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01-12-2017 | Original Article

Anatomical specificity of the brain in the modulation of Neuroglobin and Cytoglobin genes after chronic bisphenol a exposure

Authors: Rodrigo Rodrigues da Conceição, Janaina Sena de Souza, Kelen Carneiro de Oliveira, Rui Monteiro de Barros Maciel, Marco Aurélio Romano, Renata Marino Romano, Magnus Régios Dias da Silva, Maria Izabel Chiamolera, Gisele Giannocco

Published in: Metabolic Brain Disease | Issue 6/2017

Abstract

The aim of this study was to investigate the influence of Bisphenol A (BPA) exposure on Neuroglobin (Ngb) and Cytoglobin (Cygb) as well as oxidative stress gene expression in the cerebellum, hippocampus, hypothalamus and cortex. Male Wistar rats were randomly divided into 3 groups: Control and two groups receiving 2 different daily BPA dosages, 5 or 25 mg/kg from postnatal day 50 (PND50) through PND90 and they were euthanized at PND105. In the cortex, we found an increase in Ngb gene expression and also in superoxide dismutase 1 and Catalase (Cat). In the cerebellum, we found an increase in Ngb and Cat, in the hypothalamus, there was a decrease in Cygb and an increase in glutathione peroxidase and Cat and in hypoxia-inducible factor 1 alpha (Hif1α) at the low dosage and a decrease in Hif1α at the high BPA dosage. Finally, in the hippocampus, we observed a decrease in Ngb and Cygb and an increase in Hif1α. In summary, BPA promotes the modulation of both Ngb and Cygb, but such changes occur by different mechanisms depending on the exposure dose and anatomical area.

Andrionou XD, Gängler S, Piciu A, Charisiadis P, ZIra C, Aristidou K, Piciu D, Hauser R, Makris KC (2016) Human exposures to bisphenol a, bisphenol F and chlorinated bisphenol a derivatives and thyroid function. PLoS One 11(10):e0155237. doi:10.1371/journal.pone.0155237 CrossRef

Antao ST, Duong TT, Aran R, Witting PK (2010) Neuroglobin overexpression in cultured human neuronal cells protects against hydrogen peroxide insult via activating phosphoinositide-3 kinase and opening the mitochondrial KATP Channel. Antioxid Redox Signal 13(6):769–781CrossRefPubMed

Aung MT, Johns LE, Ferguson KK, Mukherjee B, McElrath TF, Meeker JD (2017) Thyroid hormone parameters during pregnancy in relation to urinary bisphenol a concentrations: a repeated measures study. Environ Int 104:33–40CrossRefPubMed

Biedermann S, Tschudin P, Grob K (2010) Transfer of bisphenol a from thermal printer paper to the skin. Anal Bioanal Chem 398(1):571–576. doi:10.1007/s00216-010-3936-9 CrossRefPubMed

Brunori M, Vallone B (2007) Neuroglobin, seven years after. Cell Mol Life Sci 64(10):1259–1268. doi:10.1007/s00018-007-7090-2 CrossRefPubMed

Burmester T, Weich B, Reinhardt S et al (2000) A vertebrate globin expressed in the brain. Nature 407(6803):520–523. doi:10.1038/35035093 CrossRefPubMed

Burmester T, Ebner B, Weich B et al (2002) Cytoglobin: a novel globin type ubiquitously expressed in vertebrate tissues. Mol Biol Evol 19(4):416–421. doi:10.1093/oxfordjournals.molbev.a004096 CrossRefPubMed

De Marinis E, Ascenzi P, Pellegrini M, et al. (2010) 17β-estradiol--a new modulator of neuroglobin levels in neurons: role in neuroprotection against H₂O₂-induced toxicity. Neurosignals 18(4):223–235. doi:10.1159/000323906

de Souza JS, Kizys MM, da Conceição RR, Glebocki G, Romano RM, Ortiga-Carvalho TM, Giannocco G, da Silva ID, Dias da Silva MR, Romano MA, Chiamolera MI (2017) Perinatal exposure to glyphosate-based herbicide alters the thyrotrophic axis and causes thyroid hormone homeostasis imbalance in male rats. Toxicology 377:25–37CrossRefPubMed

