Skip to main content
Top
Published in: Behavioral and Brain Functions 1/2019

Open Access 01-12-2019 | Research

Neuroprotective effects of Withania somnifera in BPA induced-cognitive dysfunction and oxidative stress in mice

Authors: Hareram Birla, Chetan Keswani, Sachchida Nand Rai, Saumitra Sen Singh, Walia Zahra, Hagera Dilnashin, Aaina Singh Rathore, Surya Pratap Singh

Published in: Behavioral and Brain Functions | Issue 1/2019

Login to get access

Abstract

Background

Bisphenol A (BPA), a major endocrine disruptor and a xenobiotic compound is used abundantly in the production of polycarbonate plastics and epoxy resins. Human exposure to this compound is primarily via its leaching from the protective internal epoxy resin coatings of containers into the food and beverages. In addition, the plastics used in dental prostheses and sealants also contain considerable amount of BPA and have a high risk of human exposure. Since it is a well-known endocrine disruptor and closely mimics the molecular structure of human estrogen thereby impairing learning and memory. Withania somnifera (Ws), commonly known as Ashwagandha is known for its varied therapeutic uses in Ayurvedic system of medicine. The present study was undertaken to demonstrate the impairment induced by BPA on the spatial learning, working memory and its alleviation by Ws in Swiss albino mice. The study was conducted on thirty Swiss albino mice, randomly distributed among three groups: control, BPA and BPA + Ws. The behavioral recovery after treatment with Ws was investigated using the Y-maize and Morris water maize test. Whereas, for the estimation of recovery of NMDA receptor which is related to learning and memory in hippocampus region by western blot and immunohistochemistry. Furthermore, the oxidative stress and antioxidant level was assessed by biochemical tests like MDA, SOD and catalase.

Results

The study revealed that administration of Ws alleviated the behavioral deficits induced by BPA. Alongside, Ws treatment reinstated the number of NMDA receptors in hippocampus region and showed anti-oxidative property while ameliorating the endogenous anti-oxidant level in the brain.

Conclusion

These findings suggest that Ws significantly ameliorates the level of BPA intoxicated oxidative stress thereby potentially treating cognitive dysfunction which acts as the primary symptom in a number of neurodegenerative diseases.
Literature
1.
go back to reference Fromme H, Küchler T, Otto T, Pilz K, Müller J, Wenzel A. Occurrence of phthalates and bisphenol A and F in the environment. Water Res. 2002;36(6):1429–38.PubMed Fromme H, Küchler T, Otto T, Pilz K, Müller J, Wenzel A. Occurrence of phthalates and bisphenol A and F in the environment. Water Res. 2002;36(6):1429–38.PubMed
2.
go back to reference Vandenberg LN, Hauser R, Marcus M, Olea N, Welshons WV. Human exposure to bisphenol A (BPA). Reprod Toxicol. 2007;24(2):139–77.PubMed Vandenberg LN, Hauser R, Marcus M, Olea N, Welshons WV. Human exposure to bisphenol A (BPA). Reprod Toxicol. 2007;24(2):139–77.PubMed
3.
go back to reference Geens T, Aerts D, Berthot C, Bourguignon J-P, Goeyens L, Lecomte P, et al. A review of dietary and non-dietary exposure to bisphenol-A. Food Chem Toxicol. 2012;50(10):3725–40.PubMed Geens T, Aerts D, Berthot C, Bourguignon J-P, Goeyens L, Lecomte P, et al. A review of dietary and non-dietary exposure to bisphenol-A. Food Chem Toxicol. 2012;50(10):3725–40.PubMed
4.
go back to reference Rochester JR, Bolden AL. Bisphenol S and F: a systematic review and comparison of the hormonal activity of bisphenol A substitutes. Environ Health Perspect. 2015;123(7):643–50.PubMedPubMedCentral Rochester JR, Bolden AL. Bisphenol S and F: a systematic review and comparison of the hormonal activity of bisphenol A substitutes. Environ Health Perspect. 2015;123(7):643–50.PubMedPubMedCentral
5.
