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Research Article

Obesity aggravates neuroinflammatory and neurodegenerative effects of bisphenol A in female rats

, , , , , , , , & ORCID Icon show all
Received 07 Jan 2024, Accepted 25 Apr 2024, Published online: 16 May 2024

References

  • Abdou HM, Abd Elkader HAE, El-Gendy AH, Eweda SM. 2022. Neurotoxicity and neuroinflammatory effects of bisphenol A in male rats: the neuroprotective role of grape seed proanthocyanidins. Environ Sci Pollut Res Int. 29(6):9257–9268. doi: 10.1007/s11356-021-16311-1.
  • Abo-Zaid OAR, Moawed FSM, Hassan HA, Moustafa EM. 2022. Hydrogen sulfide attenuates lung injury instigated by Bisphenol-A via suppressing inflammation and oxidative stress. BMC Pharmacol Toxicol. 23(1):98. doi: 10.1186/s40360-022-00636-9.
  • Ali SA, Begum T, Reza F. 2018. Hormonal influences on cognitive function. Malays J Med Sci. 25(4):31–41. doi: 10.21315/mjms2018.25.4.3.
  • Alkan I, Altunkaynak BZ, Gültekin Gİ, Bayçu C. 2021. Hippocampal neural cell loss in high-fat diet-induced obese rats-exploring the protein networks, ultrastructure, biochemical and bioinformatical markers. J Chem Neuroanat. 114:101947. doi: 10.1016/j.jchemneu.2021.101947.
  • Antunes M, Biala G. 2012. The novel object recognition memory: neurobiology, test procedure, and its modifications. Cogn Process. 13(2):93–110. doi: 10.1007/s10339-011-0430-z.
  • Balasubramanian P, Jagannathan L, Mahaley RE, Subramanian M, Gilbreath ET, Mohankumar PS, Mohankumar SM. 2012. High fat diet affects reproductive functions in female diet-induced obese and dietary resistant rats. J Neuroendocrinol. 24(5):748–755. doi: 10.1111/j.1365-2826.2011.02276.x.
  • Banerjee O, Singh S, Prasad SK, Bhattacharjee A, Banerjee A, Banerjee A, Saha A, Maji BK, Mukherjee S. 2018. Inhibition of catalase activity with 3-amino-1,2,4-triazole intensifies bisphenol A (BPA)-induced toxicity in granulosa cells of female albino rats. Toxicol Ind Health. 34(11):787–797. doi: 10.1177/0748233718795744.
  • Broughton DE, Moley KH. 2017. Obesity and female infertility: potential mediators of obesity’s impact. Fertil Steril. 107(4):840–847. doi: 10.1016/j.fertnstert.2017.01.017.
  • Cavaliere G, Trinchese G, Penna E, Cimmino F, Pirozzi C, Lama A, Annunziata C, Catapano A, Mattace Raso G, Meli R, et al. 2019. High-fat diet induces neuroinflammation and mitochondrial impairment in mice cerebral cortex and synaptic fraction. Front Cell Neurosci. 13:509. doi: 10.3389/fncel.2019.00509.
  • Chaudhari N, Talwar P, Parimisetty A, Lefebvre d’Hellencourt C, Ravanan P. 2014. A molecular web: endoplasmic reticulum stress, inflammation, and oxidative stress. Front Cell Neurosci. 8:213. doi: 10.3389/fncel.2014.00213.
  • Claiborne A. 1985. Catalase activity. In Greenwald RA ed. CRC handbook of methods in oxygen radical research. Boca Raton: CRC Press. p. 283–84.
  • Cobley JN, Fiorello ML, Bailey DM. 2018. 13 reasons why the brain is susceptible to oxidative stress. Redox Biol. 15:490–503. doi: 10.1016/j.redox.2018.01.008.
  • Convit A, Wolf OT, Tarshish C, de Leon MJ. 2003. Reduced glucose tolerance is associated with poor memory performance and hippocampal atrophy among normal elderly. Proc Natl Acad Sci U S A. 100(4):2019–2022. doi: 10.1073/pnas.0336073100.
  • Dabeer S, Afjal MA, Ahmad S, Fatima M, Habib H, Parvez S, Raisuddin S. 2020. Transgenerational effect of parental obesity and chronic parental bisphenol A exposure on hormonal profile and reproductive organs of preadolescent Wistar rats of F1 generation: a one-generation study. Hum Exp Toxicol. 39(1):59–76. doi: 10.1177/0960327119873017.
