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Review Articles

An integrative translational framework for chemical induced neurotoxicity – a systematic review

, , ORCID Icon & ORCID Icon
Pages 424-438 | Received 15 Jan 2020, Accepted 28 Apr 2020, Published online: 12 Jun 2020

References

  • Adcock IM, Chung KF, Auffray C, Pison C, Sterk PJ, Djukanovic R. 2010. An integrative systems biology approach to understanding pulmonary diseases. Chest. 137(6):1410–1416.
  • Adgent MA, Hoffman K, Goldman BD, Sjödin A, Daniels JL. 2014. Brominated flame retardants in breast milk and behavioural and cognitive development at 36 months. Paediatr Perinat Epidemiol. 28(1):48–57.
  • Al Aïn S, Perry RE, Nuñez B, Kayser K, Hochman C, Brehman E, LaComb M, Wilson DA, Sullivan RM. 2017. Neurobehavioral assessment of maternal odor in developing rat pups: implications for social buffering. Soc Neurosci. 12(1):32–49.
  • Al-Mousa F, Michelangeli F. 2012. Some commonly used brominated flame retardants cause ca 2+-atpase inhibition, beta-amyloid peptide release and apoptosis in sh-sy5y neuronal cells. PLoS One. 7(4):e33059–10.
  • Asimakopoulos AG, Xue J, De Carvalho BP, Iyer A, Abualnaja KO, Yaghmoor SS, Kumosani TA, Kannan K. 2016. Urinary biomarkers of exposure to 57 xenobiotics and its association with oxidative stress in a population in Jeddah, Saudi Arabia. Environ Res. 150:573–581.
  • Audouze K, Taboureau O, Grandjean P. 2018. A systems biology approach to predictive developmental neurotoxicity of a larvicide used in the prevention of Zika virus transmission. Toxicol Appl Pharmacol. 354:56–63.
  • Auffray C, Imbeaud S, Roux-Rouquié M, Hood L. 2003. From functional genomics to systems biology: Concepts and practices. Comptes Rendus – Biol. 326(10-11):879–892.
  • Bal-Price A, Crofton KM, Sachana M, Shafer TJ, Behl M, Forsby A, Hargreaves A, Landesmann B, Lein PJ, Louisse J, et al. 2015. Putative adverse outcome pathways relevant to neurotoxicity. Crit Rev Toxicol. 45(1):83–91.
  • Bal-Price A, Lein PJ, Keil KP, Sethi S, Shafer T, Barenys M, Fritsche E, Sachana M, Meek ME(B). 2017. Developing and applying the adverse outcome pathway concept for understanding and predicting neurotoxicity. Neurotoxicology. 59:240–255.
  • Basha MR, Braddy NS, Zawia NH, Kodavanti P. 2006. Ontogenetic alterations in prototypical transcription factors in the rat cerebellum and hippocampus following perinatal exposure to a commercial PCB mixture. Neurotoxicology. 27(1):118–124.
  • Benfenati E, Diaza RG, Cassano A, Pardoe S, Gini G, Mays C, Knauf R, Benighaus L. 2011. The acceptance of in silico models for REACH: requirements, barriers, and perspectives. Chem Cent J. 5:58
  • Boberg J, Dybdahl M, Petersen A, Hass U, Svingen T, Vinggaard AM. 2019. A pragmatic approach for human risk assessment of chemical mixtures. Curr Opin Toxicol. 15:1–7.
  • Boix J, Cauli O, Felipo V. 2010. Developmental exposure to polychlorinated biphenyls 52, 138 or 180 affects differentially learning or motor coordination in adult rats. mechanisms involved. Neuroscience. 167(4):994–1003.
  • Bornstein SR, Licinio J. 2011. Improving the efficacy of translational medicine by optimally integrating health care, academia and industry. Nat Med. 17(12):1567–1569.
  • Bradner JM, Suragh TA, Caudle WM. 2013. Alterations to the circuitry of the frontal cortex following exposure to the polybrominated diphenyl ether mixture, DE-71. Toxicology. 312:48–55.
  • Braun JM, Bellinger DC, Hauser R, Wright RO, Chen A, Calafat AM, Yolton K, Lanphear BP. 2017a. Prenatal phthalate, triclosan, and bisphenol A exposures and child visual-spatial abilities. Neurotoxicology. 58:75–83.
  • Braun JM, Yolton K, Stacy SL, Erar B, Papandonatos GD, Bellinger DC, Lanphear BP, Chen A. 2017b. Prenatal environmental chemical exposures and longitudinal patterns of child neurobehavior. Neurotoxicology. 62:192–199.
  • Breznan D, Karthikeyan S, Phaneuf M, Kumarathasan P, Cakmak S, Denison MS, Brook JR, Vincent R. 2015. Development of an integrated approach for comparison of in vitro and in vivo responses to particulate matter. Part Fibre Toxicol. 13(1):1–24.
  • Brunelli L, LLansola M, Felipo V, Campagna R, Airoldi L, De Paola M, Fanelli R, Mariani A, Mazzoletti M, Pastorelli R, et al. 2012. Insight into the neuroproteomics effects of the food-contaminant non-dioxin like polychlorinated biphenyls. J Proteomics. 75(8):2417–2430.
  • Burczynski ME. 2000. Toxicogenomics-based discrimination of toxic mechanism in hepg2 human hepatoma cells. Toxicol Sci. 58(2):399–415.
  • Bushnell PJ, Kavlock RJ, Crofton KM, Weiss B, Rice DC. 2010. Behavioral toxicology in the 21st century: Challenges and opportunities for behavioral scientists. Summary of a symposium presented at the annual meeting of the Neurobehavioral Teratology Society, June. Neurotoxicol Teratol. 32(3):313–328.
