Skip to main content

Advertisement

SpringerLink
Log in

Bisphenol-A Mediated Inhibition of Hippocampal Neurogenesis Attenuated by Curcumin via Canonical Wnt Pathway

  • Published:
Molecular Neurobiology Aims and scope Submit manuscript

A Correction to this article was published on 28 June 2019

This article has been updated

Abstract

Bisphenol A (BPA) is an environmental xenoestrogenic endocrine disruptor, utilized for production of consumer products, and exerts adverse effects on the developing nervous system. Recently, we found that BPA impairs the finely tuned dynamic processes of neurogenesis (generation of new neurons) in the hippocampus of the developing rat brain. Curcumin is a natural polyphenolic compound, which provides neuroprotection against various environmental neurotoxicants and in the cellular and animal models of neurodegenerative disorders. Here, we have assessed the neuroprotective efficacy of curcumin against BPA-mediated reduced neurogenesis and the underlying cellular and molecular mechanism(s). Both in vitro and in vivo studies showed that curcumin protects against BPA-induced hippocampal neurotoxicity. Curcumin protects against BPA-mediated reduced neural stem cells (NSC) proliferation and neuronal differentiation and enhanced neurodegeneration. Curcumin also enhances the expression/levels of neurogenic and the Wnt pathway genes/proteins, which were reduced due to BPA exposure in the hippocampus. Curcumin-mediated neuroprotection against BPA-induced neurotoxicity involved activation of the Wnt/β-catenin signaling pathway, which was confirmed by the use of Wnt specific activators (LiCl and GSK-3β siRNA) and inhibitor (Dkk-1). BPA-mediated increased β-catenin phosphorylation, decreased GSK-3β levels, and β-catenin nuclear translocation were significantly reversed by curcumin, leading to enhanced neurogenesis. Curcumin-induced protective effects on neurogenesis were blocked by Dkk-1 in NSC culture treated with BPA. Curcumin-mediated enhanced neurogenesis was correlated well with improved learning and memory in BPA-treated rats. Overall, our results conclude that curcumin provides neuroprotection against BPA-mediated impaired neurogenesis via activation of the Wnt/β-catenin signaling pathway.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

Change history

  • 28 June 2019

    Correction to be published. The authors regret that inadvertent errors were observed in Fig.��3A, 5A&D and 8D. The corrected representative images are now incorporated. These corrections do not change the conclusions, text of the article and figure legends.

  • 28 June 2019

    Correction to be published. The authors regret that inadvertent errors were observed in Fig.��3A, 5A&D and 8D. The corrected representative images are now incorporated. These corrections do not change the conclusions, text of the article and figure legends.

Abbreviations

BPA:

Bisphenol A

NSC:

Neural stem cells

NPC:

Neural progenitor cells

HP:

Hippocampus

SVZ:

Subventricular zone

SGZ:

Subgranular zone

AD:

Alzheimer’s disease

PD:

Parkinson’s disease

HD:

Huntington’s disease

DCX:

Doublecortin

GD:

Gestational day

PND:

Postnatal day

GFAP:

Glial fibrillary acidic protein

References

  1. Kempermann G, Jessberger S, Steiner B, Kronenberg G (2004) Milestones of neuronal development in the adult hippocampus. Trends Neurosci 27:447–452

    Article  CAS  PubMed  Google Scholar 

  2. Zhao C, Deng W, Gage FH (2008) Mechanisms and functional implications of adult neurogenesis. Cell 132:645–660

    Article  CAS  PubMed  Google Scholar 

  3. Antonova E, Sharma T, Morris R, Kumari V (2004) The relationship between brain structure and neurocognition in schizophrenia: a selective review. Schizophr Res 70:117–145

    Article  PubMed  Google Scholar 

  4. Keller SS, Roberts N (2008) Voxel-based morphometry of temporal lobe epilepsy: an introduction and review of the literature. Epilepsia 49:741–757

    Article  PubMed  Google Scholar 

  5. Lucassen PJ, Heine VM, Muller MB, van der Beek EM, Wiegant VM, De Kloet ER, Joels M, Fuchs E et al (2006) Stress, depression and hippocampal apoptosis. CNS Neurol Disord Drug Targets 5:531–546

    Article  PubMed  Google Scholar 

  6. Rice D, Barone S Jr (2000) Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environ Health Perspect 108(Suppl 3):511–533