go back to reference Ribeiro E, Ladeira C, Viegas S. Occupational exposure to bisphenol A (BPA): a reality that still needs to be unveiled. Toxics. 2017;5(3):22.PubMedCentral Ribeiro E, Ladeira C, Viegas S. Occupational exposure to bisphenol A (BPA): a reality that still needs to be unveiled. Toxics. 2017;5(3):22.PubMedCentral
6.
go back to reference Kawato S. Endocrine disrupters as disrupters of brain function: a neurosteroid viewpoint. Environ Sci. 2004;11(1):1–14.PubMed Kawato S. Endocrine disrupters as disrupters of brain function: a neurosteroid viewpoint. Environ Sci. 2004;11(1):1–14.PubMed
7.
go back to reference Chin-Chan M, Navarro-Yepes J, Quintanilla-Vega B. Environmental pollutants as risk factors for neurodegenerative disorders: Alzheimer and Parkinson diseases. Front Cell Neurosci. 2015;9:124.PubMedPubMedCentral Chin-Chan M, Navarro-Yepes J, Quintanilla-Vega B. Environmental pollutants as risk factors for neurodegenerative disorders: Alzheimer and Parkinson diseases. Front Cell Neurosci. 2015;9:124.PubMedPubMedCentral
9.
go back to reference Gilmour G, Dix S, Fellini L, Gastambide F, Plath N, Steckler T, et al. NMDA receptors, cognition and schizophrenia-testing the validity of the NMDA receptor hypofunction hypothesis. Neuropharmacology. 2012;62(3):1401–12.PubMed Gilmour G, Dix S, Fellini L, Gastambide F, Plath N, Steckler T, et al. NMDA receptors, cognition and schizophrenia-testing the validity of the NMDA receptor hypofunction hypothesis. Neuropharmacology. 2012;62(3):1401–12.PubMed
10.
go back to reference Xu X, Li T, Luo Q, Hong X, Xie L, Tian D. Bisphenol-A rapidly enhanced passive avoidance memory and phosphorylation of NMDA receptor subunits in hippocampus of young rats. Toxicol Appl Pharmacol. 2011;255(2):221–8.PubMed Xu X, Li T, Luo Q, Hong X, Xie L, Tian D. Bisphenol-A rapidly enhanced passive avoidance memory and phosphorylation of NMDA receptor subunits in hippocampus of young rats. Toxicol Appl Pharmacol. 2011;255(2):221–8.PubMed
11.
go back to reference Dar PA, Singh LR, Kamal MA, Dar TA. Unique medicinal properties of Withania somnifera: phytochemical constituents and protein component. Curr Pharm Des. 2016;22(5):535–40.PubMed Dar PA, Singh LR, Kamal MA, Dar TA. Unique medicinal properties of Withania somnifera: phytochemical constituents and protein component. Curr Pharm Des. 2016;22(5):535–40.PubMed
12.
go back to reference Keswani C, Bisen K, Singh S, Singh H. Traditional knowledge and medicinal plants of India in intellectual property landscape. Med Plants Int J Phytomed Relat Ind. 2017;9(1):1–11. Keswani C, Bisen K, Singh S, Singh H. Traditional knowledge and medicinal plants of India in intellectual property landscape. Med Plants Int J Phytomed Relat Ind. 2017;9(1):1–11.
13.
go back to reference Baitharu I, Jain V, Deep SN, Hota KB, Hota SK, Prasad D, et al. Withania somnifera root extract ameliorates hypobaric hypoxia induced memory impairment in rats. J Ethnopharmacol. 2013;145(2):431–41 (PubMed PMID: 23211660. Epub 2012/12/06. eng).PubMed Baitharu I, Jain V, Deep SN, Hota KB, Hota SK, Prasad D, et al. Withania somnifera root extract ameliorates hypobaric hypoxia induced memory impairment in rats. J Ethnopharmacol. 2013;145(2):431–41 (PubMed PMID: 23211660. Epub 2012/12/06. eng).PubMed
14.
go back to reference Choudhary D, Bhattacharyya S, Bose S. Efficacy and safety of Ashwagandha (Withania somnifera (L.) Dunal) root extract in improving memory and cognitive functions. J Diet Suppl. 2017;14(6):599–612.PubMed Choudhary D, Bhattacharyya S, Bose S. Efficacy and safety of Ashwagandha (Withania somnifera (L.) Dunal) root extract in improving memory and cognitive functions. J Diet Suppl. 2017;14(6):599–612.PubMed
15.
go back to reference Verma SK, Kumar A. Therapeutic uses of Withania somnifera (Ashwagandha) with a note on with anolides and its pharmacological actions. Asian J Pharm Clin Res. 2011;4(1):1–4. Verma SK, Kumar A. Therapeutic uses of Withania somnifera (Ashwagandha) with a note on with anolides and its pharmacological actions. Asian J Pharm Clin Res. 2011;4(1):1–4.
