Prenatal exposure to bisphenol A alters the transcriptome-interactome profiles of genes associated with Alzheimer's disease in the offspring hippocampus.
Alzheimer Disease
/ chemically induced
Animals
Autistic Disorder
/ chemically induced
Benzhydryl Compounds
/ agonists
Female
Gene Expression Profiling
/ methods
Hippocampus
/ drug effects
Inflammation
/ chemically induced
Male
Maternal Exposure
NF-kappa B
/ genetics
Phenols
/ agonists
Pregnancy
Prenatal Exposure Delayed Effects
/ chemically induced
Rats
Rats, Wistar
Transcriptome
/ drug effects
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
11 06 2020
11 06 2020
Historique:
received:
02
12
2019
accepted:
27
04
2020
entrez:
13
6
2020
pubmed:
13
6
2020
medline:
1
12
2020
Statut:
epublish
Résumé
Our recent study revealed that prenatal exposure to bisphenol A (BPA) disrupted the transcriptome profiles of genes in the offspring hippocampus. In addition to genes linked to autism, several genes associated with Alzheimer's disease (AD) were found to be differentially expressed, although the association between BPA-responsive genes and AD-related genes has not been thoroughly investigated. Here, we demonstrated that in utero BPA exposure also disrupted the transcriptome profiles of genes associated with neuroinflammation and AD in the hippocampus. The level of NF-κB protein and its AD-related target gene Bace1 were significantly increased in the offspring hippocampus in a sex-dependent manner. Quantitative RT-PCR analysis also showed an increase in the expression of Tnf gene. Moreover, the reanalysis of transcriptome profiling data from several previously published BPA studies consistently showed that BPA-responsive genes were significantly associated with top AD candidate genes. The findings from this study suggest that maternal BPA exposure may increase AD risk in offspring by dysregulating genes associated with AD neuropathology and inflammation and reveal a possible relationship between AD and autism, which are linked to the same environmental factor. Sex-specific effects of prenatal BPA exposure on the susceptibility of AD deserve further investigation.
Identifiants
pubmed: 32528016
doi: 10.1038/s41598-020-65229-0
pii: 10.1038/s41598-020-65229-0
pmc: PMC7289845
doi:
Substances chimiques
Benzhydryl Compounds
0
NF-kappa B
0
Phenols
0
bisphenol A
MLT3645I99
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
9487Références
Prince, M. et al. The global prevalence of dementia: a systematic review and metaanalysis. Alzheimer’s & dementia: the journal of the Alzheimer’s Association 9, 63–75.e62, https://doi.org/10.1016/j.jalz.2012.11.007 (2013).
doi: 10.1016/j.jalz.2012.11.007
Lane, C. A., Hardy, J. & Schott, J. M. Alzheimer’s disease. European journal of neurology 25, 59–70, https://doi.org/10.1111/ene.13439 (2018).
doi: 10.1111/ene.13439
pubmed: 28872215
Sabuncu, M. R. et al. The dynamics of cortical and hippocampal atrophy in Alzheimer disease. Archives of neurology 68, 1040–1048, https://doi.org/10.1001/archneurol.2011.167 (2011).
doi: 10.1001/archneurol.2011.167
pubmed: 21825241
pmcid: 3248949
Bakkour, A., Morris, J. C., Wolk, D. A. & Dickerson, B. C. The effects of aging and Alzheimer’s disease on cerebral cortical anatomy: specificity and differential relationships with cognition. NeuroImage 76, 332–344, https://doi.org/10.1016/j.neuroimage.2013.02.059 (2013).
doi: 10.1016/j.neuroimage.2013.02.059
pubmed: 23507382
pmcid: 4098706
Selkoe, D. J. Alzheimer’s disease: genes, proteins, and therapy. Physiological reviews 81, 741–766, https://doi.org/10.1152/physrev.2001.81.2.741 (2001).
doi: 10.1152/physrev.2001.81.2.741
pubmed: 11274343
Golde, T. E., Eckman, C. B. & Younkin, S. G. Biochemical detection of Abeta isoforms: implications for pathogenesis, diagnosis, and treatment of Alzheimer’s disease. Biochimica et biophysica acta 1502, 172–187, https://doi.org/10.1016/s0925-4439(00)00043-0 (2000).