  • Diniz YS, Faine LA, Galhardi CM, Rodrigues HG, Ebaid GX, Burneiko RC, Cicogna AC, Novelli EL. 2005. Monosodium glutamate in standard and high-fiber diets: metabolic syndrome and oxidative stress in rats. Nutrition. 21(6):749–755. doi: 10.1016/j.nut.2004.10.013.
  • Dugger BN, Dickson DW. 2017. Pathology of neurodegenerative diseases. Cold Spring Harb Perspect Biol. 9(7):a028035. doi: 10.1101/cshperspect.a028035.
  • Evilsizor MN, Ray-Jones HF, Lifshitz J, Ziebell J. 2015. Primer for immunohistochemistry on cryosectioned rat brain tissue: example staining for microglia and neurons. J Vis Exp. (99):e52293. doi: 10.3791/52293.
  • Egusquiza RJ, Blumberg B. 2020. Environmental obesogens and their impact on susceptibility to obesity: new mechanisms and chemicals. Endocrinology. 161(3):bqaa024. doi: 10.1210/endocr/bqaa024.
  • Feng J, Zheng Y, Guo M, Ares I, Martínez M, Lopez-Torres B, Martínez-Larrañaga MR, Wang X, Anadón A, Martínez MA. 2023. Oxidative stress, the blood-brain barrier and neurodegenerative diseases: the critical beneficial role of dietary antioxidants. Acta Pharm Sin B. 13(10):3988–4024. doi: 10.1016/j.apsb.2023.07.010.
  • Friedewald WT, Levy RI, Fredrickson DS. 1972. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem. 18(6):499–502. doi: 10.1093/clinchem/18.6.499.
  • Gao X, Li Y, Ma Z, Jing J, Zhang Z, Liu Y, Ding Z. 2021. Obesity induces morphological and functional changes in female reproductive system through increases in NF-κB and MAPK signaling in mice. Reprod Biol Endocrinol. 19(1):148. doi: 10.1186/s12958-021-00833-x.
  • Gómez-Apo E, Mondragón-Maya A, Ferrari-Díaz M, Silva-Pereyra J. 2021. Structural brain changes associated with overweight and obesity. J Obes. 2021:6613385–6613318. doi: 10.1155/2021/6613385.
  • Goswami P, Afjal MA, Akhter J, Mangla A, Khan J, Parvez S, Raisuddin S. 2020. Involvement of endoplasmic reticulum stress in amyloid β (1-42)-induced Alzheimer’s like neuropathological process in rat brain. Brain Res Bull. 165:108–117. doi: 10.1016/j.brainresbull.2020.09.022.
  • Habig WH, Pabst MJ, Jakoby WB. 1974. Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem. 249(22):7130–7139.
  • Hamer M, Batty GD. 2019. Association of body mass index and waist-to-hip ratio with brain structure: UK Biobank study. Neurology. 92(6):e594–e600. doi: 10.1212/WNL.0000000000006879.
  • Henn RE, Elzinga SE, Glass E, Parent R, Guo K, Allouch AM, Mendelson FE, Hayes J, Webber-Davis I, Murphy GG, et al. 2022. Obesity-induced neuroinflammation and cognitive impairment in young adult versus middle-aged mice. Immun Ageing. 19(1):67. doi: 10.1186/s12979-022-00323-7.
  • Hong X, Zhou Y, Zhu Z, Li Y, Li Z, Zhang Y, Hu X, Zhu F, Wang Y, Fang M, et al. 2023. Environmental endocrine disruptor Bisphenol A induces metabolic derailment and obesity via upregulating IL-17A in adipocytes. Environ Int. 172:107759. doi: 10.1016/j.envint.2023.107759.
  • Hu F, Li T, Gong H, Chen Z, Jin Y, Xu G, Wang M. 2017. Bisphenol A impairs synaptic plasticity by both pre- and postsynaptic mechanisms. Adv Sci (Weinh). 4(8):1600493. doi: 10.1002/advs.201600493.
  • Ijaz S, Ullah A, Shaheen G, Jahan S. 2020. Exposure of BPA and its alternatives like BPB, BPF, and BPS impair subsequent reproductive potentials in adult female Sprague Dawley rats. Toxicol Mech Methods. 30(1):60–72. doi: 10.1080/15376516.2019.1652873.
  • Jie Z, Ko CJ, Wang H, Xie X, Li Y, Gu M, Zhu L, Yang JY, Gao T, Ru W, et al. 2021. Microglia promote autoimmune inflammation via the noncanonical NF-κB pathway. Sci Adv. 7(36):eabh0609. doi: 10.1126/sciadv.abh0609.
  • Jollow DJ, Mitchell JR, Zampaglione N, Gillette JR. 1974. Bromobenzene-induced liver necrosis. Protective role of glutathione and evidence for 3,4-bromobenzene oxide as the hepatotoxic metabolite. Pharmacology. 11(3):151–169. doi: 10.1159/000136485.