  • Canzoniero LMT, Di Renzo G, Molinaro P, Montuori P, Mascolo L, Formisano L, Guida N, Laudati G, Serani A. 2017. The neurotoxicant PCB-95 by increasing the neuronal transcriptional repressor REST down-regulates caspase-8 and increases Ripk1, Ripk3 and MLKL expression determining necroptotic neuronal death. Biochem Pharmacol. 142:229–241.
  • Carrasco MA, Hidalgo C. 2006. Calcium microdomains and gene expression in neurons and skeletal muscle cells. Cell Calcium. 40(5-6):575–583.
  • Chen H, Streifel KM, Singh V, Yang D, Mangini L, Wulff H, Lein PJ. 2017. From the cover: BDE-47 and BDE-49 inhibit axonal growth in primary rat hippocampal neuron-glia co-cultures via ryanodine receptor-dependent mechanisms. Toxicol Sci. 156(2):375–386.
  • Chen J, Li X, Li X, Chen D. 2018. The environmental pollutant BDE-209 regulates NO/cGMP signaling through activation of NMDA receptors in neurons. Environ Sci Pollut Res. 25(4):3397–3407.
  • Chen MH, Ha EH, Liao HF, Jeng SF, Su YN, Wen TW, Lien GW, Chen CY, Hsieh WS, Chen PC, et al. 2013. Perfluorinated compound levels in cord blood and neurodevelopment at 2 years of age. Epidemiology. 24(6):800–808.
  • Chen T, Yang W, Li Y, Chen X, Xu S. 2011. Mono-(2-ethylhexyl) phthalate impairs neurodevelopment: Inhibition of proliferation and promotion of differentiation in PC12 cells. Toxicol Lett. 201(1):34–41.
  • Chen Y, Cheng F, Sun L, Li W, Liu G, Tang Y. 2014. Computational models to predict endocrine-disrupting chemical binding with androgen or oestrogen receptors. Ecotoxicol Environ Saf. 110:280–287.
  • Chiu W. 2017. "Chemical risk assessment and translation to socio-economic assessments", OECD Environment Working Papers, No. 117, OECD Publishing, Paris. DOI:10.1787/a930054b-en
  • Cho JH, Kim AH, Lee S, Lee Y, Lee WJ, Chang SC, Lee J. 2018. Sensitive neurotoxicity assessment of bisphenol A using double immunocytochemistry of DCX and MAP2. Arch Pharm Res. 41(11):1098–1107.
  • Coecke S, Eskes C, Gartlon J, Kinsner A, Price A, van Vliet E, Prieto P, Boveri M, Bremer S, Adler S, et al. 2006. The value of alternative testing for neurotoxicity in the context of regulatory needs. Environ Toxicol Pharmacol. 21(2):153–167.
  • Costa LG, Fattori V, Giordano G, Vitalone A. 2007. An in vitro approach to assess the toxicity of certain food contaminants: Methylmercury and polychlorinated biphenyls. Toxicology. 237(1-3):65–76.
  • Costa LG, Tagliaferri S, Roqué PJ, Pellacani C. 2016. Role of glutamate receptors in tetrabrominated diphenyl ether (BDE-47) neurotoxicity in mouse cerebellar granule neurons. Toxicol Lett. 241:159–166.
  • Cowell WJ, Sjödin A, Jones R, Wang Y, Wang S, Herbstman JB. 2018. Determinants of prenatal exposure to polybrominated diphenyl ethers (PBDEs) among urban, minority infants born between 1998 and 2006. Environ Pollut. 233:774–781.
  • Craciunoiu O, Holsti L. 2017. A systematic review of the predictive validity of neurobehavioral assessments during the preterm period. Phys Occup Ther Pediatr. 37(3):292–307.
  • Croom EL, Shafer TJ, Evans MV, Mundy WR, Eklund CR, Johnstone AFM, Mack CM, Pegram RA. 2015. Improving in vitro to in vivo extrapolation by incorporating toxicokinetic measurements: A case study of lindane-induced neurotoxicity. Toxicol Appl Pharmacol. 283(1):9–19.
  • Dingemans MML, Heusinkveld HJ, De Groot A, Bergman Å, Van den Berg M, Westerink R. 2009. Hexabromocyclododecane inhibits depolarization-induced increase in intracellular calcium levels and neurotransmitter release in PC12 cells. Toxicol Sci. 107(2):490–497.
  • Dingemans MML, Ramakers GMJ, Gardoni F, van Kleef RGDM, Bergman Å, Di Luca M, van den Berg M, Westerink RHS, Vijverberg HPM. 2007. Neonatal exposure to brominated flame retardant BDE-47 reduces long-term potentiation and postsynaptic protein levels in mouse hippocampus. Environ Health Perspect. 115(6):865–870.
  • Dishaw LV, Powers CM, Ryde IT, Roberts SC, Seidler FJ, Slotkin TA, Stapleton HM. 2011. Is the PentaBDE replacement, tris (1,3-dichloro-2-propyl) phosphate (TDCPP), a developmental neurotoxicant? Studies in PC12 cells. Toxicol Appl Pharmacol. 256(3):281–289.
  • Doherty BT, Engel SM, Buckley JP, Silva MJ, Calafat AM, Wolff MS. 2017. Prenatal phthalate biomarker concentrations and performance on the Bayley Scales of Infant Development-II in a population of young urban children. Environ Res. 152:51–58.
  • Dolgos H, Trusheim M, Gross D, Halle J-P, Ogden J, Osterwalder B, Sedman E, Rossetti L. 2016. Translational Medicine Guide transforms drug development processes: the recent Merck experience. Drug Discov Today. 21(3):517–526.
  • Drolet BC, Lorenzi NM. 2011. Translational research: Understanding the continuum from bench to bedside. Transl Res. 157(1):1–5.
  • Eeles AL, Olsen JE, Walsh JM, McInnes EK, Molesworth CML, Cheong JLY, Doyle LW, Spittle AJ. 2017. Reliability of neurobehavioral assessments from birth to term equivalent age in preterm and term born infants. Phys Occup Ther Pediatr. 37(1):108–119.
