https://doi.org/10.4081/ejh.2021.3282
Benzo[a]pyrene impairs the migratory pattern of human gonadotropin-releasing-hormone-secreting neuroblasts
Submitted: 31 May 2021
Accepted: 27 July 2021
Published: 13 August 2021
Accepted: 27 July 2021
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All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.
Authors
Benzo[a]pyrene (BaP) is a widespread pollutant that can act as an endocrine disrupting compound (EDC) and interferes with reproductive function. The central regulatory network of the reproductive system is mediated by gonadotropin-releasing hormone (GnRH) neurons, which originate in the olfactory placode and, during ontogenesis, migrate into the hypothalamus. Given the importance of the migratory process for GnRH neuron maturation, we investigated the effect of BaP (10 µM for 24 h) on GnRH neuroblasts isolated from the human fetal olfactory epithelium (FNCB4). BaP exposure significantly reduced the mRNA level of genes implicated in FNCB4 cell migration and affected their migratory ability. Our findings demonstrate that BaP may interfere with the central neuronal network controlling human reproduction affecting GnRH neuron maturation.
Casoni F, Malone SA, Belle M, Luzzati F, Collier F, Allet C, et al. Development of the neurons controlling fertility in humans: new insights from 3D imaging and transparent fetal brains. Development 2016;143:3969–81.
DOI: https://doi.org/10.1242/dev.139444
Sisk CL, Foster DL. The neural basis of puberty and adolescence. Nat Neurosci 2004;7:1040–7.
DOI: https://doi.org/10.1038/nn1326
Frye C, Bo E, Calamandrei G, Calzà L, Dessì-Fulgheri F, Fernández M, et al. Endocrine disrupters: A review of some sources, effects, and mechanisms of actions on behaviour and neuroendocrine systems: EDCs-sources, effects & mechanisms. J Neuroendocrinol 2012;24:144–59.
DOI: https://doi.org/10.1111/j.1365-2826.2011.02229.x
Street M, Angelini S, Bernasconi S, Burgio E, Cassio A, Catellani C, et al. Current Knowledge on endocrine disrupting chemicals (EDCs) from animal biology to humans, from pregnancy to adulthood: Highlights from a National Italian Meeting. Int J Mol Sci 2018;19:1647.
DOI: https://doi.org/10.3390/ijms19061647
Guerreiro CBB, Horálek J, de Leeuw F, Couvidat F. Benzo(a)pyrene in Europe: Ambient air concentrations, population exposure and health effects. Environ Pollut 2016;214:657–67.
DOI: https://doi.org/10.1016/j.envpol.2016.04.081
Plunk EC, Richards SM. Endocrine-disrupting air pollutants and their effects on the hypothalamus-pituitary-gonadal axis. Int J Mol Sci 2020;21:9191.
DOI: https://doi.org/10.3390/ijms21239191
McCabe DP, Flynn EJ. Deposition of low dose benzo(a)pyrene into fetal tissue: Influence of protein binding. Teratology 1990;41:85–95.
DOI: https://doi.org/10.1002/tera.1420410109
Lopez-Rodriguez D, Franssen D, Bakker J, Lomniczi A, Parent A-S. Cellular and molecular features of EDC exposure: consequences for the GnRH network. Nat Rev Endocrinol 2021;17:83-96.
DOI: https://doi.org/10.1038/s41574-020-00436-3
Vannelli G, Ensoli F, Zonefrati R, Kubota Y, Arcangeli A, Becchetti A, et al. Neuroblast long-term cell cultures from human fetal olfactory epithelium respond to odors. J Neurosci 1995;15:4382–94.
DOI: https://doi.org/10.1523/JNEUROSCI.15-06-04382.1995
Romanelli RG, Barni T, Maggi M, Luconi M, Failli P, Pezzatini A, et al. Expression and function of gonadotropin-releasing hormone (GnRH) receptor in human olfactory GnRH-secreting neurons: an autocrine GnRH loop underlies neuronal migration. J Biol Chem 2004;279:117–26.