16.
go back to reference Prakash J, Yadav SK, Chouhan S, Singh SP. Neuroprotective role of Withania somnifera root extract in Maneb–Paraquat induced mouse model of parkinsonism. Neurochem Res. 2013;38(5):972–80.PubMed Prakash J, Yadav SK, Chouhan S, Singh SP. Neuroprotective role of Withania somnifera root extract in Maneb–Paraquat induced mouse model of parkinsonism. Neurochem Res. 2013;38(5):972–80.PubMed
17.
go back to reference Bhattacharya A, Ghosal S, Bhattacharya S. Anti-oxidant effect of Withania somnifera glycowithanolides in chronic footshock stress-induced perturbations of oxidative free radical scavenging enzymes and lipid peroxidation in rat frontal cortex and striatum. J Ethnopharmacol. 2001;74(1):1–6.PubMed Bhattacharya A, Ghosal S, Bhattacharya S. Anti-oxidant effect of Withania somnifera glycowithanolides in chronic footshock stress-induced perturbations of oxidative free radical scavenging enzymes and lipid peroxidation in rat frontal cortex and striatum. J Ethnopharmacol. 2001;74(1):1–6.PubMed
18.
go back to reference Schliebs R, Liebmann A, Bhattacharya SK, Kumar A, Ghosal S, Bigl V. Systemic administration of defined extracts from Withania somnifera (Indian Ginseng) and Shilajit differentially affects cholinergic but not glutamatergic and GABAergic markers in rat brain. Neurochem Int. 1997;30(2):181–90.PubMed Schliebs R, Liebmann A, Bhattacharya SK, Kumar A, Ghosal S, Bigl V. Systemic administration of defined extracts from Withania somnifera (Indian Ginseng) and Shilajit differentially affects cholinergic but not glutamatergic and GABAergic markers in rat brain. Neurochem Int. 1997;30(2):181–90.PubMed
19.
go back to reference King DL, Arendash GW. Behavioral characterization of the Tg2576 transgenic model of Alzheimer’s disease through 19 months. Physiol Behav. 2002;75(5):627–42.PubMed King DL, Arendash GW. Behavioral characterization of the Tg2576 transgenic model of Alzheimer’s disease through 19 months. Physiol Behav. 2002;75(5):627–42.PubMed
20.
go back to reference Kumar D, Thakur MK. Perinatal exposure to bisphenol-A impairs spatial memory through upregulation of neurexin1 and neuroligin3 expression in male mouse brain. PLoS ONE. 2014;9(10):e110482.PubMedPubMedCentral Kumar D, Thakur MK. Perinatal exposure to bisphenol-A impairs spatial memory through upregulation of neurexin1 and neuroligin3 expression in male mouse brain. PLoS ONE. 2014;9(10):e110482.PubMedPubMedCentral
21.
go back to reference Yadav SK, Pandey S, Singh B. Role of estrogen and levodopa in 1-methyl-4-pheny-l-1, 2, 3, 6-tetrahydropyridine (mptp)-induced cognitive deficit in Parkinsonian ovariectomized mice model: a comparative study. J Chem Neuroanat. 2017;85:50–9.PubMed Yadav SK, Pandey S, Singh B. Role of estrogen and levodopa in 1-methyl-4-pheny-l-1, 2, 3, 6-tetrahydropyridine (mptp)-induced cognitive deficit in Parkinsonian ovariectomized mice model: a comparative study. J Chem Neuroanat. 2017;85:50–9.PubMed
22.