doi: 10.1016/s0925-4439(00)00043-0
pubmed: 10899442
Huang, Y. & Mucke, L. Alzheimer mechanisms and therapeutic strategies. Cell 148, 1204–1222, https://doi.org/10.1016/j.cell.2012.02.040 (2012).
doi: 10.1016/j.cell.2012.02.040
pubmed: 22424230
pmcid: 3319071
De Strooper, B., Vassar, R. & Golde, T. The secretases: enzymes with therapeutic potential in Alzheimer disease. Nature reviews. Neurology 6, 99–107, https://doi.org/10.1038/nrneurol.2009.218 (2010).
doi: 10.1038/nrneurol.2009.218
pubmed: 20139999
Qiu, C., Winblad, B. & Fratiglioni, L. The age-dependent relation of blood pressure to cognitive function and dementia. The Lancet. Neurology 4, 487–499, https://doi.org/10.1016/s1474-4422(05)70141-1 (2005).
doi: 10.1016/s1474-4422(05)70141-1
pubmed: 16033691
Shobab, L. A., Hsiung, G. Y. & Feldman, H. H. Cholesterol in Alzheimer’s disease. The. Lancet. Neurology 4, 841–852, https://doi.org/10.1016/s1474-4422(05)70248-9 (2005).
doi: 10.1016/s1474-4422(05)70248-9
pubmed: 16297842
Arvanitakis, Z., Wilson, R. S., Bienias, J. L., Evans, D. A. & Bennett, D. A. Diabetes mellitus and risk of Alzheimer disease and decline in cognitive function. Archives of neurology 61, 661–666, https://doi.org/10.1001/archneur.61.5.661 (2004).
doi: 10.1001/archneur.61.5.661
pubmed: 15148141
Moulton, P. V. & Yang, W. Air pollution, oxidative stress, and Alzheimer’s disease. Journal of environmental and public health 2012, 472751, https://doi.org/10.1155/2012/472751 (2012).
doi: 10.1155/2012/472751
pubmed: 22523504
pmcid: 3317180
House, E. et al. Aluminium, iron, zinc and copper influence the in vitro formation of amyloid fibrils of Abeta42 in a manner which may have consequences for metal chelation therapy in Alzheimer’s disease. Journal of Alzheimer’s disease: JAD 6, 291–301 (2004).
doi: 10.3233/JAD-2004-6310
Raven, E. P., Lu, P. H., Tishler, T. A., Heydari, P. & Bartzokis, G. Increased iron levels and decreased tissue integrity in hippocampus of Alzheimer’s disease detected in vivo with magnetic resonance imaging. Journal of Alzheimer’s disease: JAD 37, 127–136, https://doi.org/10.3233/jad-130209 (2013).
doi: 10.3233/jad-130209
pubmed: 23792695
Song, Y. et al. Endocrine-disrupting chemicals, risk of type 2 diabetes, and diabetes-related metabolic traits: A systematic review and meta-analysis. Journal of diabetes 8, 516–532, https://doi.org/10.1111/1753-0407.12325 (2016).
doi: 10.1111/1753-0407.12325
pubmed: 26119400
Rachon, D. Endocrine disrupting chemicals (EDCs) and female cancer: Informing the patients. Reviews in endocrine & metabolic disorders 16, 359–364, https://doi.org/10.1007/s11154-016-9332-9 (2015).
doi: 10.1007/s11154-016-9332-9
Foulds, C. E., Trevino, L. S., York, B. & Walker, C. L. Endocrine-disrupting chemicals and fatty liver disease. Nature reviews. Endocrinology 13, 445–457, https://doi.org/10.1038/nrendo.2017.42 (2017).
doi: 10.1038/nrendo.2017.42
pubmed: 28524171
pmcid: 5657429
Johansson, H. K. et al. Perinatal exposure to mixtures of endocrine disrupting chemicals reduces female rat follicle reserves and accelerates reproductive aging. Reproductive toxicology (Elmsford, N.Y.) 61, 186–194, https://doi.org/10.1016/j.reprotox.2016.03.045 (2016).
doi: 10.1016/j.reprotox.2016.03.045
Masuo, Y. & Ishido, M. Neurotoxicity of endocrine disruptors: possible involvement in brain development and neurodegeneration. Journal of toxicology and environmental health. Part B. Critical reviews 14, 346–369, https://doi.org/10.1080/10937404.2011.578557 (2011).