DOI: https://doi.org/10.1074/jbc.M307955200
Maggi M, Barni T, Fantoni G, Mancina R, Pupilli C, Luconi M, et al. Expression and biological effects of endothelin-1 in human gonadotropin-releasing hormone-secreting neurons. J Clin Endocrinol Metab 2000;85:8.
DOI: https://doi.org/10.1210/jc.85.4.1658
Sarma SN, Blais JM, Chan HM. Neurotoxicity of alkylated polycyclic aromatic compounds in human neuroblastoma cells. J Toxicol Environ Health A 2017;80:285–300.
DOI: https://doi.org/10.1080/15287394.2017.1314840
Slotkin TA, Skavicus S, Card J, Giulio RTD, Seidler FJ. In vitro models reveal differences in the developmental neurotoxicity of an environmental polycylic aromatic hydrocarbon mixture compared to benzo[a]pyrene: Neuronotypic PC12 Cells and embryonic neural stem cells. Toxicology 2017;377:49–56.
DOI: https://doi.org/10.1016/j.tox.2016.12.008
Sarchielli E, Morelli A, Guarnieri G, Iorizzi M, Sgambati E. Neuroprotective effects of quercetin 4’- O -β- d -diglucoside on human striatal precursor cells in nutrient deprivation condition. Acta Histochem 2018;120:122–8.
DOI: https://doi.org/10.1016/j.acthis.2018.01.003
Guarnieri G, Sarchielli E, Comeglio P, Herrera-Puerta E, Piaceri I, Nacmias B, et al. Tumor necrosis factor α influences phenotypic plasticity and promotes epigenetic changes in human basal fore brain cholinergic neuroblasts. Int J Mol Sci 2020;21:6128.
DOI: https://doi.org/10.3390/ijms21176128
Sarchielli E, Guarnieri G, Idrizaj E, Squecco R, Mello T, Comeglio P, et al. The G protein‐coupled oestrogen receptor, GPER1, mediates direct anti‐inflammatory effects of oestrogens in human cholinergic neurones from the nucleus basalis of Meynert. J Neuroendocrinol 2020;32:e12837.
Sarchielli E, Comeglio P, Squecco R, Ballerini L, Mello T, Guarnieri G, et al. Tumor necrosis factor α impairs kisspeptin signaling in human gonadotropin-releasing hormone primary neurons. J Clin Endocrinol Metab 2017;102:45-56.
Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 2001;25:402–8.
DOI: https://doi.org/10.1006/meth.2001.1262
Morelli A, Comeglio P, Sarchielli E, Cellai I, Vignozzi L, Vannelli GB, et al. Negative effects of high glucose exposure in human gonadotropin-releasing hormone neurons. Int J Endocrinol 2013;2013:1–8.
DOI: https://doi.org/10.1155/2013/684659
Romanelli RG, Barni T, Maggi M, Luconi M, Failli P, Pezzatini A, et al. Role of endothelin-1 in the migration of human olfactory gonadotropin-releasing hormone-secreting neuroblasts. Endocrinology 2005;146:4321-30.
DOI: https://doi.org/10.1210/en.2005-0060
Gelboin HV. Benzo[alpha]pyrene metabolism, activation and carcinogenesis: role and regulation of mixed-function oxidases and related enzymes. Physiol Rev 1980;60:1107-66.
DOI: https://doi.org/10.1152/physrev.1980.60.4.1107
Bai Y, Chang F, Zhou R, Jin P-P, Matsumoto H, Sokabe M, et al. Increase of anteroventral periventricular kisspeptin neurons and generation of E2-induced LH-surge system in male rats exposed perinatally to environmental dose of bisphenol-A. Endocrinology 2011;152:1562–71.
DOI: https://doi.org/10.1210/en.2010-1042
Pillon D, Cadiou V, Angulo L, Duittoz AH. Maternal exposure to 17-alpha-ethinylestradiol alters embryonic development of GnRH-1 neurons in mouse. Brain Res 2012;1433:29-37.