go back to reference Prabhu VV, Nguyen TB, Cui Y, Oh Y-E, Lee K-H, Bagalkot TR, et al. Effects of social defeat stress on dopamine D2 receptor isoforms and proteins involved in intracellular trafficking. Behav Brain Funct. 2018;14(1):16.PubMedPubMedCentral Prabhu VV, Nguyen TB, Cui Y, Oh Y-E, Lee K-H, Bagalkot TR, et al. Effects of social defeat stress on dopamine D2 receptor isoforms and proteins involved in intracellular trafficking. Behav Brain Funct. 2018;14(1):16.PubMedPubMedCentral
23.
go back to reference Rai SN, Birla H, Singh SS, Zahra W, Patil RR, Jadhav JP, et al. Mucuna pruriens protects against MPTP Intoxicated neuroinflammation in Parkinson’s disease through NF-κB/pAKT signaling pathways. Front Aging Neurosci. 2017;9:421.PubMedPubMedCentral Rai SN, Birla H, Singh SS, Zahra W, Patil RR, Jadhav JP, et al. Mucuna pruriens protects against MPTP Intoxicated neuroinflammation in Parkinson’s disease through NF-κB/pAKT signaling pathways. Front Aging Neurosci. 2017;9:421.PubMedPubMedCentral
24.
go back to reference Kumar A, Prakash A, Dogra S. Naringin alleviates cognitive impairment, mitochondrial dysfunction and oxidative stress induced by d-galactose in mice. Food Chem Toxicol. 2010;48(2):626–32.PubMed Kumar A, Prakash A, Dogra S. Naringin alleviates cognitive impairment, mitochondrial dysfunction and oxidative stress induced by d-galactose in mice. Food Chem Toxicol. 2010;48(2):626–32.PubMed
25.
go back to reference McCord JM, Fridovich I. Superoxide dismutase an enzymic function for erythrocuprein (hemocuprein). J Biol Chem. 1969;244(22):6049–55.PubMed McCord JM, Fridovich I. Superoxide dismutase an enzymic function for erythrocuprein (hemocuprein). J Biol Chem. 1969;244(22):6049–55.PubMed
26.
go back to reference Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72(1–2):248–54.PubMed Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72(1–2):248–54.PubMed
27.
go back to reference Scheetz A, Nairn AC, Constantine-Paton M. NMDA receptor-mediated control of protein synthesis at developing synapses. Nat Neurosci. 2000;3(3):211.PubMed Scheetz A, Nairn AC, Constantine-Paton M. NMDA receptor-mediated control of protein synthesis at developing synapses. Nat Neurosci. 2000;3(3):211.PubMed
28.
go back to reference Birla H, Rai SN, Singh SS, Zahra W, Rawat A, Tiwari N, et al. Tinospora cordifolia suppresses neuroinflammation in parkinsonian mouse model. NeuroMol Med. 2019;21:42–53. Birla H, Rai SN, Singh SS, Zahra W, Rawat A, Tiwari N, et al. Tinospora cordifolia suppresses neuroinflammation in parkinsonian mouse model. NeuroMol Med. 2019;21:42–53.
29.
go back to reference Gorbatyuk OS, Li S, Sullivan LF, Chen W, Kondrikova G, Manfredsson FP, et al. The phosphorylation state of Ser-129 in human α-synuclein determines neurodegeneration in a rat model of Parkinson disease. Proc Natl Acad Sci. 2008;105(2):763–8.PubMed Gorbatyuk OS, Li S, Sullivan LF, Chen W, Kondrikova G, Manfredsson FP, et al. The phosphorylation state of Ser-129 in human α-synuclein determines neurodegeneration in a rat model of Parkinson disease. Proc Natl Acad Sci. 2008;105(2):763–8.PubMed
30.
go back to reference Singh SS, Rai SN, Birla H, Zahra W, Kumar G, Gedda MR, et al. Effect of chlorogenic acid supplementation in MPTP-intoxicated mouse. Front Pharmacol. 2018;9:757.PubMedPubMedCentral Singh SS, Rai SN, Birla H, Zahra W, Kumar G, Gedda MR, et al. Effect of chlorogenic acid supplementation in MPTP-intoxicated mouse. Front Pharmacol. 2018;9:757.PubMedPubMedCentral
31.
