539:1 (1991), 19–30.
46. [46] Wang, H., Yu, Y., Chen, W., Cui, Y., Luo, T., Ma, J., et al. PLTP deficiency impairs learning and memory capabilities partially due to alteration of amyloid-beta metabolism in old mice. J. Alzheimers Dis. 39:1 (2014), 79–88.
47. [47] Gutierres, J.M., Carvalho, F.B., Schetinger, M.R., Agostinho, P., Marisco, P.C., Vieira, J.M., et al. Neuroprotective effect of anthocyanins on acetylcholinesterase activity and attenuation of scopolamine-induced amnesia in rats. Int. J. Dev. Neurosci. 33 (2014), 88–97.
48. [48] Alvarez, A., Opazo, C., Alarcon, R., Garrido, J., Inestrosa, N.C., Acetylcholinesterase promotes the aggregation of amyloid-beta-peptide fragments by forming a complex with the growing fibrils. J. Mol. Biol. 272:3 (1997), 348–361.
49. [49] Spencer, J.P., Vafeiadou, K., Williams, R.J., Vauzour, D., Neuroinflammation: modulation by flavonoids and mechanisms of action. Mol. Aspects Med. 33:1 (2012), 83–97.
50. [50] Hidalgo, M., Martin-Santamaria, S., Recio, I., Sanchez-Moreno, C., de Pascual-Teresa, B., Rimbach, G., et al. Potential anti-inflammatory, anti-adhesive, anti/estrogenic, and angiotensin-converting enzyme inhibitory activities of anthocyanins and their gut metabolites. Genes Nutr., 2012, 1–12.
51. [51] Hämäläinen, M., Nieminen, R., Vuorela, P., Heinonen, M., Moilanen, E., Anti-inflammatory effects of flavonoids: genistein, kaempferol, quercetin, and daidzein inhibit STAT-1 and NF-κ B activations, whereas flavone, isorhamnetin, naringenin, and pelargonidin inhibit only NF-κ B activation along with their inhibitory effect on iNOS expression and NO production in activated macrophages. Mediators Inflamm., 2007, 2007.
52. [52] Kruger, M.J., Davies, N., Myburgh, K.H., Lecour, S., Proanthocyanidins, anthocyanins and cardiovascular diseases. Food Res. Int. 59 (2014), 41–52.
53. [53] Spencer, J.P., Crozier, A., Flavonoids and Related Compounds: Bioavailability and Function. 2012, CRC Press.
54. [54] Fader, A.J., Johnson, P.E., Dohanich, G.P., Estrogen improves working but not reference memory and prevents amnestic effects of scopolamine on a radial-arm maze. Pharmacol. Biochem. Behav. 62:4 (1999), 711–717.
55. [55] Keskin, I., Forsgren, E., Lange, D.J., Weber, M., Birve, A., Synofzik, M., et al. Effects of cellular pathway disturbances on misfolded superoxide dismutase-1 in fibroblasts derived from ALS patients. PLoS One, 11(2), 2016, e0150133.
56. [56] Umeda, T., Ono, K., Sakai, A., Yamashita, M., Mizuguchi, M., Klein, W.L., et al. Rifampicin is a candidate preventive medicine against amyloid-beta and tau oligomers. Brain 139:Pt. 5 (2016), 1568–1586.
57. [57] Pickford, F., Masliah, E., Britschgi, M., Lucin, K., Narasimhan, R., Jaeger, P.A., et al. The autophagy-related protein beclin 1 shows reduced expression in early Alzheimer disease and regulates amyloid beta accumulation in mice. J. Clin. Invest. 118:6 (2008), 2190–2199.
58. [58] Li, D., Wang, P., Luo, Y., Zhao, M., Chen, F., Health benefits of anthocyanins and molecular mechanisms: update from recent decade. Crit. Rev. Food Sci. Nutr., 2015, 0.
59. [59] El Mohsen, M.A., Marks, J., Kuhnle, G., Moore, K., Debnam, E., Kaila Srai, S., et al. Absorption, tissue distribution and excretion of pelargonidin and its metabolites following oral administration to rats. Br. J. Nutr. 95:1 (2006), 51–58.
60. [60] Minarini, A., Milelli, A., Simoni, E., Rosini, M., Bolognesi, M.L., Marchetti, C., et al. Multifunctional tacrine derivatives in Alzheimer's disease. Curr. Top. Med. Chem. 13:15 (2013), 1771–1786.