Protective effects of vitamin D on learning and memory deficit induced by scopolamine in male rats: the roles of brain-derived neurotrophic factor and oxidative stress.
Adjuvants, Anesthesia
/ toxicity
Animals
Antioxidants
/ pharmacology
Brain-Derived Neurotrophic Factor
/ metabolism
Dose-Response Relationship, Drug
Learning
/ drug effects
Male
Memory Disorders
/ chemically induced
Nitric Oxide
/ antagonists & inhibitors
Oxidative Stress
/ drug effects
Rats
Rats, Wistar
Scopolamine
/ toxicity
Vitamin D
/ pharmacology
Brain-derived neurotrophic factor
Learning
Memory
Nitric oxide
Oxidative stress
Scopolamine
Vitamin D
Journal
Naunyn-Schmiedeberg's archives of pharmacology
ISSN: 1432-1912
Titre abrégé: Naunyn Schmiedebergs Arch Pharmacol
Pays: Germany
ID NLM: 0326264
Informations de publication
Date de publication:
07 2021
07 2021
Historique:
received:
04
11
2020
accepted:
04
02
2021
pubmed:
3
3
2021
medline:
15
1
2022
entrez:
2
3
2021
Statut:
ppublish
Résumé
The beneficial effects of vitamin D (vit D) on central nervous system disorders have been suggested. In the current research, the protective effects of vit D on learning and memory deficit induced by scopolamine, oxidative stress criteria, brain-derived neurotrophic factor (BDNF), and nitric oxide (NO) in the brain were investigated. Rats were divided into five groups, including (1) Control, (2) Scopolamine (2 mg/kg), (3-5) Scopolamine + Vit D (100, 1000, and 10,000 IU/kg) groups. Vit D administrated for 2 weeks and in the third week scopolamine co-administrated with vit D and behavioral tests, including Morris water maze (MWM) and passive avoidance (PA) tests, were carried out. The cortical and hippocampal tissues were analyzed for BDNF, catalase (CAT), and superoxide dismutase (SOD) activities, thiol content, NO metabolites, and malondialdehyde (MDA) concentration. Scopolamine injection significantly impaired rats' performance on the MWM and PA test. It further enhanced the MDA and nitrite level while decreased thiol content and BDNF levels and SOD and CAT activities in the brain. Administration of both 1000 and 10,000 IU/kg vit D improved cognitive outcome in MWM and PA tests. In addition, vit D elevated thiol content, SOD and CAT activities, and BDNF levels, while reduced nitrite and MDA concentration. Vit D also increased the levels of vit D and calcium in the serum. The results demonstrated that vit D has protective effects on scopolamine-associated learning and memory impairment by improving BDNF levels and attenuating NO and brain tissue oxidative damage.
Identifiants
pubmed: 33649977
doi: 10.1007/s00210-021-02062-w
pii: 10.1007/s00210-021-02062-w
doi:
Substances chimiques
Adjuvants, Anesthesia
0
Antioxidants
0
Bdnf protein, rat
0
Brain-Derived Neurotrophic Factor
0
Vitamin D
1406-16-2
Nitric Oxide
31C4KY9ESH
Scopolamine
DL48G20X8X
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1451-1466Références
Abareshi A, Hosseini M, Beheshti F, Norouzi F, Khazaei M, Sadeghnia HR et al (2016) The effects of captopril on lipopolysaccharide induced learning and memory impairments and the brain cytokine levels and oxidative damage in rats. Life Sci 167(Supplement C):46–56
pubmed: 27794490
doi: 10.1016/j.lfs.2016.10.026
Aebi H (1984) [13] Catalase in vitro. Methods Enzymol 105:121–126