Di Pietro V, Lazzarino G, Amorini AM et al (2014) Neuroglobin expression and oxidant/antioxidant balance after graded traumatic brain injury in the rat. Free Radic Biol Med 69:258–264. doi:10.1016/j.freeradbiomed.2014.01.032 CrossRefPubMed

Fago A, Hundahl C, Malte H et al (2004) Functional properties of neuroglobin and cytoglobin. Insights into the ancestral physiological roles of globins. IUBMB Life 56(11–12):689–696. doi:10.1080/15216540500037299 CrossRefPubMed

Fan YY, Zheng JL, Ren JH et al (2014) Effects of storage temperature and duration on release of antimony and bisphenol a from polyethylene terephthalate drinking water bottles of China. Environ Pollut 192:113–120. doi:10.1016/j.envpol.2014.05.012 CrossRefPubMed

Fang X, Cao S, Liu R (2011) Interaction of bisphenol a with bovine hemoglobin using spectroscopic and molecular modeling methods. Appl Spectrosc 65(11):1250–1253. doi:10.1366/11-06357 CrossRefPubMed

FAO/WHO (2010). Reproductive and Developmental Toxicity of Bisphenol A in Mammalian Species.WHO Press, Ottawa

Farabollini F, Porrini S, Della Seta D et al (2002) Effects of perinatal exposure to bisphenol a on sociosexual behavior of female and male rats. Environ Health Perspect 110(Suppl 3):409–414CrossRefPubMedPubMedCentral

Finkel T (1998) Oxygen radicals and signaling. Curr Opin Cell Biol 10(2):248–253. doi:10.1016/S0955-0674(98)80147-6 CrossRefPubMed

Finkel T, Holbrook NJ (2000) Oxidants, oxidative stress and the biology of ageing. Nature 408(6809):239–247. doi:10.1038/35041687 CrossRefPubMed

Fordel E, Geuens E, Dewilde S et al (2004) Hypoxia/ischemia and the regulation of neuroglobin and cytoglobin expression. IUBMB Life 56(11–12):681–687. doi:10.1080/15216540500037406 CrossRefPubMed

Fordel E, Thijs L, Martinet W, Lenjou LT, Van Backstaele D, Moens L, Dewlde S (2006) Neuroglobin and cytoglobin overexpression protects human SH-SY5Y neuroblastoma cells agaisnt oxidative stress-induced cell death. Neurosci Lett 401(2):146–151CrossRef

Fordel E, Thijs L, Martinet W et al (2007) Anoxia or oxygen and glucose deprivation in SH-SY5Y cells: a step closer to the unraveling of neuroglobin and cytoglobin functions. Gene 398(1–2):114–122. doi:10.1016/j.gene.2007.03.022 CrossRefPubMed

Geens T, Aerts D, Berthot C et al (2012) A review of dietary and non-dietary exposure to bisphenol a. Food Chem Toxicol 50(10):3725–3740. doi:10.1016/j.fct.2012.07.059 CrossRefPubMed

Gould JC, Leonard LS, Maness SC et al (1998) Bisphenol a interacts with the estrogen receptor alpha in a distinct manner from estradiol. Mol Cell Endocrinol 142(1–2):203–214. doi:10.1016/S0303-7207(98)00084-7 CrossRefPubMed

Greenberg DA, Jin K, Khan AA (2008) Neuroglobin: an endogenous neuroprotectant. Curr Opin Pharmacol 8(1):20–24. doi:10.1016/j.coph.2007.09.003 CrossRefPubMed

Guignard D, Gayrard V, Lacroix MZ, Puel S, Picard-Hagen N, Viguié C (2017) Evidence for bisphenol A-induced disruption of maternal thyroid homeostasis in the pregnant ewe at low level representative of human exposure. Chemosphere 182:458–467CrossRefPubMed