doi: 10.1080/10937404.2011.578557
pubmed: 21790316
Moosa, A., Shu, H., Sarachana, T. & Hu, V. W. Are endocrine disrupting compounds environmental risk factors for autism spectrum disorder? Horm Behav 101, 13–21, https://doi.org/10.1016/j.yhbeh.2017.10.003 (2018).
doi: 10.1016/j.yhbeh.2017.10.003
pubmed: 29042182
Vandenberg, L. N., Hauser, R., Marcus, M., Olea, N. & Welshons, W. V. Human exposure to bisphenol A (BPA). Reproductive toxicology (Elmsford, N.Y.) 24, 139–177, https://doi.org/10.1016/j.reprotox.2007.07.010 (2007).
doi: 10.1016/j.reprotox.2007.07.010
Porras, S. P., Heinala, M. & Santonen, T. Bisphenol A exposure via thermal paper receipts. Toxicology letters 230, 413–420, https://doi.org/10.1016/j.toxlet.2014.08.020 (2014).
doi: 10.1016/j.toxlet.2014.08.020
pubmed: 25175590
World Health Organization. Food and Agriculture Organization of United Nations: Bisphenol A (BPA) Current state of knowledge and future actions by WHO and FAO. International Food Safety Authorities Network (INFOSAN) (2009).
Wang, T. et al. Involvement of Insulin Signaling Disturbances in Bisphenol A-Induced Alzheimer’s Disease-like Neurotoxicity. Scientific reports 7, 7497, https://doi.org/10.1038/s41598-017-07544-7 (2017).
doi: 10.1038/s41598-017-07544-7
pubmed: 28790390
pmcid: 5548741
Tanabe, N. et al. Nanomolar dose of bisphenol A rapidly modulates spinogenesis in adult hippocampal neurons. Molecular and cellular endocrinology 351, 317–325, https://doi.org/10.1016/j.mce.2012.01.008 (2012).
doi: 10.1016/j.mce.2012.01.008
pubmed: 22281313
Elsworth, J. D. et al. Prenatal exposure to bisphenol A impacts midbrain dopamine neurons and hippocampal spine synapses in non-human primates. Neurotoxicology 35, 113–120, https://doi.org/10.1016/j.neuro.2013.01.001 (2013).
doi: 10.1016/j.neuro.2013.01.001
pubmed: 23337607
pmcid: 3660149
Nishikawa, M. et al. Placental transfer of conjugated bisphenol A and subsequent reactivation in the rat fetus. Environmental health perspectives 118, 1196–1203, https://doi.org/10.1289/ehp.0901575 (2010).
doi: 10.1289/ehp.0901575
pubmed: 20382578
pmcid: 2944077
Zimmers, S. M. et al. Determination of free Bisphenol A (BPA) concentrations in breast milk of U.S. women using a sensitive LC/MS/MS method. Chemosphere 104, 237–243, https://doi.org/10.1016/j.chemosphere.2013.12.085 (2014).
doi: 10.1016/j.chemosphere.2013.12.085
pubmed: 24507723
Kawai, K. et al. Aggressive behavior and serum testosterone concentration during the maturation process of male mice: the effects of fetal exposure to bisphenol A. Environmental health perspectives 111, 175–178, https://doi.org/10.1289/ehp.5440 (2003).
doi: 10.1289/ehp.5440
pubmed: 12573901
pmcid: 1241346
Tian, Y. H., Baek, J. H., Lee, S. Y. & Jang, C. G. Prenatal and postnatal exposure to bisphenol a induces anxiolytic behaviors and cognitive deficits in mice. Synapse (New York, N.Y.) 64, 432–439, https://doi.org/10.1002/syn.20746 (2010).
doi: 10.1002/syn.20746
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. Hormones and behavior 58, 326–333, https://doi.org/10.1016/j.yhbeh.2010.02.012 (2010).
doi: 10.1016/j.yhbeh.2010.02.012
pubmed: 20206181
Thongkorn, S. et al. Sex Differences in the Effects of Prenatal Bisphenol A Exposure on Genes Associated with Autism Spectrum Disorder in the Hippocampus. Sci Rep 9, 3038, https://doi.org/10.1038/s41598-019-39386-w (2019).