  • European Chemicals Agency. 2006. Guidance on information requirements and chemical safety assessment Chapter R.16: Environmental Exposure Estimation.
  • Fàbrega F, Kumar V, Schuhmacher M, Domingo JL, Nadal M. 2014. PBPK modeling for PFOS and PFOA: Validation with human experimental data. Toxicol Lett. 230(2):244–251.
  • Fàbrega F, Nadal M, Schuhmacher M, Domingo JL, Kumar V. 2016. Influence of the uncertainty in the validation of PBPK models: A case-study for PFOS and PFOA. Regul Toxicol Pharm. 77:230–239.
  • Fan CY, Besas J, Kodavanti P. 2010. Changes in mitogen-activated protein kinase in cerebellar granule neurons by polybrominated diphenyl ethers and polychlorinated biphenyls. Toxicol Appl Pharmacol. 245(1):1–8.
  • Fanelli R, De Paola M, Brunelli L, Felipo V, Airoldi L, Pastorelli R, Llansola M, Campagna R, Mariani A, Mazzoletti M. 2012. Insight into the neuroproteomics effects of the food-contaminant non-dioxin like polychlorinated biphenyls. J Proteomics. 75(8):2417–2430.
  • Fonnum F, Mariussen E. 2009. Mechanisms involved in the neurotoxic effects of environmental toxicants such as polychlorinated biphenyls and brominated flame retardants. J Neurochem. 111(6):1327–1347.
  • Fritsche E, Grandjean P, Crofton KM, Aschner M, Goldberg A, Heinonen T, Hessel EVS, Hogberg HT, Bennekou SH, Lein PJ, et al. 2018. Consensus statement on the need for innovation, transition and implementation of developmental neurotoxicity (DNT) testing for regulatory purposes. Toxicol Appl Pharmacol. 354:3–6.
  • Gartlon J, Kinsner A, Bal-Price A, Coecke S, Clothier RH. 2006. Evaluation of a proposed in vitro test strategy using neuronal and non-neuronal cell systems for detecting neurotoxicity. Toxicol Vitr. 20(8):1569–1581.
  • Gascon M, Verner M-A, Guxens M, Grimalt JO, Forns J, Ibarluzea J, Lertxundi N, Ballester F, Llop S, Haddad S, et al. 2013. Evaluating the neurotoxic effects of lactational exposure to persistent organic pollutants (POPs) in Spanish children. Neurotoxicology. 34:9–15.
  • Gassmann K, Schreiber T, Dingemans MML, Krause G, Roderigo C, Giersiefer S, Schuwald J, Moors M, Unfried K, Bergman Å, et al. 2014. BDE-47 and 6-OH-BDE-47 modulate calcium homeostasis in primary fetal human neural progenitor cells via ryanodine receptor-independent mechanisms. Arch Toxicol. 88(8):1537–1548.
  • Gaum PM, Gube M, Schettgen T, Putschögl FM, Kraus T, Fimm B, et al. 2017. Polychlorinated biphenyls and depression: Cross-sectional and longitudinal investigation of a dopamine-related Neurochemical path in the German HELPcB surveillance program. Environ Heal A Glob Access Sci Source. 16:106.
  • Gee JR, Moser VC, McDanie KL, Herr DW. 2011. Neurochemical changes following a single dose of polybrominated diphenyl ether 47 in mice. Drug Chem Toxicol. 34(2):213–219.
  • Geschwind DH, Konopka G. 2009. Neuroscience in the era of functional genomics and systems biology. Nature. 461(7266):908–915.
  • Giordano G, Kavanagh TJ, Costa LG. 2008. Neurotoxicity of a polybrominated diphenyl ether mixture (DE-71) in mouse neurons and astrocytes is modulated by intracellular glutathione levels. Toxicol Appl Pharmacol. 232(2):161–168.
  • Giordano G, Kavanagh TJ, Costa LG. 2009. Mouse cerebellar astrocytes protect cerebellar granule neurons against toxicity of the polybrominated diphenyl ether (PBDE) mixture DE-71. Neurotoxicology. 30(2):326–329.
  • Goudarzi H, Nakajima S, Ikeno T, Sasaki S, Kobayashi S, Miyashita C, Ito S, Araki A, Nakazawa H, Kishi R. 2016. Prenatal exposure to perfluorinated chemicals and neurodevelopment in early infancy: The Hokkaido Study. Sci Total Environ. 541:1002–1010.
  • Grandjean P, Landrigan P. 2006. Developmental neurotoxicity of industrial chemicals. Lancet. 368(9553):2167–2178.
  • Grandjean P, White RF, Weihe P. 1996. Neurobehavioral Epidemiology: Application in Risk Assessment. Environ Health Perspect. 104:397.
  • Hartung T, Daston G. 2009. Are in vitro tests suitable for regulatory use?. Toxicol Sci. 111(2):233–237.
  • Hendriks HS, Koolen LAE, Dingemans MML, Viberg H, Lee I, Leonards PEG, Ramakers GMJ, Westerink RHS. 2015. Effects of neonatal exposure to the flame retardant tetrabromobisphenol-A, aluminum diethylphosphinate or zinc stannate on long-term potentiation and synaptic protein levels in mice. Arch Toxicol. 89(12):2345–2354.
  • Hendriks HS, Meijer M, Muilwijk M, Van Den Berg M, Westerink R. 2014. A comparison of the in vitro cyto- and neurotoxicity of brominated and halogen-free flame retardants: Prioritization in search for safe(r) alternatives. Arch Toxicol. 88(4):857–869.
  • Hendriks HS, Van Kleef R, Van den Berg M, Westerink R. 2012. Multiple novel modes of action involved in the in vitro neurotoxic effects of tetrabromobisphenol-A. Toxicol Sci. 128(1):235–246.