Haines B, Demaria M, Mao X et al (2012) Hypoxia-inducible factor-1 and neuroglobin expression. Neurosci Lett 514(2):137–140. doi:10.1016/j.neulet.2012.01.080 CrossRefPubMedPubMedCentral

Hu CL, Xia JM, Cai J, Li X et al (2013) Ulinastatin attenuates oxidation, inflammation and neural apoptosis in the cerebral cortex of adult rats with ventricular fibrillation after cardiopulmonary resuscitation. Clinics (Sao Paulo) 68(9):1231–1238. doi:10.6061/clinics/2013(09)10 CrossRef

Hundahl CA, Allen GC, Hannibal J et al (2010) Anatomical characterization of cytoglobin and neuroglobin mRNA and protein expression in the mouse brain. Brain Res 1331:58–73. doi:10.1016/j.brainres.2010.03.056 CrossRefPubMed

Jin K, Mao XO, Xie L et al (2008) Neuroglobin protects against nitric oxide toxicity. Neurosci Lett 430(2):135–137. doi:10.1016/j.neulet.2007.10.031 CrossRefPubMed

Kawai K, Nozaki T, Nishikata H et al (2003) Aggressive behavior and serum testosterone concentration during the maturation process of male mice: the effects of fetal exposure to bisphenol a. Environ Health Perspect 111(2):175–178CrossRefPubMedPubMedCentral

Khadrawy YA, Noor NA, Mourad IM (2016) Neurochemical impact of bisphenol a in the hippocampus and cortex of adult male albino rats. Toxicol Ind Health 32(9):1711–1719. doi:10.1177/0748233715579803 CrossRefPubMed

Kim CS, Sapienza PP, Ross IA et al (2004) Distribution of bisphenol a in the neuroendocrine organs of female rats. Toxicol Ind Health 20(1–5):41–50CrossRefPubMed

Kim K, Son TG, Park HR et al (2009) Potencies of bisphenol a on the neuronal differentiation and hippocampal neurogenesis. J Toxic Environ Health A 72(21–22):1343–1351. doi:10.1080/15287390903212501 CrossRef

Kinch CD, Ibhazehiebo K, Jeong JH et al (2015) Low-dose exposure to bisphenol a and replacement bisphenol S induces precocious hypothalamic neurogenesis in embryonic zebrafish. Proc Natl Acad Sci USA 112(5):1475–1480. doi:10.1073/pnas.1417731112 CrossRefPubMedPubMedCentral

Klenke U, Constantin S, Wray S (2016) BPA directly decreases GnRH neuronal activity via noncanonical pathway. Endocrinology 157(5):1980–1990CrossRefPubMedPubMedCentral

Kubo K, Arai O, Omura M et al (2003) Low dose effects of bisphenol a on sexual differentiation of the brain and behavior in rats. Neurosci Res 45(3):345–356. doi:10.1016/S0168-0102(02)00251-1 CrossRefPubMed

Kuiper GG, Gustafsson JA (1997) The novel estrogen receptor-beta subtype: potential role in the cell- and promoter-specific actions of estrogens and anti-estrogens. FEBS Lett 410(1):87–90. doi:10.1016/S0014-5793(97)00413-4 CrossRefPubMed

Kuiper GG, Lemmen JG, Carlsson B et al (1998) Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology 139(10):4252–4263. doi:10.1210/endo.139.10.6216 CrossRefPubMed

Lee CK, Kim SH, Moon DH et al (2005) Effects of bisphenol a on the placental function and reproduction in rats. J Prev Med Public Health 38(3):330–336PubMed

Leranth C, Hajszan T, Szigeti-Buck K et al (2008) Bisphenol a prevents the synaptogenic response to estradiol in hippocampus and prefrontal cortex of ovariectomized nonhuman primates. Proc Natl Acad Sci USA 105(37):14187–14191. doi:10.1073/pnas.0806139105 CrossRefPubMedPubMedCentral

Li T, Liu J, Yang C (2010) Pretreatment with hemoglobin-based oxygen carriers protect isolated rat heart from myocardial infarction. Artif Cells Blood Substit Immobil Biotechnol 38(3):115–118. doi:10.3109/10731191003670541 CrossRefPubMed

Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods 25(4):402–408. doi:10.1006/meth.2001.1262 CrossRefPubMed

López-Cervantes J, Paseiro-Losada P (2003) Determination of bisphenol a in, and its migration from, PVC stretch film used for food packaging. Food Addit Contam 20(6):596–606. doi:10.1080/0265203031000109495 CrossRefPubMed

MacKay H, Paterson ZR, Abizaid A (2017) Perinatal exposure to low-dose bisphenol-a disrupts the structural and functional development of the hypothalamic feeding circuitry. Endocrinology 158(4):768–777CrossRefPubMed

Masuo Y, Morita M, Oka S et al (2004) Motor hyperactivity caused by a deficit in dopaminergic neurons and the effects of endocrine disruptors: a study inspired by the physiological roles of PACAP in the brain. Regul Pept 123(1–3):225–234. doi:10.1016/j.regpep.2004.05.010 CrossRefPubMed

Mathisen GH, Yazdani M, Rakkestad KE et al (2013) Prenatal exposure to bisphenol a interferes with the development of cerebellar granule neurons in mice and chicken. Int J Dev Neurosci 31(8):762–769. doi:10.1016/j.ijdevneu.2013.09.009 CrossRefPubMed

Melgarejo-Gutiérrez M, Acosta-Peña E, Venebra-Muñoz A et al (2013) Sleep deprivation reduces neuroglobin immunoreactivity in the rat brain. Neuroreport 24(3):120–125. doi:10.1097/WNR.0b013e32835d4b74 CrossRefPubMed

Moriyama K, Tagami T, Akamizu T et al (2002) Thyroid hormone action is disrupted by bisphenol a as an antagonist. J Clin Endocrinol Metab 87(11):5185–5190. doi:10.1210/jc.2002-020209 CrossRefPubMed

Nappi F, Barrea L, Di Somma C, Savanelli MC, Muscogiuri G, Orio F, Savatano S (2016) Endocrine aspects of environmental “Obesogen” pollutants. Int J Environ Res Public Health 13(8):765CrossRefPubMedCentral

Olea N, Pulgar R, Pérez P et al (1996) Estrogenicity of resin-based composites and sealants used in dentistry. Environ Health Perspect 104(3):298–305CrossRefPubMedPubMedCentral

Oliveira KC, da Conceição RR, Piedade GC et al (2015) Thyroid hormone modulates neuroglobin and cytoglobin in rat brain. Metab Brain Dis 30(6):1401–1408. doi:10.1007/s11011-015-9718-5 CrossRefPubMed

Preciados M, Yoo C, Roy D (2016) Estrogenic endocrine disrupting chemicals influencing NRF1 regulated gene networks in the development of complex human brain diseases. Int J Mol Sci 17(12):2086CrossRefPubMedCentral

Rashid H, Ahmad F, Rahman S et al (2009) Iron deficiency augments bisphenol A-induced oxidative stress in rats. Toxicology 256(1–2):7–12. doi:10.1016/j.tox.2008.10.022 CrossRefPubMed

Schwetz BA, Harris MW (1993) Developmental toxicology: status of the field and contribution of the National Toxicology Program. Environ Health Perspect 100:269–282CrossRefPubMedPubMedCentral

Semenza GL (2011) Hypoxia-inducible factor 1: regulator of mitochondrial metabolism and mediator of ischemic preconditioning. Biochim Biophys Acta 1813(7):1263–1268. doi:10.1016/j.bbamcr.2010.08.006 CrossRefPubMed

Sharp FR, Ran R, Lu A et al (2004) Hypoxic preconditioning protects against ischemic brain injury. NeuroRx 1(1):26–35. doi:10.1602/neurorx.1.1.26 CrossRefPubMedPubMedCentral

Staples CA, Dorn PB, Klecka GM et al (1998) A review of the environmental fate, effects, and exposures of bisphenol a. Chemosphere 36(10):2149–2173. doi:10.1016/S0045-6535(97)10133-3 CrossRefPubMed