pubmed: 6727660
doi: 10.1016/S0076-6879(84)05016-3
AlJohri R, AlOkail M, Haq SH (2019) Neuroprotective role of vitamin D in primary neuronal cortical culture. eNeurologicalSci. 14:43–48
pubmed: 30619951
doi: 10.1016/j.ensci.2018.12.004
Alrefaie Z, Moustafa I (2020) Vitamin D3 favorable outcome on recognition memory and prefrontal cortex expression of choline acetyltransferase and acetylcholinesterase in experimental model of chronic high-fat feeding. Int J Neurosci 130(3):262–269
pubmed: 31544572
doi: 10.1080/00207454.2019.1671839
Amini Y, Saif N, Greer C, Hristov H, Isaacson R (2020) The role of nutrition in individualized Alzheimer's risk reduction. Curr Nutr Rep 9(2):55–63
pubmed: 32277428
doi: 10.1007/s13668-020-00311-7
Anaeigoudari A, Shafei MN, Soukhtanloo M, Sadeghnia HR, Reisi P, Beheshti F et al (2015) Lipopolysaccharide-induced memory impairment in rats is preventable using 7-nitroindazole. Arq Neuropsiquiatr 73(9):784–790
pubmed: 26352498
doi: 10.1590/0004-282X20150121
Annweiler C, Beauchet O (2012) Possibility of a new anti-alzheimer's disease pharmaceutical composition combining memantine and vitamin D. Drugs Aging 29(2):81–91
pubmed: 22233455
doi: 10.2165/11597550-000000000-00000
Annweiler C, Schott AM, Berrut G, Chauvire V, Le Gall D, Inzitari M et al (2010) Vitamin D and ageing: neurological issues. Neuropsychobiology. 62(3):139–150
pubmed: 20628264
doi: 10.1159/000318570
Anu KR, Das S, Joseph A, Shenoy GG, Alex AT, Mudgal J (2020) Neurodegenerative pathways in Alzheimer's disease: a review. Curr Neuropharmacol. https://doi.org/10.2174/1570159X18666200807130637
Atif F, Yousuf S, Espinosa-Garcia C, Harris WAC, Stein DG (2020) Post-ischemic stroke systemic inflammation: immunomodulation by progesterone and vitamin D hormone. Neuropharmacology. 181:108327
pubmed: 32950558
doi: 10.1016/j.neuropharm.2020.108327
Babaei P, Damirchi A, Hoseini Z, Hoseini R (2019) Co-treatment of vitamin D supplementation and aerobic training improves memory deficit in ovariectomized rat. Int J Neurosci 130(6):595–600
Balmus IM, Ciobica A (2017) Main plant extracts' active properties effective on scopolamine-induced memory loss. Am J Alzheimers Dis Other Dement 32(7):418–428
doi: 10.1177/1533317517715906
Beheshti F, Karimi S, Vafaee F, Shafei MN, Sadeghnia HR, Hadjzadeh MAR et al (2017) The effects of vitamin C on hypothyroidism-associated learning and memory impairment in juvenile rats. Metab Brain Dis 32(3):703–715
pubmed: 28127705
doi: 10.1007/s11011-017-9954-y
Bivona G, Gambino CM, Iacolino G, Ciaccio M, Vitamin D (2019) the nervous system. Neurol Res 41(9):827–835
pubmed: 31142227
doi: 10.1080/01616412.2019.1622872
Bostanciklioglu M (2019) An update on the interactions between Alzheimer's disease, autophagy and inflammation. Gene. 705:157–166
pubmed: 31029603
doi: 10.1016/j.gene.2019.04.040
Bothwell M (2014) NGF, BDNF, NT3, and NT4. Handb Exp Pharmacol 220:3–15
Camara AB, Brandao IA (2019) The relationship between vitamin D deficiency and oxidative stress can be independent of age and gender. Int J Vitam Nutr Res 91(1–2):108–123
Cenini G, Lloret A, Cascella R (2019) Oxidative stress in neurodegenerative diseases: from a mitochondrial point of view. Oxidative Med Cell Longev 2019:2105607
doi: 10.1155/2019/2105607