  • Hendriks HS, Westerink R. 2015. Neurotoxicity and risk assessment of brominated and alternative flame retardants. Neurotoxicol Teratol. 52(Pt B):248–269.
  • Hirsch C, Striegl B, Mathes S, Adlhart C, Edelmann M, Bono E, Gaan S, Salmeia KA, Hoelting L, Krebs A, et al. 2017. Multiparameter toxicity assessment of novel DOPO-derived organophosphorus flame retardants. Arch Toxicol. 91(1):407–425.
  • Holland EB, Feng W, Zheng J, Dong Y, Li X, Lehmler H-J, Pessah IN. 2017. An extended structure-Activity relationship of nondioxin-like PCBs evaluates and supports modeling predictions and identifies picomolar potency of PCB 202 towards ryanodine receptors. Toxicol Sci. 155(1):170–181.
  • Huang R, Xia M, Sakamuru S, Zhao J, Shahane SA, Attene-Ramos M, Zhao T, Austin CP, Simeonov A. 2016. Modelling the Tox21 10 K chemical profiles for in vivo toxicity prediction and mechanism characterization. Nat Commun. 7(1):1–10.
  • Hughes C, Waters M, Allen D, Obasanjo I. 2013. Translational toxicology: a developmental focus for integrated research strategies. BMC Pharmacol Toxicol. 14:51. DOI: 10.1186/2050-6511-14-51
  • Ishido M, Suzuki J. 2014. Classification of phthalates based on an in vitro neurosphere assay using rat mesencephalic neural stem cells. J Toxicol Sci. 39(1):25–32.
  • Jiang C, Zhang S, Liu H, Zeng Q, Xia T, Chen Y, Kuang G, Zhao G, Wu X, Zhang X, et al. 2012. The role of the IRE1 pathway in PBDE-47-induced toxicity in human neuroblastoma SH-SY5Y cells in vitro. Toxicol Lett. 211(3):325–333.
  • Karri V, Kumar V, Ramos D, Oliveira E, Schuhmacher M. 2018a. Comparative in vitro toxicity evaluation of heavy metals (lead, cadmium, arsenic, and methylmercury) on HT-22 hippocampal cell line. Biol Trace Elem Res. 184(1):226–239.
  • Karri V, Ramos D, Martinez JB, Odena A, Oliveira E, Coort SL, Evelo CT, Mariman ECM, Schuhmacher M, Kumar V, et al. 2018b. Differential protein expression of hippocampal cells associated with heavy metals (Pb, As, and MeHg) neurotoxicity: deepening into the molecular mechanism of neurodegenerative diseases. J Proteomics. 187:106–125.
  • Karri V, Kumar V, Ramos D, Oliveira E, Schuhmacher M. 2018c. An in vitro cytotoxic approach to assess the toxicity of heavy metals and their binary mixtures on hippocampal HT-22 cell line. Toxicol Lett. 282:25–36.
  • Karri V, Schuhmacher M, Kumar V. 2016. Heavy metals (Pb, Cd, MeHg, As) as risk factors for cognitive dysfunction: A general review of metal mixture mechanism in Brain. Environ Toxicol Pharmacol. 48:203–2013.
  • Karri V, Schuhmacher M, Kumar V. 2020. A systems toxicology approach to compare the heavy metal mixtures (Pb, As, MeHg) impact in neurodegenerative diseases. Food Chem Toxicol. 139:111257. (In Press);
  • Kim KH, Pessah IN. 2011. Perinatal exposure to environmental polychlorinated biphenyls sensitizes hippocampus to excitotoxicity ex vivo. Neurotoxicology. 32(6):981–985.
  • Kolodkin A, Sharma RP, Colangelo AM, Ignatenko A, Martorana F, Jennen D, et al. 2019. Design principles of ROS dynamic networks relevant to precision therapies for age-related diseases. bioRxiv. 647776
  • Krauss M, Hofmann U, Schafmayer C, Igel S, Schlender J, Mueller C, Brosch M, von Schoenfels W, Erhart W, Schuppert A, et al. 2017. Translational learning from clinical studies predicts drug pharmacokinetics across patient populations. NPJ Syst Biol Appl. 3:11. DOI:10.1038/s41540-017-0012-5.
  • Langeveld WT, Meijer M, Westerink R. 2012. Differential effects of 20 non-dioxin-like PCBs on basal and depolarization-evoked intracellular calcium levels in PC12 cells. Toxicol Sci. 126(2):487–496.
  • Laroche C, Aggarwal M, Bender H, Benndorf P, Birk B, Crozier J, Dal Negro G, De Gaetano F, Desaintes C, Gardner I, et al. 2018. Finding synergies for 3Rs – Toxicokinetics and read-across: Report from an EPAA partners’ Forum. Regul Toxicol Pharmacol. 99:5–21.
  • Le HH, Carlson EM, Chua JP, Belcher SM. 2008. Bisphenol A is released from polycarbonate drinking bottles and mimics the neurotoxic actions of estrogen in developing cerebellar neurons. Toxicol Lett. 176(2):149–156.
  • Lee YM, Seong MJ, Lee JW, Lee YK, Kim TM, Nam S-Y, Kim DJ, Yun YW, Kim TS, Han SY, et al. 2007. Estrogen receptor independent neurotoxic mechanism of bisphenol A, an environmental estrogen. J Vet Sci. 8(1):27–38.
  • Lei ENY, Yau MS, Yeung CC, Murphy MB, Wong KL, Lam M. 2017. Profiling of selected functional metabolites in the central nervous system of Marine Medaka (Oryzias melastigma) for environmental neurotoxicological assessments. Arch Environ Contam Toxicol. 72(2):269–280.
  • Lesiak A, Zhu M, Chen H, Appleyard SM, Impey S, Lein PJ, Wayman GA. 2014. The environmental neurotoxicant PCB 95 promotes synaptogenesis via ryanodine receptor-dependent miR132 upregulation. J Neurosci. 34(3):717–725.