go back to reference Kulkarni S, Dhir A. Withania somnifera: an Indian ginseng. Prog Neuropsychopharmacol Biol Psychiatry. 2008;32(5):1093–105.PubMed Kulkarni S, Dhir A. Withania somnifera: an Indian ginseng. Prog Neuropsychopharmacol Biol Psychiatry. 2008;32(5):1093–105.PubMed
32.
go back to reference Bhatnagar M, Sharma D, Salvi M. Neuroprotective effects of Withania somnifera Dunal.: a possible mechanism. Neurochem Res. 2009;34(11):1975–83.PubMed Bhatnagar M, Sharma D, Salvi M. Neuroprotective effects of Withania somnifera Dunal.: a possible mechanism. Neurochem Res. 2009;34(11):1975–83.PubMed
33.
go back to reference Prakash J, Chouhan S, Yadav SK, Westfall S, Rai SN, Singh SP. Withania somnifera alleviates parkinsonian phenotypes by inhibiting apoptotic pathways in dopaminergic neurons. Neurochem Res. 2014;39(12):2527–36.PubMed Prakash J, Chouhan S, Yadav SK, Westfall S, Rai SN, Singh SP. Withania somnifera alleviates parkinsonian phenotypes by inhibiting apoptotic pathways in dopaminergic neurons. Neurochem Res. 2014;39(12):2527–36.PubMed
34.
go back to reference Zhao J, Nakamura N, Hattori M, Kuboyama T, Tohda C, Komatsu K. Withanolide derivatives from the roots of Withania somnifera and their neurite outgrowth activities. Chem Pharm Bull. 2002;50(6):760–5.PubMed Zhao J, Nakamura N, Hattori M, Kuboyama T, Tohda C, Komatsu K. Withanolide derivatives from the roots of Withania somnifera and their neurite outgrowth activities. Chem Pharm Bull. 2002;50(6):760–5.PubMed
35.
go back to reference Tohda C, Komatsu K, Kuboyama T. Scientific basis for the anti-dementia drugs of constituents from Ashwagandha (Withania somnifera). J Tad Med. 2005;22:176–82. Tohda C, Komatsu K, Kuboyama T. Scientific basis for the anti-dementia drugs of constituents from Ashwagandha (Withania somnifera). J Tad Med. 2005;22:176–82.
36.
go back to reference Pati PK, Sharma M, Salar RK, Sharma A, Gupta A, Singh B. Studies on leaf spot disease of Withania somnifera and its impact on secondary metabolites. Indian J Microbiol. 2008;48(4):432–7.PubMed Pati PK, Sharma M, Salar RK, Sharma A, Gupta A, Singh B. Studies on leaf spot disease of Withania somnifera and its impact on secondary metabolites. Indian J Microbiol. 2008;48(4):432–7.PubMed
37.
go back to reference Maitra R, Porter MA, Huang S, Gilmour BP. Inhibition of NFκB by the natural product Withaferin A in cellular models of cystic fibrosis inflammation. J Inflamm. 2009;6(1):15. Maitra R, Porter MA, Huang S, Gilmour BP. Inhibition of NFκB by the natural product Withaferin A in cellular models of cystic fibrosis inflammation. J Inflamm. 2009;6(1):15.
38.
go back to reference Narayan M, Zhang J, Braswell K, Gibson C, Zitnyar A, Lee DC, et al. Withaferin A regulates LRRK2 levels by interfering with the Hsp90-Cdc37 chaperone complex. Curr Aging Sci. 2015;8(3):259–65.PubMed Narayan M, Zhang J, Braswell K, Gibson C, Zitnyar A, Lee DC, et al. Withaferin A regulates LRRK2 levels by interfering with the Hsp90-Cdc37 chaperone complex. Curr Aging Sci. 2015;8(3):259–65.PubMed
39.
go back to reference Yan Z, Guo R, Gan L, Lau WB, Cao X, Zhao J, et al. Withaferin A inhibits apoptosis via activated Akt-mediated inhibition of oxidative stress. Life Sci. 2018;211:91–101.PubMed Yan Z, Guo R, Gan L, Lau WB, Cao X, Zhao J, et al. Withaferin A inhibits apoptosis via activated Akt-mediated inhibition of oxidative stress. Life Sci. 2018;211:91–101.PubMed
40.
go back to reference Banu MR, Ibrahim M, Prabhu K, Rajasankar S. Ameliorative effect of Withaferin A on ageing-mediated impairment in the dopamine system and its associated behavior of Wistar Albino Rat. Pharmacology. 2019;103(3–4):114–9. Banu MR, Ibrahim M, Prabhu K, Rajasankar S. Ameliorative effect of Withaferin A on ageing-mediated impairment in the dopamine system and its associated behavior of Wistar Albino Rat. Pharmacology. 2019;103(3–4):114–9.