Chang JM, Kuo MC, Kuo HT, Hwang SJ, Tsai JC, Chen HC et al (2004) 1-alpha,25-Dihydroxyvitamin D3 regulates inducible nitric oxide synthase messenger RNA expression and nitric oxide release in macrophage-like RAW 264.7 cells. J Lab Clin Med 143(1):14–22
pubmed: 14749681
doi: 10.1016/j.lab.2003.08.002
Chen WN, Yeong KY (2020) Scopolamine, a toxin-induced experimental model, used for research in Alzheimer's disease. CNS Neurol Disord Drug Targets 19(2):85–93
pubmed: 32056532
doi: 10.2174/1871527319666200214104331
Cheng YW, Chang CC, Chang TS, Li HH, Hung HC, Liu GY et al (2019) Abeta stimulates microglial activation through antizyme-dependent downregulation of ornithine decarboxylase. J Cell Physiol 234(6):9733–9745
pubmed: 30417362
doi: 10.1002/jcp.27659
Cho N, Lee KY, Huh J, Choi JH, Yang H, Jeong EJ et al (2013) Cognitive-enhancing effects of Rhus verniciflua bark extract and its active flavonoids with neuroprotective and anti-inflammatory activities. Food Chem Toxicol 58:355–361
pubmed: 23688860
doi: 10.1016/j.fct.2013.05.007
Cui X, Gooch H, Petty A, McGrath JJ, Eyles D, Vitamin D (2017) the brain: genomic and non-genomic actions. Mol Cell Endocrinol 453:131–143
pubmed: 28579120
doi: 10.1016/j.mce.2017.05.035
Dursun E, Gezen-Ak D (2013) Yilmazer S. A new mechanism for amyloid-β induction of iNOS: vitamin D-VDR pathway disruption. J Alzheimers Dis 36(3):459–474
pubmed: 23624519
doi: 10.3233/JAD-130416
Fan YG, Pang ZQ, Wu TY, Zhang YH, Xuan WQ, Wang Z et al (2020) Vitamin D deficiency exacerbates Alzheimer-like pathologies by reducing antioxidant capacity. Free Radic Biol Med 161:139–149
pubmed: 33068737
doi: 10.1016/j.freeradbiomed.2020.10.007
Farina N, Page TE, Daley S, Brown A, Bowling A, Basset T, Livingston G, Knapp M, Murray J, Banerjee S (2017) Factors associated with the quality of life of family carers of people with dementia: A systematic review. Alzheimers Dement 13(5):572–581
Fernandes de Abreu DA, Eyles D, Feron F, Vitamin D (2009) a neuro-immunomodulator: implications for neurodegenerative and autoimmune diseases. Psychoneuroendocrinology. 34(Suppl 1):S265–S277
pubmed: 19545951
doi: 10.1016/j.psyneuen.2009.05.023
Fukasawa H, Nakagomi M, Yamagata N, Katsuki H, Kawahara K, Kitaoka K et al (2012) Tamibarotene: a candidate retinoid drug for Alzheimer's disease. Biol Pharm Bull 35(8):1206–1212
pubmed: 22863914
doi: 10.1248/bpb.b12-00314
Garcion E, Wion-Barbot N, Montero-Menei CN, Berger F, Wion D (2002) New clues about vitamin D functions in the nervous system. Trends Endocrinol Metab 13(3):100–105
pubmed: 11893522
doi: 10.1016/S1043-2760(01)00547-1
Gascon-Barré M, Huet PM (1983) Apparent [3H]1,25-dihydroxyvitamin D3 uptake by canine and rodent brain. Am J Phys 244(3):E266–E271
Giridharan VV, Thandavarayan RA, Sato S, Ko KM, Konishi T (2011) Prevention of scopolamine-induced memory deficits by schisandrin B, an antioxidant lignan from Schisandra chinensis in mice. Free Radic Res 45(8):950–958
pubmed: 21615274
doi: 10.3109/10715762.2011.571682
Gonzalez MC, Radiske A, Cammarota M (2019) On the Involvement of BDNF signaling in memory reconsolidation. Front Cell Neurosci 13:383
pubmed: 31507380
pmcid: 6713924
doi: 10.3389/fncel.2019.00383
Grecksch G, Rüthrich H, Höllt V, Becker A (2009) Transient prenatal vitamin D deficiency is associated with changes of synaptic plasticity in the dentate gyrus in adult rats. Psychoneuroendocrinology. 34(Suppl 1):S258–S264