  • Li J, Settivari R, LeBaron MJ, Marty MS. 2019. An industry perspective: a streamlined screening strategy using alternative models for chemical assessment of developmental neurotoxicity. Neurotoxicology. 73:17–30.
  • Li T, Wang W, Pan YW, Xu L, Xia Z. 2013. A hydroxylated metabolite of flame-retardant PBDE-47 decreases the survival, proliferation, and neuronal differentiation of primary cultured adult neural stem cells and interferes with signaling of ERK5 map kinase and neurotrophin 3. Toxicol Sci. 134(1):111–124.
  • Li R, Zhou P, Guo Y, Zhou B. 2017. The involvement of autophagy and cytoskeletal regulation in TDCIPP-induced SH-SY5Y cell differentiation. Neurotoxicology. 62:14–23.
  • Lien G-W, Huang C-C, Shiu J-S, Chen M-H, Hsieh W-S, Guo Y-L, Chen P-C. 2016. Perfluoroalkyl substances in cord blood and attention deficit/hyperactivity disorder symptoms in seven-year-old children. Chemosphere. 156:118–127.
  • Linne ML. 2018. Neuroinformatics and computational modelling as complementary tools for neurotoxicology studies. Basic Clin Pharmacol Toxicol. 123:56–61.
  • Liu H, Papa E, Walker JD, Gramatica P. 2007. In silico screening of estrogen-like chemicals based on different nonlinear classification models. J Mol Graph Model. 26(1):135–144.
  • Liu QS, Liu N, Sun Z, Zhou Q, Jiang G. 2018. Intranasal administration of tetrabromobisphenol A bis(2-hydroxyethyl ether) induces neurobehavioral changes in neonatal Sprague Dawley rats. J Environ Sci (China). 63:76–86.
  • Liu X, Jin Y, Liu W, Wang F, Hao S. 2011. Possible mechanism of perfluorooctane sulfonate and perfluorooctanoate on the release of calcium ion from calcium stores in primary cultures of rat hippocampal neurons. Toxicol Vitr. 25(7):1294–1301.
  • Lyng GD, Seegal RF. 2008. Polychlorinated biphenyl-induced oxidative stress in organotypic co-cultures: Experimental dopamine depletion prevents reductions in GABA. Neurotoxicology. 29(2):301–308.
  • Lyng GD, Snyder-Keller A, Seegal RF. 2007. Polychlorinated Biphenyl-Induced Neurotoxicity in Organotypic Cocultures of Developing Rat Ventral Mesencephalon and Striatum. Toxicol Sci. 97(1):128–139.
  • Ma P, Liu X, Wu J, Yan B, Zhang Y, Lu Y, Wu Y, Liu C, Guo J, Nanberg E, et al. 2015. Cognitive deficits and anxiety induced by diisononyl phthalate in mice and the neuroprotective effects of melatonin. Sci Rep. 5(1):14.
  • Maffini MV, Neltner TG. 2015. Brain drain: the cost of neglected responsibilities in evaluating cumulative effects of environmental chemicals. J Epidemiol Community Health. 69(5):496–499.
  • Malkiewicz K, Mohammed R, Folkesson R, Winblad B, Szutowski M, Benedikz E. 2006. Polychlorinated biphenyls alter expression of α-synuclein, synaptophysin and parkin in the rat brain. Toxicol Lett. 161(2):152–158.
  • Martínez MA, Rovira J, Prasad Sharma R, Nadal M, Schuhmacher M, Kumar V. 2018. Comparing dietary and non-dietary source contribution of BPA and DEHP to prenatal exposure: a Catalonia (Spain) case study. Environ Res. 166:25–34.
  • Mochida S. 2000. Protein–protein interactions in neurotransmitter release. Neurosci Res. 36(3):175–182.
  • Morfeld P, Bruch J, Levy L, Ngiewih Y, Chaudhuri I, Muranko HJ, Myerson R, McCunney RJ. 2015. Translational toxicology in setting occupational exposure limits for dusts and hazard classification – a critical evaluation of a recent approach to translate dust overload findings from rats to humans. Part Fibre Toxicol. 12. DOI:10.1186/s12989-015-0079-3
  • Morris E, Wood A, DeWitt JC, Franklin JN, Bryan I, Hu Q. 2012. Does developmental exposure to perflurooctanoic acid (PFOA) induce immunopathologies commonly observed in neurodevelopmental disorders? Neurotoxicology. 33(6):1491–1498.
  • Moser VC, Phillips PM, Hedge JM, McDaniel KL. 2015. Neurotoxicological and thyroid evaluations of rats developmentally exposed to tris(1,3-dichloro-2-propyl)phosphate (TDCIPP) and tris(2-chloro-2-ethyl)phosphate (TCEP). Neurotoxicol Teratol. 52:236–247.
  • Mumtaz MM, Ray M, Crowell SR, Keys D, Fisher J, Ruiz P. 2012. Translational research to develop a human pbpk models tool kit-volatile organic compounds (VOCS). J Toxicol Environ Heal - Part A Curr Issues. 75(1):6–24.
  • Ndountse LT, Chan HM. 2009. Role of N-methyl-D-aspartate receptors in polychlorinated biphenyl mediated neurotoxicity. Toxicol Lett. 184(1):50–55.
  • Park HY, Hertz-Picciotto I, Sovcikova E, Kocan A, Drobna B, Trnovec T. 2010. Neurodevelopmental toxicity of prenatal polychlorinated biphenyls (PCBs) by chemical structure and activity: A birth cohort study. Environ Heal A Glob Access Sci Source. 9:1–13.