    Article  PubMed  PubMed Central  Google Scholar 

  7. Rodier PM (1994) Vulnerable periods and processes during central nervous system development. Environ Health Perspect 102(Suppl 2):121–124

    Article  PubMed  PubMed Central  Google Scholar 

  8. Faigle R, Song H (2013) Signaling mechanisms regulating adult neural stem cells and neurogenesis. Biochim Biophys Acta 1830:2435–2448

    Article  CAS  PubMed  Google Scholar 

  9. Clevers H, Loh KM, Nusse R (2014) Stem cell signaling. An integral program for tissue renewal and regeneration: Wnt signaling and stem cell control. Science 346:1248012

    Article  PubMed  Google Scholar 

  10. Hamilton GF, Murawski NJ, St Cyr SA, Jablonski SA, Schiffino FL, Stanton ME, Klintsova AY (2011) Neonatal alcohol exposure disrupts hippocampal neurogenesis and contextual fear conditioning in adult rats. Brain Res 1412:88–101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Itoh K, Yaoi T, Fushiki S (2012) Bisphenol A, an endocrine-disrupting chemical, and brain development. Neuropathology 32:447–457

    Article  PubMed  Google Scholar 

  12. Jaako-Movits K, Zharkovsky T, Romantchik O, Jurgenson M, Merisalu E, Heidmets LT, Zharkovsky A (2005) Developmental lead exposure impairs contextual fear conditioning and reduces adult hippocampal neurogenesis in the rat brain. Int J Dev Neurosci 23:627–635

    Article  CAS  PubMed  Google Scholar 

  13. Kim K, Son TG, Park HR, Kim SJ, Kim HS, Kim HS, Kim TS, Jung KK et al (2009) Potencies of bisphenol A on the neuronal differentiation and hippocampal neurogenesis. J Toxicol Environ Health A 72:1343–1351

    Article  CAS  PubMed  Google Scholar 

  14. Mishra D, Tiwari SK, Agarwal S, Sharma VP, Chaturvedi RK (2012) Prenatal carbofuran exposure inhibits hippocampal neurogenesis and causes learning and memory deficits in offspring. Toxicol Sci 127:84–100

    Article  CAS  PubMed  Google Scholar 

  15. Tyler CR, Allan AM (2013) Adult hippocampal neurogenesis and mRNA expression are altered by perinatal arsenic exposure in mice and restored by brief exposure to enrichment. PLoS One 8, e73720

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Kim K, Son TG, Kim SJ, Kim HS, Kim TS, Han SY, Lee J (2007) Suppressive effects of bisphenol A on the proliferation of neural progenitor cells. J Toxicol Environ Health A 70:1288–1295

    Article  CAS  PubMed  Google Scholar 

  17. Lazurova Z, Lazurova I (2013) The environmental estrogen bisphenol A and its effects on the human organism. Vnitr Lek 59:466–471

    CAS  PubMed  Google Scholar 

  18. Hoekstra EJ, Simoneau C (2013) Release of bisphenol A from polycarbonate: a review. Crit Rev Food Sci Nutr 53:386–402

    Article  CAS  PubMed  Google Scholar 

  19. Lam SH, Hlaing MM, Zhang X, Yan C, Duan Z, Zhu L, Ung CY, Mathavan S et al (2011) Toxicogenomic and phenotypic analyses of bisphenol-A early-life exposure toxicity in zebrafish. PLoS One 6, e28273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Szychowski KA, Wojtowicz AK (2013) Components of plastic disrupt the function of the nervous system. Postepy Hig Med Dosw (Online) 67:499–506

    Article  Google Scholar 

  21. Vandenberg LN, Hauser R, Marcus M, Olea N, Welshons WV (2007) Human exposure to bisphenol A (BPA). Reprod Toxicol 24:139–177

    Article  CAS  PubMed  Google Scholar 

  22. Tiwari SK, Agarwal S, Seth B, Yadav A, Ray RS, Mishra VN, Chaturvedi RK (2014c) Inhibitory effects of bisphenol-A on neural stem cells proliferation and differentiation in the rat brain are dependent on Wnt/beta-catenin pathway. Mol Neurobiol. doi:10.1007/s12035-014-8940-1