DOI: https://doi.org/10.1016/j.brainres.2011.11.030
Uppstad H, Øvrebø S, Haugen A, Mollerup S. Importance of CYP1A1 and CYP1B1 in bioactivation of benzo[a]pyrene in human lung cell lines. Toxicol Lett 2010;192:221–8.
DOI: https://doi.org/10.1016/j.toxlet.2009.10.025
Kuban W, Daniel WA. Cytochrome P450 expression and regulation in the brain. Drug Metab Rev 2021;53:1-29.
DOI: https://doi.org/10.1080/03602532.2020.1858856
Morse DC, Stein AP, Thomas PE, Lowndes HE. Distribution and induction of cytochrome P450 1A1 and 1A2 in rat brain. Toxicol ApplPharmacol 1998;152:232–9.
DOI: https://doi.org/10.1006/taap.1998.8477
Rieder CR, Ramsden DB, Williams AC. Cytochrome P450 1B1 mRNA in the human central nervous system. Mol Pathol 1998;51:138-42.
DOI: https://doi.org/10.1136/mp.51.3.138
Hakkola J. Expression of CYP1B1 in human adult and fetal tissues and differential inducibility of CYP1B1 and CYP1A1 by Ah receptor ligands in human placenta and cultured cells. Carcinogenesis 1997;18:391-7.
DOI: https://doi.org/10.1093/carcin/18.2.391
Pitteloud N, Meysing A, Quinton R, Acierno JS, Dwyer AA, Plummer L, et al. Mutations in fibroblast growth factor receptor 1 cause Kallmann syndrome with a wide spectrum of reproductive phenotypes. Mol Cell Endocrinol 2006;254-255:60-9.
Cariboni A, Hickok J, Rakic S, Andrews W, Maggi R, Tischkau S, et al. Neuropilins and their ligands are important in the migration of gonadotropin-releasing hormone neurons. J Neurosci 2007;27:2387-95.
DOI: https://doi.org/10.1523/JNEUROSCI.5075-06.2007
Vidovic M, Chen M-M, Lu Q-Y, Kalloniatis KF, Martin BM, Tan AHY, et al. Deficiency in endothelin receptor B reduces proliferation of neuronal progenitors and increases apoptosis in postnatal rat cerebellum. Cell Mol Neurobiol 2008;28:1129-38.
DOI: https://doi.org/10.1007/s10571-008-9292-z
Ehrenreich H, Nau R, Dembowski C, Hasselblatt M, Barth M, Hahn A, et al. Endothelin B receptor deficiency is associated with an increased rate of neuronal apoptosis in the dentate gyrus. Neuroscience 1999;95:993-1001.
DOI: https://doi.org/10.1016/S0306-4522(99)00507-2
Clarke H, Dhillo WS, Jayasena CN. Comprehensive review on kisspeptin and its role in reproductive disorders. Endocrinol Metab 2015;30:124.
DOI: https://doi.org/10.3803/EnM.2015.30.2.124
Lee J-H, Welch DR. Suppression of metastasis in human breast carcinoma MDA-MB-435 cells after transfection with the metastasis suppressor gene, KiSS-i. Cancer Res 1997;57:2384-7.
Morelli A, Marini M, Mancina R, Luconi M, Vignozzi L, Fibbi B, et al. Sex steroids and leptin regulate the “first kiss” (KiSS 1/G-protein-coupled receptor 54 system) in human gonadotropin-releasing-hormone-secreting neuroblasts. J Sex Med 2008;5:1097-113.
DOI: https://doi.org/10.1111/j.1743-6109.2008.00782.x
How to Cite
Guarnieri, G., Becatti, M. ., Comeglio, P., Vignozzi, L., Maggi, M., Vannelli, G. B. ., & Morelli, A. (2021). Benzo[a]pyrene impairs the migratory pattern of human gonadotropin-releasing-hormone-secreting neuroblasts. European Journal of Histochemistry, 65(s1). https://doi.org/10.4081/ejh.2021.3282
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