  • Pham-Lake C, Aronoff EB, Camp CR, Vester A, Peters SJ, Caudle WM. 2017. Impairment in the mesohippocampal dopamine circuit following exposure to the brominated flame retardant. HBCDD. Environ Toxicol Pharmacol. 50:167–174.
  • Philips EM, Jaddoe VWV, Asimakopoulos AG, Kannan K, Steegers EAP, Santos S, Trasande L. 2018. Bisphenol and phthalate concentrations and its determinants among pregnant women in a population-based cohort in the Netherlands, 2004–5. Environ Res. 161:562–572.
  • Phillips JA, Bogdanffy MS. 2017. Editorial overview: translational biomarker concepts and practices for toxicological assessment. Curr Opin Toxicol. 4:i–iii.
  • Pradeep P, Carlson LM, Judson R, Lehmann GM, Patlewicz G. 2019. Integrating data gap filling techniques: A case study predicting TEFs for neurotoxicity TEQs to facilitate the hazard assessment of polychlorinated biphenyls. Regul Toxicol Pharmacol. 101:12–23.
  • Ramoju SP, Mattison DR, Milton B, McGough D, Shilnikova N, Clewell HJ, Yoon M, Taylor MD, Krewski D, Andersen ME, et al. 2017. The application of PBPK models in estimating human brain tissue manganese concentrations. Neurotoxicology. 58:226–237.
  • Rayne S, Forest K. 2010. Quantitative structure-activity relationship (QSAR) studies for predicting activation of the ryanodine receptor type 1 channel complex (RyR1) by polychlorinated biphenyl (PCB) congeners. J Environ Sci Heal - Part A Toxic/Hazardous Subst Environ Eng. 45(3):355–362.
  • Reistad T, Fonnum F, Mariussen E. 2006. Neurotoxicity of the pentabrominated diphenyl ether mixture, DE-71, and hexabromocyclododecane (HBCD) in rat cerebellar granule cells in vitro. Arch Toxicol. 80(11):785–796.
  • Rice D, Barone S. 2000. Critical periods of vulnerability for the developing nervous system: Evidence from humans and animal models. Environ Health Perspect. 108(suppl 3):511–533.
  • Roberts RA, Aschner M, Calligaro D, Guilarte TR, Hanig JP, Herr DW, Hudzik TJ, Jeromin A, Kallman MJ, Liachenko S, et al. 2015. Translational biomarkers of neurotoxicity: A health and environmental sciences institute perspective on the way forward. Toxicol Sci. 148(2):332–340.
  • Rodrigo R, Felipo V, Montoliu C, Piedrafita B, Llansola M. 2009. Polychlorinated Biphenyls PCB 153 and PCB 126 Impair the Glutamate–Nitric Oxide–cGMP Pathway in Cerebellar Neurons in Culture by Different Mechanisms. Neurotox Res. 16(2):97–105.
  • Roncaglioni A, Toropov AA, Toropova AP, Benfenati E. 2013. In silico methods to predict drug toxicity. Curr Opin Pharmacol. 13(5):802–806.
  • Ruan DY, Wang M, Chen L, Tao Y, Xing T, Chen J. 2009. Effects of decabrominated diphenyl ether (pbde 209) exposure at different developmental periods on synaptic plasticity in the dentate gyrus of adult rats in vivo. Toxicol Sci. 110(2):401–410.
  • Sayre LM, Perry G, Smith MA. 2008. Oxidative stress and neurotoxicity. Chem Res Toxicol. 21(1):172–188.
  • Schreiber T, Gassmann K, Götz C, Hübenthal U, Moors M, Krause G, Merk HF, Nguyen N-H, Scanlan TS, Abel J, et al. 2009. Polybrominated Diphenyl Ethers Induce Developmental Neurotoxicity in a Human in Vitro Model: Evidence for Endocrine Disruption. Environ Health Perspect. 118:572–578.
  • Schreiber T, Gassmann K, Götz C, Hübenthal U, Moors M, Krause G, Merk HF, Nguyen N-H, Scanlan TS, Abel J, et al. 2010. Polybrominated Diphenyl Ethers Induce Developmental Neurotoxicity in a Human in Vitro Model: Evidence for Endocrine Disruption. Environ Health Perspect. 118(4):572–578.
  • Sertbas M, Ulgen KO. 2018. Unlocking human brain metabolism by genome-scale and multiomics metabolic models: Relevance for neurology research, health, and disease. Omi A J Integr Biol. 22(7):455–467.
  • Sethi S, Keil KP, Lein PJ. 2017. Species and sex differences in the morphogenic response of primary rodent neurons to 3,3’-dichlorobiphenyl (PCB 11). Toxics. 6:4.
  • Sethi S, Keil KP, Lein PJ. 2018. 3,3′-Dichlorobiphenyl (PCB 11) promotes dendritic arborization in primary rat cortical neurons via a CREB-dependent mechanism. Arch Toxicol. 92(11):3337–3345.
  • Shah R, Pico AR, Freedman JE. 2016. Translational epidemiology: entering a brave new world of team science. Circ Res. 119(10):1060–1062.
  • Sharma R, Kumar V, Schuhmacher M, Kolodkin A, Westerhoff H. 2020. Development and evaluation of a harmonized whole body physiologically based pharmacokinetic (PBPK) model for flutamide in rats and its extrapolation to humans. Environ Res. 182:108948.
  • Sharma RP, Schuhmacher M, Kumar V. 2017. Developing integrated PBPK/PD coupled mechanistic pathway model (miRNA-BDNF): An approach towards system toxicology. Toxicol Lett. 280:79–91.
  • Sharma RP, Schuhmacher M, Kumar V. 2018. The development of a pregnancy PBPK Model for Bisphenol A and its evaluation with the available biomonitoring data. Sci Total Environ. 624:55–68.
  • Shin MY, Lee S, Kim HJ, Lee J, Choi G, Choi S, Kim S, Kim S, Park J, Moon HB, et al. 2016. Polybrominated diphenyl ethers in maternal serum, breast milk, umbilical cord serum, and house dust in a South Korean birth panel of mother-neonate pairs. IJERPH. 13(8):767.