pubmed: 19647946
doi: 10.1016/j.psyneuen.2009.07.004
Guo W, Nagappan G, Lu B (2018) Differential effects of transient and sustained activation of BDNF-TrkB signaling. Dev Neurobiol 78(7):647–659
pubmed: 29575722
doi: 10.1002/dneu.22592
Hampel H, Prvulovic D, Teipel S, Jessen F, Luckhaus C, Frolich L et al (2011) The future of Alzheimer's disease: the next 10 years. Prog Neurobiol 95(4):718–728
pubmed: 22137045
doi: 10.1016/j.pneurobio.2011.11.008
Haussler MR, Jurutka PW, Mizwicki M, Norman AW (2011) Vitamin D receptor (VDR)-mediated actions of 1α,25(OH)
pubmed: 21872797
doi: 10.1016/j.beem.2011.05.010
Hofer M, Pagliusi SR, Hohn A, Leibrock J, Barde YA (1990) Regional distribution of brain-derived neurotrophic factor mRNA in the adult mouse brain. EMBO J 9(8):2459–2464
pubmed: 2369898
pmcid: 552273
doi: 10.1002/j.1460-2075.1990.tb07423.x
Jamilian H, Amirani E, Milajerdi A, Kolahdooz F, Mirzaei H, Zaroudi M et al (2019) The effects of vitamin D supplementation on mental health, and biomarkers of inflammation and oxidative stress in patients with psychiatric disorders: a systematic review and meta-analysis of randomized controlled trials. Prog Neuro-Psychopharmacol Biol Psychiatry 94:109651
doi: 10.1016/j.pnpbp.2019.109651
Jayedi A, Rashidy-Pour A, Shab-Bidar S (2019) Vitamin D status and risk of dementia and Alzheimer's disease: a meta-analysis of dose-response (dagger). Nutr Neurosci 22(11):750–759
pubmed: 29447107
doi: 10.1080/1028415X.2018.1436639
Khairy EY, Attia MM (2019) Protective effects of vitamin D on neurophysiologic alterations in brain aging: role of brain-derived neurotrophic factor (BDNF). Nutr Neurosci 1–10. https://doi.org/10.1080/1028415X.2019.1665854
Koshkina A, Dudnichenko T, Baranenko D, Fedotova J, Drago F (2019) Effects of Vitamin D3 in long-term ovariectomized rats subjected to chronic unpredictable mild stress: BDNF, NT-3, and NT-4 implications. Nutrients 11(8):1726
pmcid: 6723744
doi: 10.3390/nu11081726
Latimer CS, Brewer LD, Searcy JL, Chen KC, Popović J, Kraner SD et al (2014) Vitamin D prevents cognitive decline and enhances hippocampal synaptic function in aging rats. Proc Natl Acad Sci U S A 111(41):E4359–E4366
pubmed: 25267625
pmcid: 4205629
doi: 10.1073/pnas.1404477111
Lin CI, Chang YC, Kao NJ, Lee WJ, Cross TW, Lin SH (2020) 1,25(OH)(2)D(3) alleviates Aβ(25-35)-induced tau hyperphosphorylation, excessive reactive oxygen species, and apoptosis through interplay with glial cell line-derived neurotrophic factor signaling in SH-SY5Y cells. Int J Mol Sci 21(12):4215
pmcid: 7352552
doi: 10.3390/ijms21124215
Littlejohns TJ, Henley WE, Lang IA, Annweiler C, Beauchet O, Chaves PH et al (2014) Vitamin D and the risk of dementia and Alzheimer disease. Neurology. 83(10):920–928
pubmed: 25098535
pmcid: 4153851
doi: 10.1212/WNL.0000000000000755
Madesh M, Balasubramanian K (1998) Microtiter plate assay for superoxide dismutase using MTT reduction by superoxide. Indian J Biochem Biophys 35(3):184–188
pubmed: 9803669
Mangialasche F, Solomon A, Winblad B, Mecocci P, Kivipelto M (2010) Alzheimer's disease: clinical trials and drug development. Lancet Neurol 9(7):702–716
pubmed: 20610346
doi: 10.1016/S1474-4422(10)70119-8