  23. Liu R, Xing L, Kong D, Jiang J, Shang L, Hao W (2013) Bisphenol A inhibits proliferation and induces apoptosis in micromass cultures of rat embryonic midbrain cells through the JNK, CREB and p53 signaling pathways. Food Chem Toxicol 52:76–82

    Article  CAS  PubMed  Google Scholar 

  24. Seiwa C, Nakahara J, Komiyama T, Katsu Y, Iguchi T, Asou H (2004) Bisphenol A exerts thyroid-hormone-like effects on mouse oligodendrocyte precursor cells. Neuroendocrinology 80:21–30

    Article  CAS  PubMed  Google Scholar 

  25. Tiwari SK, Agarwal S, Chauhan LK, Mishra VN, Chaturvedi RK (2014a) Bisphenol-A impairs myelination potential during development in the hippocampus of the rat brain. Mol Neurobiol. doi:10.1007/s12035-014-8817-3

  26. Leranth C, Hajszan T, Szigeti-Buck K, Bober J, MacLusky NJ (2008) Bisphenol A prevents the synaptogenic response to estradiol in hippocampus and prefrontal cortex of ovariectomized nonhuman primates. Proc Natl Acad Sci U S A 105:14187–14191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. MacLusky NJ, Hajszan T, Leranth C (2005) The environmental estrogen bisphenol A inhibits estradiol-induced hippocampal synaptogenesis. Environ Health Perspect 113:675–679

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Tanabe N, Yoshino H, Kimoto T, Hojo Y, Ogiue-Ikeda M, Shimohigashi Y, Kawato S (2012) Nanomolar dose of bisphenol A rapidly modulates spinogenesis in adult hippocampal neurons. Mol Cell Endocrinol 351:317–325

    Article  CAS  PubMed  Google Scholar 

  29. Brown JS Jr (2009) Effects of bisphenol-A and other endocrine disruptors compared with abnormalities of schizophrenia: an endocrine-disruption theory of schizophrenia. Schizophr Bull 35:256–278

    Article  PubMed  Google Scholar 

  30. de Cock M, Maas YG, van de Bor M (2012) Does perinatal exposure to endocrine disruptors induce autism spectrum and attention deficit hyperactivity disorders? Review. Acta Paediatr 101:811–818

    Article  PubMed  Google Scholar 

  31. Huang B, Jiang C, Luo J, Cui Y, Qin L, Liu J (2014) Maternal exposure to bisphenol A may increase the risks of Parkinson’s disease through down-regulation of fetal IGF-1 expression. Med Hypotheses 82:245–249

    Article  CAS  PubMed  Google Scholar 

  32. Masuo Y, Ishido M (2011) Neurotoxicity of endocrine disruptors: possible involvement in brain development and neurodegeneration. J Toxicol Environ Health B Crit Rev 14:346–369

    Article  CAS  PubMed  Google Scholar 

  33. Ooe H, Taira T, Iguchi-Ariga SM, Ariga H (2005) Induction of reactive oxygen species by bisphenol A and abrogation of bisphenol A-induced cell injury by DJ-1. Toxicol Sci 88:114–126

    Article  CAS  PubMed  Google Scholar 

  34. Doggui S, Belkacemi A, Paka GD, Perrotte M, Pi R, Ramassamy C (2013) Curcumin protects neuronal-like cells against acrolein by restoring Akt and redox signaling pathways. Mol Nutr Food Res 57:1660–1670

    Article  CAS  PubMed  Google Scholar 

  35. Flora G, Gupta D, Tiwari A (2013) Preventive efficacy of bulk and nanocurcumin against lead-induced oxidative stress in mice. Biol Trace Elem Res 152:31–40

    Article  CAS  PubMed  Google Scholar 

  36. Hoppe JB, Frozza RL, Pires EN, Meneghetti AB, Salbego C (2013) The curry spice curcumin attenuates beta-amyloid-induced toxicity through beta-catenin and PI3K signaling in rat organotypic hippocampal slice culture. Neurol Res 35:857–866

    Article  PubMed  Google Scholar 

  37. Jaisin Y, Thampithak A, Meesarapee B, Ratanachamnong P, Suksamrarn A, Phivthong-Ngam L, Phumala-Morales N, Chongthammakun S et al (2011) Curcumin I protects the dopaminergic cell line SH-SY5Y from 6-hydroxydopamine-induced neurotoxicity through attenuation of p53-mediated apoptosis. Neurosci Lett 489:192–196