  • Shrestha S, Bloom MS, Yucel R, Seegal RF, Rej R, McCaffrey RJ, Wu Q, Kannan K, Fitzgerald EF. 2017. Perfluoroalkyl substances, thyroid hormones, and neuropsychological status in older adults. Int J Hyg Environ Health. 220(4):679–685.
  • Silbereis JC, Pochareddy S, Zhu Y, Li M, Sestan N. 2016. The cellular and molecular landscapes of the developing human central nervous system. Neuron. 89(2):248–268.
  • Sirenko O, Parham F, Dea S, Sodhi N, Biesmans S, Mora-Castilla S, Ryan K, Behl M, Chandy G, Crittenden C, et al. 2019. Functional and mechanistic neurotoxicity profiling using human iPSC-derived neural 3D cultures. Toxicol Sci. 167(1):58–76.
  • Slotkin TA, MacKillop EA, Melnick RL, Thayer KA, Seidler FJ. 2008. Developmental neurotoxicity of perfluorinated chemicals modeled in vitro. Environ Health Perspect. 116(6):716–722.
  • Slotkin TA, Skavicus S, Stapleton HM, Seidler FJ. 2017. Brominated and organophosphate flame retardants target different neurodevelopmental stages, characterized with embryonic neural stem cells and neuronotypic PC12 cells. Toxicology. 390:32–42.
  • Stenberg M, Hamers T, Machala M, Fonnum F, Stenius U, Lauy A-A, van Duursen MBM, Westerink RHS, Fernandes ECA, Andersson PL. 2011. Multivariate toxicity profiles and QSAR modeling of non-dioxin-like PCBs - An investigation of in vitro screening data from ultra-pure congeners. Chemosphere. 85(9):1423–1429.
  • Szychowski KA, Wójtowicz AK. 2016. TBBPA causes neurotoxic and the apoptotic responses in cultured mouse hippocampal neurons in vitro. Pharmacol Reports. 68(1):20–26.
  • Tagliaferri S, Caglieri A, Goldoni M, Pinelli S, Alinovi R, Poli D, Pellacani C, Giordano G, Mutti A, Costa LG, et al. 2010. Low concentrations of the brominated flame retardants BDE-47 and BDE-99 induce synergistic oxidative stress-mediated neurotoxicity in human neuroblastoma cells. Toxicol in Vitro. 24(1):116–122.
  • Timchalk C, Nolan RJ, Mendrala AL, Dittenber DA, Brzak KA, Mattsson JL. 2002. A physiologically based pharmacokinetic and pharmacodynamic (PBPK/PD) model for the organophosphate insecticide chlorpyrifos in rats and humans. Toxicol Sci. 66(1):34–53.
  • Tofighi R, Wan Ibrahim WN, Rebellato P, Andersson PL, Uhlén P, Ceccatelli S. 2011. Non-dioxin-like polychlorinated biphenyls interfere with neuronal differentiation of embryonic neural stem cells. Toxicol Sci. 124(1):192–201.
  • Tollefsen KE, Scholz S, Cronin MT, Edwards SW, de Knecht J, Crofton K, Garcia-Reyero N, Hartung T, Worth A, Patlewicz G. 2014. Applying Adverse Outcome Pathways (AOPs) to support Integrated Approaches to Testing and Assessment (IATA). Regul Toxicol Pharmacol. 70(3):629–640.
  • Tsatsakis A, Goumenou M, Liesivuori J, Dekant W, Hernández AF. 2019. Toxicology for real-life risk simulation – Editorial preface to this special issue. Toxicol Lett. 309:33–34.
  • Tsatsakis AM, Docea AO, Tsitsimpikou C. 2016. New challenges in risk assessment of chemicals when simulating real exposure scenarios; simultaneous multi-chemicals’ low dose exposure. Food Chem Toxicol. 96:174–176.
  • Tsatsakis AM, Kouretas D, Tzatzarakis MN, Stivaktakis P, Tsarouhas K, Golokhvast KS, Rakitskii VN, Tutelyan VA, Hernandez AF, Rezaee R, et al. 2017. Simulating real-life exposures to uncover possible risks to human health: A proposed consensus for a novel methodological approach. Hum Exp Toxicol. 36(6):554–564.
  • Tseng IL, Yang YF, Yu CW, Li WH, Liao V. 2013. Phthalates induce neurotoxicity affecting locomotor and thermotactic behaviors and AFD neurons through oxidative stress in Caenorhabditis elegans. PLoS One. 8(12):e82657.
  • van der Merwe J, van der Veeken L, Ferraris S, Gsell W, Himmelreich U, Toelen J, Ourselin S, Melbourne A, Vercauteren T, Deprest J, et al. 2019. Early neuropathological and neurobehavioral consequences of preterm birth in a rabbit model. Sci Rep. 9(1):11.
  • Vinceti M, Violi F, Tzatzarakis M, Mandrioli J, Malagoli C, Hatch EE, Fini N, Fasano A, Rakitskii VN, Kalantzi O-I, et al. 2017. Pesticides, polychlorinated biphenyls and polycyclic aromatic hydrocarbons in cerebrospinal fluid of amyotrophic lateral sclerosis patients: a case-control study. Environ Res. 155:261–267.
  • Vinken M. 2019. Omics-based input and output in the development and use of adverse outcome pathways. Curr Opin Toxicol. 18:8–12.
  • Vitalone A, Catalani A, Chiodi V, Cinque C, Fattori V, Goldoni M, Matteucci P, Poli D, Zuena AR, Costa LG, et al. 2008. Neurobehavioral assessment of rats exposed to low doses of PCB126 and methyl mercury during development. Environ Toxicol Pharmacol. 25(1):103–113.