41.
go back to reference Kumar A. Neuroinflammation over the life span and its impact on cognitive performance. Front Aging Neurosci. 2018;10:413.PubMedPubMedCentral Kumar A. Neuroinflammation over the life span and its impact on cognitive performance. Front Aging Neurosci. 2018;10:413.PubMedPubMedCentral
42.
go back to reference Patel SB, Rao NJ, Hingorani LL. Safety assessment of Withania somnifera extract standardized for Withaferin A: acute and sub-acute toxicity study. J Ayurveda Integr Med. 2016;7(1):30–7.PubMedPubMedCentral Patel SB, Rao NJ, Hingorani LL. Safety assessment of Withania somnifera extract standardized for Withaferin A: acute and sub-acute toxicity study. J Ayurveda Integr Med. 2016;7(1):30–7.PubMedPubMedCentral
43.
go back to reference Sharada AC, Solomon FE, Devi PU. Toxicity of Withania somnifera root extract in rats and mice. Int J Pharmacogn. 1993;31(3):205–12. Sharada AC, Solomon FE, Devi PU. Toxicity of Withania somnifera root extract in rats and mice. Int J Pharmacogn. 1993;31(3):205–12.
44.
go back to reference Bittner GD, Yang CZ, Stoner MA. Estrogenic chemicals often leach from BPA-free plastic products that are replacements for BPA-containing polycarbonate products. Environ Health. 2014;13(1):41.PubMedPubMedCentral Bittner GD, Yang CZ, Stoner MA. Estrogenic chemicals often leach from BPA-free plastic products that are replacements for BPA-containing polycarbonate products. Environ Health. 2014;13(1):41.PubMedPubMedCentral
45.
go back to reference Brown JS Jr. Effects of bisphenol-A and other endocrine disruptors compared with abnormalities of schizophrenia: an endocrine-disruption theory of schizophrenia. Schizophr Bull. 2008;35(1):256–78.PubMedPubMedCentral Brown JS Jr. Effects of bisphenol-A and other endocrine disruptors compared with abnormalities of schizophrenia: an endocrine-disruption theory of schizophrenia. Schizophr Bull. 2008;35(1):256–78.PubMedPubMedCentral
46.
go back to reference Agarwal S, Tiwari SK, Seth B, Yadav A, Singh A, Mudawal A, et al. Activation of autophagic flux against xenoestrogen bisphenol-A induced hippocampal neurodegeneration via AMPK/mTOR pathways. J Biol Chem. 2015;290:21163–84.PubMedPubMedCentral Agarwal S, Tiwari SK, Seth B, Yadav A, Singh A, Mudawal A, et al. Activation of autophagic flux against xenoestrogen bisphenol-A induced hippocampal neurodegeneration via AMPK/mTOR pathways. J Biol Chem. 2015;290:21163–84.PubMedPubMedCentral
47.
go back to reference Palanza P, Gioiosa L, vom Saal FS, Parmigiani S. Effects of developmental exposure to bisphenol A on brain and behavior in mice. Environ Res. 2008;108(2):150–7.PubMed Palanza P, Gioiosa L, vom Saal FS, Parmigiani S. Effects of developmental exposure to bisphenol A on brain and behavior in mice. Environ Res. 2008;108(2):150–7.PubMed
48.
go back to reference Kajta M, Wójtowicz AK. Impact of endocrine-disrupting chemicals on neural development and the onset of neurological disorders. Pharmacol Rep. 2013;65(6):1632–9.PubMed Kajta M, Wójtowicz AK. Impact of endocrine-disrupting chemicals on neural development and the onset of neurological disorders. Pharmacol Rep. 2013;65(6):1632–9.PubMed
49.