Masoumi A, Goldenson B, Ghirmai S, Avagyan H, Zaghi J, Abel K et al (2009) 1alpha,25-dihydroxyvitamin D3 interacts with curcuminoids to stimulate amyloid-beta clearance by macrophages of Alzheimer's disease patients. J Alzheimers Dis 17(3):703–717
pubmed: 19433889
doi: 10.3233/JAD-2009-1080
Mecocci P, Boccardi V, Cecchetti R, Bastiani P, Scamosci M, Ruggiero C et al (2018) A long journey into aging, brain aging, and Alzheimer's disease following the oxidative stress tracks. J Alzheimers Dis 62(3):1319–1335
pubmed: 29562533
pmcid: 5870006
doi: 10.3233/JAD-170732
Medhat E, Rashed L, Abdelgwad M, Aboulhoda BE, Khalifa MM, El-Din SS (2020) Exercise enhances the effectiveness of vitamin D therapy in rats with Alzheimer's disease: emphasis on oxidative stress and inflammation. Metab Brain Dis 35(1):111–120
Miranda M, Morici JF, Zanoni MB, Bekinschtein P (2019) Brain-derived neurotrophic factor: a key molecule for memory in the healthy and the pathological brain. Front Cell Neurosci 13:363
pubmed: 31440144
pmcid: 6692714
doi: 10.3389/fncel.2019.00363
Mokhtari-Zaer A, Hosseini M, Salmani H, Arab Z, Zareian P (2020) Vitamin D3 attenuates lipopolysaccharide-induced cognitive impairment in rats by inhibiting inflammation and oxidative stress. Life Sci 253:117703
pubmed: 32334010
doi: 10.1016/j.lfs.2020.117703
Navabi SP, Sarkaki A, Mansouri E, Badavi M, Ghadiri A, Farbood Y (2018) The effects of betulinic acid on neurobehavioral activity, electrophysiology and histological changes in an animal model of the Alzheimer's disease. Behav Brain Res 337:99–106
pubmed: 28986104
doi: 10.1016/j.bbr.2017.10.002
Naveilhan P, Neveu I, Baudet C, Funakoshi H, Wion D, Brachet P et al (1996) 1,25-Dihydroxyvitamin D3 regulates the expression of the low-affinity neurotrophin receptor. Brain Res Mol Brain Res 41(1-2):259–268
pubmed: 8883959
doi: 10.1016/0169-328X(96)00103-9
Neveu I, Naveilhan P, Baudet C, Brachet P, Metsis M (1994) 1,25-dihydroxyvitamin D3 regulates NT-3, NT-4 but not BDNF mRNA in astrocytes. Neuroreport 6(1):124–126
pubmed: 7703399
doi: 10.1097/00001756-199412300-00032
Ng TKS, Ho CSH, Tam WWS, Kua EH, Ho RC (2019) Decreased serum brain-derived neurotrophic factor (BDNF) levels in patients with Alzheimer’s disease (AD): a systematic review and meta-analysis. Int J Mol Sci 20(2):257
Overeem K, Alexander S, Burne THJ, Ko P, Eyles DW (2019) Developmental vitamin D deficiency in the rat impairs recognition memory, but has no effect on social approach or hedonia. Nutrients. 11(11):2713
pmcid: 6893501
doi: 10.3390/nu11112713
Salami M, Talaei SA, Davari S, Taghizadeh M (2012) Hippocampal long term potentiation in rats under different regimens of vitamin D: an in vivo study. Neurosci Lett 509(1):56–59
pubmed: 22227619
doi: 10.1016/j.neulet.2011.12.050
Saleh SR, Abady MM, Nofal M, Yassa NW, Abdel-Latif MS, Nounou MI et al (2020) Berberine nanoencapsulation attenuates hallmarks of scoplomine induced Alzheimer's-like disease in rats. Curr Clin Pharmacol. https://doi.org/10.2174/1574884715666200628112844
Sanders KM, Stuart AL, Williamson EJ, Jacka FN, Dodd S, Nicholson G et al (2011) Annual high-dose vitamin D3 and mental well-being: randomised controlled trial. Br J Psychiatry 198(5):357–364
pubmed: 21525520
doi: 10.1192/bjp.bp.110.087544