    Article  CAS  PubMed  Google Scholar 

  38. Noorafshan A, Asadi-Golshan R, Karbalay-Doust S, Abdollahifar MA, Rashidiani-Rashidabadi A (2013) Curcumin, the main part of turmeric, prevents learning and memory changes induced by sodium metabisulfite, a preservative agent, in rats. Exp Neurobiol 22:23–30

    Article  PubMed  PubMed Central  Google Scholar 

  39. Rajasekar N, Dwivedi S, Tota SK, Kamat PK, Hanif K, Nath C, Shukla R (2013) Neuroprotective effect of curcumin on okadaic acid induced memory impairment in mice. Eur J Pharmacol 715:381–394

    Article  CAS  PubMed  Google Scholar 

  40. Sharma C, Suhalka P, Sukhwal P, Jaiswal N, Bhatnagar M (2014) Curcumin attenuates neurotoxicity induced by fluoride: an in vivo evidence. Pharmacogn Mag 10:61–65

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Tiwari SK, Agarwal S, Seth B, Yadav A, Nair S, Bhatnagar P, Karmakar M, Kumari M et al (2014) Curcumin-loaded nanoparticles potently induce adult neurogenesis and reverse cognitive deficits in Alzheimer’s disease model via canonical Wnt/beta-catenin pathway. ACS Nano 8:76–103

    Article  CAS  PubMed  Google Scholar 

  42. Yadav RS, Shukla RK, Sankhwar ML, Patel DK, Ansari RW, Pant AB, Islam F, Khanna VK (2010) Neuroprotective effect of curcumin in arsenic-induced neurotoxicity in rats. Neurotoxicology 31:533–539

    Article  CAS  PubMed  Google Scholar 

  43. Yang J, Song S, Li J, Liang T (2014) Neuroprotective effect of curcumin on hippocampal injury in 6-OHDA-induced Parkinson’s disease rat. Pathol Res Pract 210:357–362

    Article  CAS  PubMed  Google Scholar 

  44. Yu SY, Gao R, Zhang L, Luo J, Jiang H, Wang S (2013) Curcumin ameliorates ethanol-induced memory deficits and enhanced brain nitric oxide synthase activity in mice. Prog Neuropsychopharmacol Biol Psychiatry 44:210–216

    Article  CAS  PubMed  Google Scholar 

  45. Kim DS, Kim JY, Han Y (2012) Curcuminoids in neurodegenerative diseases. Recent Pat CNS Drug Discov 7:184–204

    Article  CAS  PubMed  Google Scholar 

  46. Lavoie S, Chen Y, Dalton TP, Gysin R, Cuenod M, Steullet P, Do KQ (2009) Curcumin, quercetin, and tBHQ modulate glutathione levels in astrocytes and neurons: importance of the glutamate cysteine ligase modifier subunit. J Neurochem 108:1410–1422

    Article  CAS  PubMed  Google Scholar 

  47. Lee WH, Loo CY, Bebawy M, Luk F, Mason RS, Rohanizadeh R (2013) Curcumin and its derivatives: their application in neuropharmacology and neuroscience in the 21st century. Curr Neuropharmacol 11:338–378

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Lopresti AL, Maes M, Maker GL, Hood SD, Drummond PD (2014) Curcumin for the treatment of major depression: a randomised, double-blind, placebo controlled study. J Affect Disord 167:368–375

    Article  CAS  PubMed  Google Scholar 

  49. Kim SJ, Son TG, Park HR, Park M, Kim MS, Kim HS, Chung HY, Mattson MP et al (2008) Curcumin stimulates proliferation of embryonic neural progenitor cells and neurogenesis in the adult hippocampus. J Biol Chem 283:14497–14505

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Maekawa M, Takashima N, Arai Y, Nomura T, Inokuchi K, Yuasa S, Osumi N (2005) Pax6 is required for production and maintenance of progenitor cells in postnatal hippocampal neurogenesis. Genes Cells 10:1001–1014

    Article  CAS  PubMed  Google Scholar 

  51. Nacher J, Varea E, Blasco-Ibanez JM, Castillo-Gomez E, Crespo C, Martinez-Guijarro FJ, McEwen BS (2005) Expression of the transcription factor Pax 6 in the adult rat dentate gyrus. J Neurosci Res 81:753–761