go back to reference Fujimoto T, Kubo K, Aou S. Prenatal exposure to bisphenol A impairs sexual differentiation of exploratory behavior and increases depression-like behavior in rats. Brain Res. 2006;1068(1):49–55.PubMed Fujimoto T, Kubo K, Aou S. Prenatal exposure to bisphenol A impairs sexual differentiation of exploratory behavior and increases depression-like behavior in rats. Brain Res. 2006;1068(1):49–55.PubMed
50.
go back to reference Xu X-H, Zhang J, Wang Y-M, Ye Y-P, Luo Q-Q. Perinatal exposure to bisphenol-A impairs learning-memory by concomitant down-regulation of N-methyl-d-aspartate receptors of hippocampus in male offspring mice. Horm Behav. 2010;58(2):326–33.PubMed Xu X-H, Zhang J, Wang Y-M, Ye Y-P, Luo Q-Q. Perinatal exposure to bisphenol-A impairs learning-memory by concomitant down-regulation of N-methyl-d-aspartate receptors of hippocampus in male offspring mice. Horm Behav. 2010;58(2):326–33.PubMed
51.
go back to reference Dudchenko PA. An overview of the tasks used to test working memory in rodents. Neurosci Biobehav Rev. 2004;28(7):699–709.PubMed Dudchenko PA. An overview of the tasks used to test working memory in rodents. Neurosci Biobehav Rev. 2004;28(7):699–709.PubMed
52.
go back to reference Kumar A, Foster TC. Alteration in NMDA receptor mediated glutamatergic neurotransmission in the hippocampus during senescence. Neurochem Res. 2019;44(1):38–48.PubMed Kumar A, Foster TC. Alteration in NMDA receptor mediated glutamatergic neurotransmission in the hippocampus during senescence. Neurochem Res. 2019;44(1):38–48.PubMed
53.
go back to reference Foster TC, Kyritsopoulos C, Kumar A. Central role for NMDA receptors in redox mediated impairment of synaptic function during aging and Alzheimer’s disease. Behav Brain Res. 2017;322(Pt B):223–32 (PubMed PMID: 27180169. Epub 2016/05/18. eng).PubMed Foster TC, Kyritsopoulos C, Kumar A. Central role for NMDA receptors in redox mediated impairment of synaptic function during aging and Alzheimer’s disease. Behav Brain Res. 2017;322(Pt B):223–32 (PubMed PMID: 27180169. Epub 2016/05/18. eng).PubMed
54.
go back to reference Berlett BS, Stadtman ER. Protein oxidation in aging, disease, and oxidative stress. J Biol Chem. 1997;272(33):20313–6.PubMed Berlett BS, Stadtman ER. Protein oxidation in aging, disease, and oxidative stress. J Biol Chem. 1997;272(33):20313–6.PubMed
55.
go back to reference Barnham KJ, Masters CL, Bush AI. Neurodegenerative diseases and oxidative stress. Nat Rev Drug Discov. 2004;3(3):205.PubMed Barnham KJ, Masters CL, Bush AI. Neurodegenerative diseases and oxidative stress. Nat Rev Drug Discov. 2004;3(3):205.PubMed
56.
go back to reference Muthuvel R, Venkataraman P, Krishnamoorthy G, Gunadharini D, Kanagaraj P, Stanley AJ, et al. Antioxidant effect of ascorbic acid on PCB (Aroclor 1254) induced oxidative stress in hypothalamus of albino rats. Clin Chim Acta. 2006;365(1–2):297–303.PubMed Muthuvel R, Venkataraman P, Krishnamoorthy G, Gunadharini D, Kanagaraj P, Stanley AJ, et al. Antioxidant effect of ascorbic acid on PCB (Aroclor 1254) induced oxidative stress in hypothalamus of albino rats. Clin Chim Acta. 2006;365(1–2):297–303.PubMed
57.
go back to reference Bindhumol V, Chitra K, Mathur P. Bisphenol A induces reactive oxygen species generation in the liver of male rats. Toxicology. 2003;188(2–3):117–24.PubMed Bindhumol V, Chitra K, Mathur P. Bisphenol A induces reactive oxygen species generation in the liver of male rats. Toxicology. 2003;188(2–3):117–24.PubMed
58.