  • Vodovotz Y, Csete M, Bartels J, Chang S, An G. 2008. Translational systems biology of inflammation. PLoS Comput Biol. 4(4):e1000014.
  • Vuong AM, Yolton K, Wang Z, Xie C, Webster GM, Ye X, Calafat AM, Braun JM, Dietrich KN, Lanphear BP, et al. 2018. Childhood perfluoroalkyl substance exposure and executive function in children at 8 years. Environ Int. 119:212–219.
  • Wang Q, Lai NL-S, Wang X, Guo Y, Lam PK-S, Lam JC-W, Zhou B. 2015. Bioconcentration and transfer of the organophorous flame retardant 1,3-dichloro-2-propyl phosphate causes thyroid endocrine disruption and developmental neurotoxicity in zebrafish larvae. Environ Sci Technol. 49(8):5123–5132.
  • Warita K, Mitsuhashi T, Ohta K-i, Suzuki S, Hoshi N, Miki T, Takeuchi Y. 2013. In vitro evaluation of gene expression changes for gonadotropin-releasing hormone 1, brain-derived neurotrophic factor and neurotrophic tyrosine kinase, receptor, type 2, in response to bisphenol A treatment. Congenit Anom (Kyoto). 53(1):42–45.
  • Weiss B. 2000. Vulnerability of children and the developing brain to neurotoxic hazards. Environ Health Perspect. 108:375–381.
  • Westerink R. 2006. Targeting exocytosis: ins and outs of the modulation of quantal dopamine release. CNSNDDT. 5(1):57–77.
  • Wilson MS, Graham JR, Ball AJ. 2014. Multiparametric High Content Analysis for assessment of neurotoxicity in differentiated neuronal cell lines and human embryonic stem cell-derived neurons. Neurotoxicology. 42:33–48.
  • Wójtowicz AK, Sitarz-Głownia AM, Szczęsna M, Szychowski KA. 2019. The action of Di-(2-Ethylhexyl) phthalate (DEHP) in mouse cerebral cells involves an impairment in aryl hydrocarbon receptor (AhR) signaling. Neurotox Res. 35(1):183–195.
  • Wu X, Majumder A, Webb R, Stice SL. 2016. High content imaging quantification of multiple in vitro human neurogenesis events after neurotoxin exposure. BMC Pharmacol Toxicol. 17(1):1–15.
  • Wu Y, Li K, Zuo H, Yuan Y, Sun Y, Yang X. 2014. Primary neuronal-astrocytic co-culture platform for neurotoxicity assessment of di-(2-ethylhexyl) phthalate. J Environ Sci (China). 26(5):1145–1153.
  • Xu X, Lu Y, Zhang G, Chen L, Tian D, Shen X, Yang Y, Dong F. 2014. Bisphenol A promotes dendritic morphogenesis of hippocampal neurons through estrogen receptor-mediated ERK1/2 signal pathway. Chemosphere. 96:129–137.
  • Yang D, Lein PJ. 2010. Polychlorinated biphenyls increase apoptosis in the developing rat brain. Curr Neurobiol. 1(1):70–76.
  • Yang W, Zhao F, Fang Y, Li L, Li C, Ta N. 2018. 1H-nuclear magnetic resonance metabolomics revealing the intrinsic relationships between neurochemical alterations and neurobehavioral and neuropathological abnormalities in rats exposed to tris(2-chloroethyl)phosphate. Chemosphere. 200:649–659.
  • Yin N, Liang S, Liang S, Yang R, Hu B, Qin Z, Liu A, Faiola F. 2018a. TBBPA and its alternatives disturb the early stages of neural development by interfering with the NOTCH and WNT pathways. Environ Sci Technol. 52(9):5459–5468.
  • Yin N, Yang R, Liang S, Liang S, Hu B, Ruan T, Faiola F. 2018b. Evaluation of the early developmental neural toxicity of F-53B, as compared to PFOS, with an in vitro mouse stem cell differentiation model. Chemosphere. 204:109–118.
  • Yin N, Yao X, Qin Z, Wang YL, Faiola F. 2015. Assessment of Bisphenol A (BPA) neurotoxicity in vitro with mouse embryonic stem cells. J Environ Sci (China). 36:181–187.
  • Yoon M, Campbell JL, Andersen ME, Clewell HJ. 2012. Quantitative in vitro to in vivo extrapolation of cell-based toxicity assay results. Crit Rev Toxicol. 42(8):633–652.
  • Zhang D, Zhou S, Lu X, Jin M, Zhang Y, Zhao H. 2018. Neurological responses of embryo-larval zebrafish to short-term sediment exposure to decabromodiphenylethane底泥中的十溴二苯乙烷的短期暴露对斑马鱼胚胎和幼鱼神经毒性的研究. J Zhejiang Univ Sci B. 19(5):400–408.
  • Zhang Q, Liu W, Niu Q, Wang Y, Zhao H, Zhang H, Song J, Tsuda S, Saito N. 2016. Effects of perfluorooctane sulfonate and its alternatives on long-term potentiation in the hippocampus CA1 region of adult rats in vivo. Toxicol Res. 5(2):539–546.
  • Zhang Y, Wei L, Wang Y, Zhang Y, Wang L, Chang W. 2019. Neurotoxic effects of perfluoroalkyl acids:neurobehavioral deficit and its molecular mechanism. Toxicol Lett. 305:65–72.
  • Zhu B, Zhao G, Yang L, Zhou B. 2018. Tetrabromobisphenol A caused neurodevelopmental toxicity via disrupting thyroid hormones in zebrafish larvae. Chemosphere. 197:353–361.
  • Ziemińska E, Stafiej A, Toczyłowska B, Łazarewicz JW. 2012. Synergistic neurotoxicity of oxygen-glucose deprivation and tetrabromobisphenol A in vitro: role of oxidative stress. Pharmacol Reports. 64(5):1166–1178.

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