    Article  CAS  PubMed  Google Scholar 

  52. Ferri AL, Cavallaro M, Braida D, Di Cristofano A, Canta A, Vezzani A, Ottolenghi S, Pandolfi PP et al (2004) Sox2 deficiency causes neurodegeneration and impaired neurogenesis in the adult mouse brain. Development 131:3805–3819

    Article  CAS  PubMed  Google Scholar 

  53. Steiner B, Klempin F, Wang L, Kott M, Kettenmann H, Kempermann G (2006) Type-2 cells as link between glial and neuronal lineage in adult hippocampal neurogenesis. Glia 54:805–814

    Article  PubMed  Google Scholar 

  54. Lee HY, Kleber M, Hari L, Brault V, Suter U, Taketo MM, Kemler R, Sommer L (2004) Instructive role of Wnt/beta-catenin in sensory fate specification in neural crest stem cells. Science 303:1020–1023

    Article  CAS  PubMed  Google Scholar 

  55. Zechner D, Fujita Y, Hulsken J, Muller T, Walther I, Taketo MM, Crenshaw EB 3rd, Birchmeier W et al (2003) beta-Catenin signals regulate cell growth and the balance between progenitor cell expansion and differentiation in the nervous system. Dev Biol 258:406–418

    Article  CAS  PubMed  Google Scholar 

  56. Nusse R, Fuerer C, Ching W, Harnish K, Logan C, Zeng A, ten Berge D, Kalani Y (2008) Wnt signaling and stem cell control. Cold Spring Harb Symp Quant Biol 73:59–66

    Article  CAS  PubMed  Google Scholar 

  57. Nusse R, Varmus H (2012) Three decades of Wnts: a personal perspective on how a scientific field developed. EMBO J 31:2670–2684

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Parent JM, Murphy GG (2008) Mechanisms and functional significance of aberrant seizure-induced hippocampal neurogenesis. Epilepsia 49(Suppl 5):19–25

    Article  PubMed  Google Scholar 

  59. Sahay A, Hen R (2007) Adult hippocampal neurogenesis in depression. Nat Neurosci 10:1110–1115

    Article  CAS  PubMed  Google Scholar 

  60. Ben Abdallah NM, Filipkowski RK, Pruschy M, Jaholkowski P, Winkler J, Kaczmarek L, Lipp HP (2013) Impaired long-term memory retention: common denominator for acutely or genetically reduced hippocampal neurogenesis in adult mice. Behav Brain Res 252:275–286

    Article  PubMed  Google Scholar 

  61. Hamilton A, Holscher C (2012) The effect of ageing on neurogenesis and oxidative stress in the APP(swe)/PS1(deltaE9) mouse model of Alzheimer’s disease. Brain Res 1449:83–93

    Article  CAS  PubMed  Google Scholar 

  62. Ouchi Y, Banno Y, Shimizu Y, Ando S, Hasegawa H, Adachi K, Iwamoto T (2013) Reduced adult hippocampal neurogenesis and working memory deficits in the Dgcr8-deficient mouse model of 22q11.2 deletion-associated schizophrenia can be rescued by IGF2. J Neurosci 33:9408–9419

    Article  CAS  PubMed  Google Scholar 

  63. Regensburger M, Prots I, Winner B (2014) Adult hippocampal neurogenesis in Parkinson’s disease: impact on neuronal survival and plasticity. Neural Plast 2014:454696

    Article  PubMed  PubMed Central  Google Scholar 

  64. Yeung ST, Myczek K, Kang AP, Chabrier MA, Baglietto-Vargas D, Laferla FM (2014) Impact of hippocampal neuronal ablation on neurogenesis and cognition in the aged brain. Neuroscience 259:214–222

    Article  CAS  PubMed  Google Scholar 

  65. Michalowicz J (2014) Bisphenol A—sources, toxicity and biotransformation. Environ Toxicol Pharmacol 37:738–758

    Article  CAS  PubMed  Google Scholar 

  66. Sadowski RN, Wise LM, Park PY, Schantz SL, Juraska JM (2014) Early exposure to bisphenol A alters neuron and glia number in the rat prefrontal cortex of adult males, but not females. Neuroscience 279:122–131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Xu X, Gu T, Shen Q (2014) Different effects of bisphenol-A on memory behavior and synaptic modification in intact and estrogen-deprived female mice. J Neurochem. doi:10.1111/jnc.12998