go back to reference Chitra K, Latchoumycandane C, Mathur P. Induction of oxidative stress by bisphenol A in the epididymal sperm of rats. Toxicology. 2003;185(1–2):119–27.PubMed Chitra K, Latchoumycandane C, Mathur P. Induction of oxidative stress by bisphenol A in the epididymal sperm of rats. Toxicology. 2003;185(1–2):119–27.PubMed
59.
go back to reference Richter CA, Taylor JA, Ruhlen RL, Welshons WV, vom Saal FS. Estradiol and bisphenol A stimulate androgen receptor and estrogen receptor gene expression in fetal mouse prostate mesenchyme cells. Environ Health Perspect. 2007;115(6):902.PubMedPubMedCentral Richter CA, Taylor JA, Ruhlen RL, Welshons WV, vom Saal FS. Estradiol and bisphenol A stimulate androgen receptor and estrogen receptor gene expression in fetal mouse prostate mesenchyme cells. Environ Health Perspect. 2007;115(6):902.PubMedPubMedCentral
60.
go back to reference Aydoğan M, Korkmaz A, Barlas N, Kolankaya D. The effect of vitamin C on bisphenol A, nonylphenol and octylphenol induced brain damages of male rats. Toxicology. 2008;249(1):35–9.PubMed Aydoğan M, Korkmaz A, Barlas N, Kolankaya D. The effect of vitamin C on bisphenol A, nonylphenol and octylphenol induced brain damages of male rats. Toxicology. 2008;249(1):35–9.PubMed
61.
go back to reference Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol. 2007;39(1):44–84.PubMed Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol. 2007;39(1):44–84.PubMed
62.
go back to reference RajaSankar S, Manivasagam T, Sankar V, Prakash S, Muthusamy R, Krishnamurti A, et al. Withania somnifera root extract improves catecholamines and physiological abnormalities seen in a Parkinson’s disease model mouse. J Ethnopharmacol. 2009;125(3):369–73.PubMed RajaSankar S, Manivasagam T, Sankar V, Prakash S, Muthusamy R, Krishnamurti A, et al. Withania somnifera root extract improves catecholamines and physiological abnormalities seen in a Parkinson’s disease model mouse. J Ethnopharmacol. 2009;125(3):369–73.PubMed
63.
go back to reference Lièvre V, Becuwe P, Bianchi A, Koziel V, Franck P, Schroeder H, et al. Free radical production and changes in superoxide dismutases associated with hypoxia/reoxygenation-induced apoptosis of embryonic rat forebrain neurons in culture. Free Radic Biol Med. 2000;29(12):1291–301.PubMed Lièvre V, Becuwe P, Bianchi A, Koziel V, Franck P, Schroeder H, et al. Free radical production and changes in superoxide dismutases associated with hypoxia/reoxygenation-induced apoptosis of embryonic rat forebrain neurons in culture. Free Radic Biol Med. 2000;29(12):1291–301.PubMed
64.
go back to reference Sehgal N, Gupta A, Valli RK, Joshi SD, Mills JT, Hamel E, et al. Withania somnifera reverses Alzheimer’s disease pathology by enhancing low-density lipoprotein receptor-related protein in liver. Proc Natl Acad Sci. 2012;109(9):3510–5.PubMed Sehgal N, Gupta A, Valli RK, Joshi SD, Mills JT, Hamel E, et al. Withania somnifera reverses Alzheimer’s disease pathology by enhancing low-density lipoprotein receptor-related protein in liver. Proc Natl Acad Sci. 2012;109(9):3510–5.PubMed
Metadata
Title
Neuroprotective effects of Withania somnifera in BPA induced-cognitive dysfunction and oxidative stress in mice
Authors
Hareram Birla
Chetan Keswani
Sachchida Nand Rai
Saumitra Sen Singh
Walia Zahra
Hagera Dilnashin
Aaina Singh Rathore
Surya Pratap Singh
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Behavioral and Brain Functions / Issue 1/2019
Electronic ISSN: 1744-9081
DOI
https://doi.org/10.1186/s12993-019-0160-4

Other articles of this Issue 1/2019

Behavioral and Brain Functions 1/2019 Go to the issue