  • Kim SH, Kang DW, Kwon D, Jung YS. 2024. Critical role of endoplasmic reticulum stress on bisphenol A-induced cytotoxicity in human keratinocyte HaCaT cells. Environ Toxicol. 1–14. doi: 10.1002/tox.24290.
  • Kovačević S, Nestorov J, Matić G, Elaković I. 2019. Chronic stress combined with a fructose diet reduces hypothalamic insulin signaling and antioxidative defense in female rats. Neuroendocrinology. 108(4):278–290. doi: 10.1159/000496391.
  • Lai M, Lü B. 2012. Tissue preparation for microscopy and histology. ComprSampl Sample Prep. 3(1):53–93.
  • Lama A, Del Piano F, Annunziata C, Comella F, Opallo N, Melini S, Grumetto L, Pirozzi C, Mattace Raso G, Meli R, et al. 2023. Bisphenol A exacerbates anxiety-like behavior and neuroinflammation in prefrontal cortex of adult obese mice. Life Sci. 313:121301. doi: 10.1016/j.lfs.2022.121301.
  • Lee CT, Wang JY, Chou KY, Hsu MI. 2019. 1,25-Dihydroxyvitamin D3 modulates the effects of sublethal BPA on mitochondrial function via activating PI3K-Akt pathway and 17β-estradiol secretion in rat granulosa cells. J Steroid Biochem Mol Biol. 185:200–211. doi: 10.1016/j.jsbmb.2018.09.002.
  • Lee YM, Kim KS, Jacobs DR, Jr, Lee DH. 2017. Persistent organic pollutants in adipose tissue should be considered in obesity research. Obes Rev. 18(2):129–139. doi: 10.1111/obr.12481.
  • Lie ME, Overgaard A, Mikkelsen JD. 2013. Effect of a postnatal high-fat diet exposure on puberty onset, estrous cycle regularity, and kisspeptin expression in female rats. Reprod Biol. 13(4):298–308. doi: 10.1016/j.repbio.2013.08.001.
  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. 1951. Protein measurement with the Folin phenol reagent. J Biol Chem. 193(1):265–275. doi: 10.1016/S0021-9258(19)52451-6.
  • Luine VN. 2014. Estradiol and cognitive function: past, present and future. Horm Behav. 66(4):602–618. doi: 10.1016/j.yhbeh.2014.08.011.
  • Michałowicz J. 2014. Bisphenol A–sources, toxicity and biotransformation. Environ Toxicol Pharmacol. 37(2):738–758. doi: 10.1016/j.etap.2014.02.003.
  • Mezo-González CE, García Santillán JA, Reyes-Castro LA, Gourdel M, Croyal M, Bolaños-Jiménez F. 2023. Obesity-induced memory deficits in female rats are oestrous cycle dependent and linked to impaired brain kynurenine pathway metabolism. Neuroendocrinology. 113(5):549–562. doi: 10.1159/000528856.
  • Mihara M, Uchiyama M. 1978. Determination of malonaldehyde precursor in tissues by thiobarbituric acid test. Anal Biochem. 86(1):271–278. doi: 10.1016/0003-2697(78)90342-1.
  • Mohammed JN, Okaiyeto K, Haruna S, Dagang WRZW, Oguntibeju OO, Ekundayo TC. 2024. Systematic assessment on the remediation of Bisphenol A in the global environments: a mixed method analysis of research outputs. Discov Environ. 2(1). doi: 10.1007/s44274-024-00045-1.
  • Mohandas J, Marshall JJ, Duggin GG, Horvath JS, Tiller DJ. 1984. Differential distribution of glutathione and glutathione-related enzymes in rabbit kidney. Possible implications in analgesic nephropathy. Biochem Pharmacol. 33(11):1801–1807. doi: 10.1016/0006-2952(84)90353-8.
  • Monje L, Varayoud J, Muñoz-de-Toro M, Luque EH, Ramos JG. 2010. Exposure of neonatal female rats to bisphenol A disrupts hypothalamic LHRH pre-mRNA processing and estrogen receptor alpha expression in nuclei controlling estrous cyclicity. Reprod Toxicol. 30(4):625–634. doi: 10.1016/j.reprotox.2010.08.004.
  • Moon S, Seo MY, Choi K, Chang YS, Kim SH, Park MJ. 2021. Urinary bisphenol A concentrations and the risk of obesity in Korean adults. Sci Rep. 11(1):1603. doi: 10.1038/s41598-021-80980-8.