doi: 10.1038/s41598-019-39386-w
pubmed: 30816183
pmcid: 6395584
Mattson, M. P. & Camandola, S. NF-kappaB in neuronal plasticity and neurodegenerative disorders. J Clin Invest 107, 247–254, https://doi.org/10.1172/jci11916 (2001).
doi: 10.1172/jci11916
pubmed: 11160145
pmcid: 199201
Heneka, M. T. et al. Neuroinflammation in Alzheimer’s disease. The Lancet. Neurology 14, 388–405, https://doi.org/10.1016/s1474-4422(15)70016-5 (2015).
doi: 10.1016/s1474-4422(15)70016-5
pubmed: 25792098
pmcid: 5909703
Kinney, J. W. et al. Inflammation as a central mechanism in Alzheimer’s disease. Alzheimers Dement (N Y) 4, 575–590, https://doi.org/10.1016/j.trci.2018.06.014 (2018).
doi: 10.1016/j.trci.2018.06.014
Kimura, E. et al. Prenatal exposure to bisphenol A impacts neuronal morphology in the hippocampal CA1 region in developing and aged mice. Archives of toxicology 90, 691–700, https://doi.org/10.1007/s00204-015-1485-x (2016).
doi: 10.1007/s00204-015-1485-x
pubmed: 25804199
Bansal, A. et al. Transgenerational effects of maternal bisphenol: a exposure on offspring metabolic health. J Dev Orig Health Dis 10, 164–175, https://doi.org/10.1017/s2040174418000764 (2019).
doi: 10.1017/s2040174418000764
pubmed: 30362448
Majdalawieh, A., Zhang, L. & Ro, H. S. Adipocyte enhancer-binding protein-1 promotes macrophage inflammatory responsiveness by up-regulating NF-kappaB via IkappaBalpha negative regulation. Molecular biology of the cell 18, 930–942, https://doi.org/10.1091/mbc.e06-03-0217 (2007).
doi: 10.1091/mbc.e06-03-0217
pubmed: 17202411
pmcid: 1805081
Shi, Z. M. et al. Upstream regulators and downstream effectors of NF-kappaB in Alzheimer’s disease. Journal of the neurological sciences 366, 127–134, https://doi.org/10.1016/j.jns.2016.05.022 (2016).
doi: 10.1016/j.jns.2016.05.022
pubmed: 27288790
Terai, K., Matsuo, A. & McGeer, P. L. Enhancement of immunoreactivity for NF-kappa B in the hippocampal formation and cerebral cortex of Alzheimer’s disease. Brain research 735, 159–168 (1996).
doi: 10.1016/0006-8993(96)00310-1
Takahashi, M., Komada, M., Miyazawa, K., Goto, S. & Ikeda, Y. Bisphenol A exposure induces increased microglia and microglial related factors in the murine embryonic dorsal telencephalon and hypothalamus. Toxicology letters 284, 113–119, https://doi.org/10.1016/j.toxlet.2017.12.010 (2018).
doi: 10.1016/j.toxlet.2017.12.010
pubmed: 29248573
Luo, G. et al. Maternal bisphenol a diet induces anxiety-like behavior in female juvenile with neuroimmune activation. Toxicological sciences: an official journal of the Society of Toxicology 140, 364–373, https://doi.org/10.1093/toxsci/kfu085 (2014).
doi: 10.1093/toxsci/kfu085
Janelsins, M. C. et al. Early correlation of microglial activation with enhanced tumor necrosis factor-alpha and monocyte chemoattractant protein-1 expression specifically within the entorhinal cortex of triple transgenic Alzheimer’s disease mice. Journal of neuroinflammation 2, 23, https://doi.org/10.1186/1742-2094-2-23 (2005).
doi: 10.1186/1742-2094-2-23
pubmed: 16232318
pmcid: 1276812
Janelsins, M. C. et al. Chronic neuron-specific tumor necrosis factor-alpha expression enhances the local inflammatory environment ultimately leading to neuronal death in 3xTg-AD mice. The American journal of pathology 173, 1768–1782, https://doi.org/10.2353/ajpath.2008.080528 (2008).
doi: 10.2353/ajpath.2008.080528
pubmed: 18974297
pmcid: 2626388
Chung, I. Y. & Benveniste, E. N. Tumor necrosis factor-alpha production by astrocytes. Induction by lipopolysaccharide, IFN-gamma, and IL-1 beta. Journal of immunology (Baltimore, Md.: 1950) 144, 2999–3007 (1990).