Sepehrmanesh Z, Kolahdooz F, Abedi F, Mazroii N, Assarian A, Asemi Z et al (2016) Vitamin D supplementation affects the Beck Depression Inventory, insulin resistance, and biomarkers of oxidative stress in patients with major depressive disorder: a randomized, controlled clinical trial. J Nutr 146(2):243–248
pubmed: 26609167
doi: 10.3945/jn.115.218883
Smolders J, Moen SM, Damoiseaux J, Huitinga I, Holmoy T (2011) Vitamin D in the healthy and inflamed central nervous system: access and function. J Neurol Sci 311(1-2):37–43
pubmed: 21862439
doi: 10.1016/j.jns.2011.07.033
Sun K, Bai Y, Zhao R, Guo Z, Su X, Li P et al (2019) Neuroprotective effects of matrine on scopolamine-induced amnesia via inhibition of AChE/BuChE and oxidative stress. Metab Brain Dis 34(1):173–181
pubmed: 30406376
doi: 10.1007/s11011-018-0335-y
Taghizadeh M, Talaei SA, Djazayeri A, Salami M (2014) Vitamin D supplementation restores suppressed synaptic plasticity in Alzheimer's disease. Nutr Neurosci 17(4):172–177
pubmed: 23883541
doi: 10.1179/1476830513Y.0000000080
Taheri Moghadam M, Asadi Fard Y, Saki G, Nikbakht R (2019) Effect of vitamin D on apoptotic marker, reactive oxygen species and human sperm parameters during the process of cryopreservation. Iran J Basic Med Sci 22(9):1036–1043
pubmed: 31807247
pmcid: 6880532
Tang KS (2019) The cellular and molecular processes associated with scopolamine-induced memory deficit: a model of Alzheimer's biomarkers. Life Sci 233:116695
pubmed: 31351082
doi: 10.1016/j.lfs.2019.116695
Timmusk T, Palm K, Metsis M, Reintam T, Paalme V, Saarma M et al (1993) Multiple promoters direct tissue-specific expression of the rat BDNF gene. Neuron. 10(3):475–489
pubmed: 8461137
doi: 10.1016/0896-6273(93)90335-O
Willems HM, van den Heuvel EG, Carmeliet G, Schaafsma A, Klein-Nulend J (2012) Bakker AD. VDR dependent and independent effects of 1,25-dihydroxyvitamin D3 on nitric oxide production by osteoblasts. Steroids. 77(1-2):126–131
pubmed: 22093484
doi: 10.1016/j.steroids.2011.10.015
Wrzosek M, Lukaszkiewicz J, Wrzosek M, Jakubczyk A, Matsumoto H, Piatkiewicz P et al (2013) Vitamin D and the central nervous system. Pharmacol Rep 65(2):271–278
pubmed: 23744412
doi: 10.1016/S1734-1140(13)71003-X
Xu Y, Liang L (2020) Vitamin D3/vitamin D receptor signaling mitigates symptoms of post-stroke depression in mice by upregulating hippocampal BDNF expression. Neurosci Res. https://doi.org/10.1016/j.neures.2020.08.002
Yang Q, Huang Q, Hu Z, Tang X (2019) Potential neuroprotective treatment of stroke: targeting excitotoxicity, oxidative stress, and inflammation. Front Neurosci 13:1036
pubmed: 31611768
pmcid: 6777147
doi: 10.3389/fnins.2019.01036
Yosaee S, Soltani S, Esteghamati A, Motevalian SA, Tehrani-Doost M, Clark CCT et al (2019) Effects of zinc, vitamin D, and their co-supplementation on mood, serum cortisol, and brain-derived neurotrophic factor in patients with obesity and mild to moderate depressive symptoms: a phase II, 12-wk, 2x2 factorial design, double-blind, randomized, placebo-controlled trial. Nutrition. 71:110601
pubmed: 31837640
doi: 10.1016/j.nut.2019.110601
Zhu X, Raina AK, Lee HG, Casadesus G, Smith MA, Perry G (2004) Oxidative stress signalling in Alzheimer's disease. Brain Res 1000(1-2):32–39
pubmed: 15053949
doi: 10.1016/j.brainres.2004.01.012