  • Moustafa GG, Ahmed AAM. 2016. Impact of prenatal and postnatal exposure to bisphenol A on female rats in a two generational study: genotoxic and immunohistochemical implications. Toxicol Rep. 3:685–695. doi: 10.1016/j.toxrep.2016.08.008.
  • Negri-Cesi P. 2015. Bisphenol A interaction with brain development and functions. Dose Response. 13(2):1559325815590394. doi: 10.1177/1559325815590394.
  • Nemati M, Zardooz H, Rostamkhani F, Abadi A, Foroughi F. 2017. High-fat diet effects on metabolic responses to chronic stress. Arch Physiol Biochem. 123(3):182–191. doi: 10.1080/13813455.2017.1295083.
  • Novelli EL, Diniz YS, Galhardi CM, Ebaid GM, Rodrigues HG, Mani F, Fernandes AA, Cicogna AC, Novelli Filho JL. 2007. Anthropometrical parameters and markers of obesity in rats. Lab Anim. 41(1):111–119. doi: 10.1258/002367707779399518.
  • O’Brien PD, Hinder LM, Callaghan BC, Feldman EL. 2017. Neurological consequences of obesity. Lancet Neurol. 16(6):465–477. doi: 10.1016/S1474-4422(17)30084-4.
  • Ozkemahli G, Balci Ozyurt A, Erkekoglu P, Zeybek ND, Yersal N, Kocer-Gumusel B. 2022. The effects of prenatal and lactational bisphenol A and/or di(2-ethylhexyl) phthalate exposure on female reproductive system. Toxicol Mech Methods. 32(8):597–605. doi: 10.1080/15376516.2022.2057265.
  • Palmisano BT, Zhu L, Eckel RH, Stafford JM. 2018. Sex differences in lipid and lipoprotein metabolism. Mol Metab. 15:45–55. doi: 10.1016/j.molmet.2018.05.008.
  • Pande S, Ranjan R, Ryazanova M, Shuvaev AN, Salmina AB, Kratasyuk VA. 2022. Buckwheat-enriched diet alleviates bisphenol A mediated oxidative stress via modulation of sirtuin 1 and antioxidant status in experimental rats. Food Chem. 373(Pt B):131507. doi: 10.1016/j.foodchem.2021.131507.
  • Peng Y, Yang H, Song J, Feng D, Na Z, Jiang H, Meng Y, Shi B, Li D. 2022. Elevated serum leptin levels as a predictive marker for polycystic ovary syndrome. Front Endocrinol (Lausanne). 13:845165. doi: 10.3389/fendo.2022.845165.
  • Pirozzi C, Lama A, Annunziata C, Cavaliere G, Ruiz-Fernandez C, Monnolo A, Comella F, Gualillo O, Stornaiuolo M, Mollica MP, et al. 2020. Oral Bisphenol A worsens liver immune-metabolic and mitochondrial dysfunction induced by high-fat diet in adult mice: cross-talk between oxidative stress and inflammasome pathway. Antioxidants (Basel). 9(12):1201. doi: 10.3390/antiox9121201.
  • Rashid CS, Bansal A, Mesaros C, Bartolomei MS, Simmons RA. 2020. Paternal bisphenol A exposure in mice impairs glucose tolerance in female offspring. Food Chem Toxicol. 145:111716. doi: 10.1016/j.fct.2020.111716.
  • Röhr F, Bucholtz N, Toepfer S, Norman K, Spira D, Steinhagen-Thiessen E, Lill CM, Bertram L, Demuth I, Buchmann N, et al. 2020. Relationship between Lipoprotein (a) and cognitive function—results from the Berlin Aging Study II. Sci Rep. 10(1):10636. doi: 10.1038/s41598-020-66783-3.
  • Salas-Venegas V, Flores-Torres RP, Rodríguez-Cortés YM, Rodríguez-Retana D, Ramírez-Carreto RJ, Concepción-Carrillo LE, Pérez-Flores LJ, Alarcón-Aguilar A, López-Díazguerrero NE, Gómez-González B, et al. 2022. The Obese Brain: mechanisms of Systemic and Local Inflammation, and Interventions to Reverse the Cognitive Deficit. Front Integr Neurosci. 16:798995. doi: 10.3389/fnint.2022.798995.
  • Sharma S, Ahmad S, Khan MF, Parvez S, Raisuddin S. 2018. In silico molecular interaction of bisphenol analogues with human nuclear receptors reveals their stronger affinity vs. classical bisphenol A. Toxicol Mech Methods. 28(9):660–669. doi: 10.1080/15376516.2018.1491663.