  68. Yang CW, Chou WC, Chen KH, Cheng AL, Mao IF, Chao HR, Chuang CY (2014) Visualized gene network reveals the novel target transcripts Sox2 and Pax6 of neuronal development in trans-placental exposure to bisphenol A. PLoS One 9, e100576

    Article  PubMed  PubMed Central  Google Scholar 

  69. Dias GP, Cavegn N, Nix A, do Nascimento Bevilaqua MC, Stangl D, Zainuddin MS, Nardi AE, Gardino PF et al (2012) The role of dietary polyphenols on adult hippocampal neurogenesis: molecular mechanisms and behavioural effects on depression and anxiety. Oxidative Med Cell Longev 2012:541971

    Article  Google Scholar 

  70. Valente T, Hidalgo J, Bolea I, Ramirez B, Angles N, Reguant J, Morello JR, Gutierrez C et al (2009) A diet enriched in polyphenols and polyunsaturated fatty acids, LMN diet, induces neurogenesis in the subventricular zone and hippocampus of adult mouse brain. J Alzheimers Dis 18:849–865

    Article  CAS  PubMed  Google Scholar 

  71. Park D, Xiang AP, Mao FF, Zhang L, Di CG, Liu XM, Shao Y, Ma BF et al (2010) Nestin is required for the proper self-renewal of neural stem cells. Stem Cells 28:2162–2171

    Article  CAS  PubMed  Google Scholar 

  72. Teixeira CM, Kron MM, Masachs N, Zhang H, Lagace DC, Martinez A, Reillo I, Duan X et al (2012) Cell-autonomous inactivation of the reelin pathway impairs adult neurogenesis in the hippocampus. J Neurosci 32:12051–12065

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Graham V, Khudyakov J, Ellis P, Pevny L (2003) SOX2 functions to maintain neural progenitor identity. Neuron 39:749–765

    Article  CAS  PubMed  Google Scholar 

  74. Gao Z, Ure K, Ables JL, Lagace DC, Nave KA, Goebbels S, Eisch AJ, Hsieh J (2009) Neurod1 is essential for the survival and maturation of adult-born neurons. Nat Neurosci 12:1090–1092

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Gu F, Hata R, Ma YJ, Tanaka J, Mitsuda N, Kumon Y, Hanakawa Y, Hashimoto K et al (2005) Suppression of Stat3 promotes neurogenesis in cultured neural stem cells. J Neurosci Res 81:163–171

    Article  CAS  PubMed  Google Scholar 

  76. Ma Q, Kintner C, Anderson DJ (1996) Identification of neurogenin, a vertebrate neuronal determination gene. Cell 87:43–52

    Article  CAS  PubMed  Google Scholar 

  77. Sun Y, Nadal-Vicens M, Misono S, Lin MZ, Zubiaga A, Hua X, Fan G, Greenberg ME (2001) Neurogenin promotes neurogenesis and inhibits glial differentiation by independent mechanisms. Cell 104:365–376

    Article  CAS  PubMed  Google Scholar 

  78. Cao F, Hata R, Zhu P, Nakashiro K, Sakanaka M (2010) Conditional deletion of Stat3 promotes neurogenesis and inhibits astrogliogenesis in neural stem cells. Biochem Biophys Res Commun 394:843–847

    Article  CAS  PubMed  Google Scholar 

  79. El-Missiry MA, Othman AI, Al-Abdan MA, El-Sayed AA (2014) Melatonin ameliorates oxidative stress, modulates death receptor pathway proteins, and protects the rat cerebrum against bisphenol-A-induced apoptosis. J Neurol Sci 347:251–256

    Article  CAS  PubMed  Google Scholar 

  80. Lee S, Suk K, Kim IK, Jang IS, Park JW, Johnson VJ, Kwon TK, Choi BJ et al (2008) Signaling pathways of bisphenol A-induced apoptosis in hippocampal neuronal cells: role of calcium-induced reactive oxygen species, mitogen-activated protein kinases, and nuclear factor-kappaB. J Neurosci Res 86:2932–2942

    Article  CAS  PubMed  Google Scholar 

  81. Banji OJ, Banji D, Ch K (2014) Curcumin and hesperidin improve cognition by suppressing mitochondrial dysfunction and apoptosis induced by d-galactose in rat brain. Food Chem Toxicol 74:51–59