Zhao, M. et al. The induction of the TNFalpha death domain signaling pathway in Alzheimer’s disease brain. Neurochemical research 28, 307–318, https://doi.org/10.1023/a:1022337519035 (2003).
doi: 10.1023/a:1022337519035
pubmed: 12608703
Fillit, H. et al. Elevated circulating tumor necrosis factor levels in Alzheimer’s disease. Neuroscience letters 129, 318–320, https://doi.org/10.1016/0304-3940(91)90490-k (1991).
doi: 10.1016/0304-3940(91)90490-k
pubmed: 1745413
McAlpine, F. E. & Tansey, M. G. Neuroinflammation and tumor necrosis factor signaling in the pathophysiology of Alzheimer’s disease. Journal of inflammation research 1, 29–39 (2008).
pubmed: 22096345
pmcid: 3218716
Sun, Y., Nakashima, M. N., Takahashi, M., Kuroda, N. & Nakashima, K. Determination of bisphenol A in rat brain by microdialysis and column switching high-performance liquid chromatography with fluorescence detection. Biomedical chromatography: BMC 16, 319–326, https://doi.org/10.1002/bmc.161 (2002).
doi: 10.1002/bmc.161
pubmed: 12210505
Fukumoto, H., Cheung, B. S., Hyman, B. T. & Irizarry, M. C. Beta-secretase protein and activity are increased in the neocortex in Alzheimer disease. Arch Neurol 59, 1381–1389 (2002).
doi: 10.1001/archneur.59.9.1381
Chen, C. H. et al. Increased NF-kappaB signalling up-regulates BACE1 expression and its therapeutic potential in Alzheimer’s disease. The international journal of neuropsychopharmacology 15, 77–90, https://doi.org/10.1017/s1461145711000149 (2012).
doi: 10.1017/s1461145711000149
pubmed: 21329555
Fang, F. et al. Insulin signaling disruption in male mice due to perinatal bisphenol A exposure: Role of insulin signaling in the brain. Toxicology letters 245, 59–67, https://doi.org/10.1016/j.toxlet.2016.01.007 (2016).
doi: 10.1016/j.toxlet.2016.01.007
pubmed: 26779933
Pichitpunpong, C. et al. Phenotypic subgrouping and multi-omics analyses reveal reduced diazepam-binding inhibitor (DBI) protein levels in autism spectrum disorder with severe language impairment. PLoS One 14, e0214198–e0214198, https://doi.org/10.1371/journal.pone.0214198 (2019).
doi: 10.1371/journal.pone.0214198
pubmed: 30921354
pmcid: 6438570
Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat Methods 9, 357–359, https://doi.org/10.1038/nmeth.1923 (2012).
doi: 10.1038/nmeth.1923
pubmed: 22388286
pmcid: 22388286
Li, B. & Dewey, C. N. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12, 323–323, https://doi.org/10.1186/1471-2105-12-323 (2011).
doi: 10.1186/1471-2105-12-323
pubmed: 3163565
pmcid: 3163565
Saeed, A. I. et al. TM4: a free, open-source system for microarray data management and analysis. BioTechniques 34, 374–378, https://doi.org/10.2144/03342mt01 (2003).
doi: 10.2144/03342mt01
pubmed: 12613259
Tangsuwansri, C. et al. Investigation of epigenetic regulatory networks associated with autism spectrum disorder (ASD) by integrated global LINE-1 methylation and gene expression profiling analyses. PLoS One 13, e0201071, https://doi.org/10.1371/journal.pone.0201071 (2018).
doi: 10.1371/journal.pone.0201071
pubmed: 30036398
pmcid: 6056057
Saeliw, T. et al. Integrated genome-wide Alu methylation and transcriptome profiling analyses reveal novel epigenetic regulatory networks associated with autism spectrum disorder. Mol Autism 9, 27, https://doi.org/10.1186/s13229-018-0213-9 (2018).
doi: 10.1186/s13229-018-0213-9
pubmed: 29686828
pmcid: 5902935
Bai, Z. et al. AlzBase: an Integrative Database for Gene Dysregulation in Alzheimer’s Disease. Molecular neurobiology 53, 310–319, https://doi.org/10.1007/s12035-014-9011-3 (2016).
doi: 10.1007/s12035-014-9011-3
pubmed: 25432889