  • Sharma S, Ahmad S, Afjal MA, Habib H, Parvez S, Raisuddin S. 2019. Dichotomy of bisphenol A-induced expression of peroxisome proliferator-activated receptors in hepatic and testicular tissues in mice [published correction appears in Chemosphere. 2020 Jun;249:126601]. Chemosphere. 236:124264. doi: 10.1016/j.chemosphere.2019.06.234.
  • Simpson DSA, Oliver PL. 2020. ROS generation in microglia: understanding oxidative stress and inflammation in neurodegenerative disease. Antioxidants (Basel). 9(8):743. doi: 10.3390/antiox9080743.
  • Sivanathan S, Thavartnam K, Arif S, Elegino T, McGowan PO. 2015. Chronic high fat feeding increases anxiety-like behaviour and reduces transcript abundance of glucocorticoid signalling genes in the hippocampus of female rats. Behav Brain Res. 286:265–270. doi: 10.1016/j.bbr.2015.02.036.
  • Sui SX, Pasco JA. 2020. Obesity and brain function: the brain-body crosstalk. Medicina (Kaunas). 56(10):499. doi: 10.3390/medicina56100499.
  • Todd AS, Street SJ, Ziviani J, Byrne NM, Hills AP. 2015. Overweight and obese adolescent girls: the importance of promoting sensible eating and activity behaviors from the start of the adolescent period. Int J Environ Res Public Health. 12(2):2306–2329. doi: 10.3390/ijerph120202306.
  • Vekic J, Zeljkovic A, Stefanovic A, Jelic-Ivanovic Z, Spasojevic-Kalimanovska V. 2019. Obesity and dyslipidemia. Metabolism. 92:71–81. doi: 10.1016/j.metabol.2018.11.005.
  • Vilhardt F, Haslund-Vinding J, Jaquet V, McBean G. 2017. Microglia antioxidant systems and redox signalling. Br J Pharmacol. 174(12):1719–1732. doi: 10.1111/bph.13426.
  • Vishnoi S, Raisuddin S, Parvez S. 2015. Modulatory effects of an NMDAR partial agonist in MK-801-induced memory impairment. Neuroscience. 311:22–33. doi: 10.1016/j.neuroscience.2015.10.008.
  • Wang B, Wang S, Zhao Z, Chen Y, Xu Y, Li M, Xu M, Wang W, Ning G, Bi Y, et al. 2020. Bisphenol A exposure in relation to altered lipid profile and dyslipidemia among Chinese adults: a repeated measures study. Environ Res. 184:109382. doi: 10.1016/j.envres.2020.109382.
  • Wang Q, Zang F, He C, Zhang Z, Xie C, Alzheimer’s Disease Neuroimaging Initiative. 2022. Dyslipidemia induced large-scale network connectivity abnormality facilitates cognitive decline in the Alzheimer’s disease. J Transl Med. 20(1):567. doi: 10.1186/s12967-022-03786-w.
  • Wolf SA, Boddeke HW, Kettenmann H. 2017. Microglia in Physiology and Disease. Annu Rev Physiol. 79(1):619–643. doi: 10.1146/annurev-physiol-022516-034406.
  • Xu P, Chen A, Li Y, Xing X, Lu H. 2019. Medial prefrontal cortex in neurological diseases. Physiol Genomics. 51(9):432–442. doi: 10.1152/physiolgenomics.00006.2019.
  • Yamashita H, Shao J, Qiao L, Pagliassotti M, Friedman JE. 2003. Effect of spontaneous gestational diabetes on fetal and postnatal hepatic insulin resistance in Lepr(db/+) mice. Pediatr Res. 53(3):411–418. doi: 10.1203/01.PDR.0000049667.58071.7D.
  • Yoshitake R, Hirose Y, Murosaki S, Matsuzaki G. 2021. Heat-killed Lactobacillus plantarum L-137 attenuates obesity and associated metabolic abnormalities in C57BL/6 J mice on a high-fat diet. Biosci Microbiota Food Health. 40(2):84–91. doi: 10.12938/bmfh.2020-040.
  • Yin Z, Hua L, Chen L, Hu D, Li J, An Z, Tian T, Ning H, Ge Y. 2020. Bisphenol-A exposure induced neurotoxicity and associated with synapse and cytoskeleton in Neuro-2a cells. Toxicol in Vitro. 67:104911. doi: 10.1016/j.tiv.2020.104911.
  • Zhang W, Li Y, Wang T, Zhang X, Zhang J, Ji X, Lu L. 2024. Distribution and potential risk factors of bisphenol A in serum and urine among Chinese from 2004 to 2019. Front Public Health. 12:1196248. doi: 10.3389/fpubh.2024.1196248.

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