    Article  CAS  PubMed  Google Scholar 

  82. Zhu YG, Chen XC, Chen ZZ, Zeng YQ, Shi GB, Su YH, Peng X (2004) Curcumin protects mitochondria from oxidative damage and attenuates apoptosis in cortical neurons. Acta Pharmacol Sin 25:1606–1612

    CAS  PubMed  Google Scholar 

  83. Hirsch C, Campano LM, Wohrle S, Hecht A (2007) Canonical Wnt signaling transiently stimulates proliferation and enhances neurogenesis in neonatal neural progenitor cultures. Exp Cell Res 313:572–587

    Article  CAS  PubMed  Google Scholar 

  84. Tan Y, Yu D, Busto GU, Wilson C, Davis RL (2013) Wnt signaling is required for long-term memory formation. Cell Rep 4:1082–1089

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Davinelli S, Sapere N, Zella D, Bracale R, Intrieri M, Scapagnini G (2012) Pleiotropic protective effects of phytochemicals in Alzheimer’s disease. Oxidative Med Cell Longev 2012:386527

    Article  Google Scholar 

  86. Granzotto A, Zatta P (2014) Resveratrol and Alzheimer’s disease: message in a bottle on red wine and cognition. Front Aging Neurosci 6:95

    Article  PubMed  PubMed Central  Google Scholar 

  87. Panickar KS (2013) Beneficial effects of herbs, spices and medicinal plants on the metabolic syndrome, brain and cognitive function. Cent Nerv Syst Agents Med Chem 13:13–29

    Article  CAS  PubMed  Google Scholar 

  88. Panickar KS, Jang S (2013) Dietary and plant polyphenols exert neuroprotective effects and improve cognitive function in cerebral ischemia. Recent Pat Food Nutr Agric 5:128–143

    Article  CAS  PubMed  Google Scholar 

  89. Dong S, Zeng Q, Mitchell ES, Xiu J, Duan Y, Li C, Tiwari JK, Hu Y et al (2012) Curcumin enhances neurogenesis and cognition in aged rats: implications for transcriptional interactions related to growth and synaptic plasticity. PLoS One 7, e31211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

Authors are thankful to Director, CSIR-IITR for support during the study. This work was supported by the CSIR Network Project BSC-0111 (InDepth) and the Indian Council of Medical Research (ICMR) project grant to R.K.C. S.K.T. and S.A. are recipients of a Senior Research Fellowship from University Grants Commission and Council of Scientific and Industrial Research, New Delhi, respectively. CSIR-IITR Manuscript Communication Number is 3291.

Conflict of Interest

The authors declare no competing financial interest.

Ethical Statement

All the authors gave their consent, and experiments on the animals were approved by institutional ethical committee.

Author information

Author notes

    Authors and Affiliations

    1. Developmental Toxicology Division, Systems Toxicology Group, CSIR-Indian Institute of Toxicology Research (CSIR-IITR), 80 MG Marg, Lucknow, 226001, India

      Shashi Kant Tiwari, Swati Agarwal & Rajnish Kumar Chaturvedi

    2. Academy of Scientific and Innovative Research (AcSIR), New Delhi, India

      Shashi Kant Tiwari, Swati Agarwal & Rajnish Kumar Chaturvedi

    3. Food, Drugs and Chemical Toxicology Group, CSIR-IITR, 80 MG Marg, Lucknow, 226001, India

      Anurag Tripathi

    Authors
    1. Shashi Kant Tiwari
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Swati Agarwal
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Anurag Tripathi
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Rajnish Kumar Chaturvedi
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding author

    Correspondence to Rajnish Kumar Chaturvedi.

    Additional information

    Shashi Kant Tiwari and Swati Agarwal contributed equally to this work.

    Electronic supplementary material

    Below is the link to the electronic supplementary material.

    Figure S1

    (DOC 1585 kb)

    Supplementary Table S1

    (DOC 37 kb)

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Tiwari, S.K., Agarwal, S., Tripathi, A. et al. Bisphenol-A Mediated Inhibition of Hippocampal Neurogenesis Attenuated by Curcumin via Canonical Wnt Pathway. Mol Neurobiol 53, 3010–3029 (2016). https://doi.org/10.1007/s12035-015-9197-z

    Download citation

    • Received:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s12035-015-9197-z

    Keywords

    Search

    Navigation