Sun Y, Nakashima MN, Takahashi M et al (2002) Determination of bisphenol a in rat brain by microdialysis and column switching high-performance liquid chromatography with fluorescence detection. Biomed Chromatogr 16(5):319–326. doi:10.1002/bmc.161 CrossRefPubMed

Tae B, Oliveira KC, Conceição RR, Valenti VE, de Souza JS, Laureano-Melo R, Sato MA, Maciel RM, Giannocco G (2017) Evaluation of globins expression in brain, heart, and lung in rats exposed to side stream cigarette smoke. Environ Toxicol 32(4):1252–1261CrossRefPubMed

Ter-Minassian A (2006) Cerebral metabolism and brain injury. Ann Fr Anesth Réanim 25(7):714–721CrossRefPubMed

Vandenberg LN, Chahoud I, Padmanabhan V et al (2010) Biomonitoring studies should be used by regulatory agencies to assess human exposure levels and safety of bisphenol a. Environ Health Perspect 118(8):1051–1054. doi:10.1289/ehp.0901717 CrossRefPubMedPubMedCentral

Vinogradov SN, Moens L (2008) Diversity of globin function: enzymatic, transport, storage, and sensing. J Biol Chem 283(14):8773–8777. doi:10.1074/jbc.R700029200 CrossRefPubMed

Wang J, Zhang W, Sun D, Song L et al (2012) Analysis of neuroglobin mRNA expression in rat brain due to arsenite-induced oxidative stress. Environ Toxicol 27(9):503–509. doi:10.1002/tox.20664 CrossRefPubMed

Wise LM, Sadowski RN, Kim T, Willing J, Juraska JM (2016) Long-term effects of adolescent exposure to bisphenol a on neuron and glia number in the rat prefrontal cortex: differences between the sexes and cell type. Neurotoxicology 53:186–192CrossRefPubMedPubMedCentral

Wisniewski P, Romano RM, Kizys MM, Oliveira KC, Kasamatsu T, Giannocco G, Chiamolera MI, Dias-da-Silva MR, Romano MA (2015) Adult exposure to bisphenol a (BPA) in wistar rats reduces sperm quality with disruption of the hypothalamic-pituitary-testicular axis. Toxicology 329:1–9CrossRefPubMed

Xu LC, Sun H, Chen JF et al (2005) Evaluation of androgen receptor transcriptional activities of bisphenol a, octylphenol and nonylphenol in vitro. Toxicology 216(2–3):197–203. doi:10.1016/j.tox.2005.08.006 CrossRefPubMed

Xu X, Dong F, Yang Y et al (2015) Sex-specific effects of long-term exposure to bisphenol-a on anxiety- and depression-like behaviors in adult mice. Chemosphere 120:258–266. doi:10.1016/j.chemosphere.2014.07.021 CrossRefPubMed

Zhang Q, Xu X, Li T et al (2014) Exposure to bisphenol-a affects fear memory and histone acetylation of the hippocampus in adult mice. Horm Behav 65(2):106–113. doi:10.1016/j.yhbeh.2013.12.004 CrossRefPubMed

Title: Anatomical specificity of the brain in the modulation of Neuroglobin and Cytoglobin genes after chronic bisphenol a exposure
Authors: Rodrigo Rodrigues da Conceição
Janaina Sena de Souza
Kelen Carneiro de Oliveira
Rui Monteiro de Barros Maciel
Marco Aurélio Romano
Renata Marino Romano
Magnus Régios Dias da Silva
Maria Izabel Chiamolera
Gisele Giannocco
Publication date: 01-12-2017
Publisher: Springer US
Published in: Metabolic Brain Disease / Issue 6/2017
Print ISSN: 0885-7490
Electronic ISSN: 1573-7365
DOI: https://doi.org/10.1007/s11011-017-0066-5

At a glance: The STEP trials

Springer Medicine

Anatomical specificity of the brain in the modulation of Neuroglobin and Cytoglobin genes after chronic bisphenol a exposure

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

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