Revealing the Increased Stress Response Behavior through Transcriptomic Analysis of Adult Zebrafish Brain after Chronic Low to Moderate Dose Rates of Ionizing Radiation

High levels of ionizing radiation (IR) are known to induce neurogenesis defects with harmful consequences on brain morphogenesis and cognitive functions, but the effects of chronic low to moderate dose rates of IR remain largely unknown. In this study, we aim at defining the main molecular pathways...

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Main Authors: Elsa Cantabella, Virginie Camilleri, Isabelle Cavalie, Nicolas Dubourg, Béatrice Gagnaire, Thierry D. Charlier, Christelle Adam-Guillermin, Xavier Cousin, Oliver Armant
Format: Article
Language:English
Published: MDPI AG 2022-08-01
Series:Cancers
Subjects:
Online Access:https://www.mdpi.com/2072-6694/14/15/3793
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author Elsa Cantabella
Virginie Camilleri
Isabelle Cavalie
Nicolas Dubourg
Béatrice Gagnaire
Thierry D. Charlier
Christelle Adam-Guillermin
Xavier Cousin
Oliver Armant
author_facet Elsa Cantabella
Virginie Camilleri
Isabelle Cavalie
Nicolas Dubourg
Béatrice Gagnaire
Thierry D. Charlier
Christelle Adam-Guillermin
Xavier Cousin
Oliver Armant
author_sort Elsa Cantabella
collection DOAJ
description High levels of ionizing radiation (IR) are known to induce neurogenesis defects with harmful consequences on brain morphogenesis and cognitive functions, but the effects of chronic low to moderate dose rates of IR remain largely unknown. In this study, we aim at defining the main molecular pathways impacted by IR and how these effects can translate to higher organizational levels such as behavior. Adult zebrafish were exposed to gamma radiation for 36 days at 0.05 mGy/h, 0.5 mGy/h and 5 mGy/h. RNA sequencing was performed on the telencephalon and completed by RNA in situ hybridization that confirmed the upregulation of oxytocin and cone rod homeobox in the parvocellular preoptic nucleus. A dose rate-dependent increase in differentially expressed genes (DEG) was observed with 27 DEG at 0.05 mGy/h, 200 DEG at 0.5 mGy/h and 530 DEG at 5 mGy/h. Genes involved in neurotransmission, neurohormones and hypothalamic-pituitary-interrenal axis functions were specifically affected, strongly suggesting their involvement in the stress response behavior observed after exposure to dose rates superior or equal to 0.5 mGy/h. At the individual scale, hypolocomotion, increased freezing and social stress were detected. Together, these data highlight the intricate interaction between neurohormones (and particularly oxytocin), neurotransmission and neurogenesis in response to chronic exposure to IR and the establishment of anxiety-like behavior.
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spelling doaj.art-8678784b1d3942ccb41c1dcc77f368a72023-12-03T12:31:27ZengMDPI AGCancers2072-66942022-08-011415379310.3390/cancers14153793Revealing the Increased Stress Response Behavior through Transcriptomic Analysis of Adult Zebrafish Brain after Chronic Low to Moderate Dose Rates of Ionizing RadiationElsa Cantabella0Virginie Camilleri1Isabelle Cavalie2Nicolas Dubourg3Béatrice Gagnaire4Thierry D. Charlier5Christelle Adam-Guillermin6Xavier Cousin7Oliver Armant8Institut de Radioprotection et de Sûreté Nucléaire (IRSN), Pôle Santé Environnement-Environnement (PSE-ENV)/Service de Recherche sur les Transferts et les Effets des Radionucléides sur les Ecosystèmes (SRTE)/Laboratoire de Recherche sur les Effets des Radionucléides sur les Ecosystèmes (LECO), Cadarache, 13115 Saint-Paul-lez-Durance, FranceInstitut de Radioprotection et de Sûreté Nucléaire (IRSN), Pôle Santé Environnement-Environnement (PSE-ENV)/Service de Recherche sur les Transferts et les Effets des Radionucléides sur les Ecosystèmes (SRTE)/Laboratoire de Recherche sur les Effets des Radionucléides sur les Ecosystèmes (LECO), Cadarache, 13115 Saint-Paul-lez-Durance, FranceInstitut de Radioprotection et de Sûreté Nucléaire (IRSN), Pôle Santé Environnement-Environnement (PSE-ENV)/Service de Recherche sur les Transferts et les Effets des Radionucléides sur les Ecosystèmes (SRTE)/Laboratoire de Recherche sur les Effets des Radionucléides sur les Ecosystèmes (LECO), Cadarache, 13115 Saint-Paul-lez-Durance, FranceInstitut de Radioprotection et de Sûreté Nucléaire (IRSN), Pôle Santé Environnement-Environnement (PSE-ENV)/Service de Recherche sur les Transferts et les Effets des Radionucléides sur les Ecosystèmes (SRTE)/Laboratoire de Recherche sur les Effets des Radionucléides sur les Ecosystèmes (LECO), Cadarache, 13115 Saint-Paul-lez-Durance, FranceInstitut de Radioprotection et de Sûreté Nucléaire (IRSN), Pôle Santé Environnement-Environnement (PSE-ENV)/Service de Recherche sur les Transferts et les Effets des Radionucléides sur les Ecosystèmes (SRTE)/Laboratoire de Recherche sur les Effets des Radionucléides sur les Ecosystèmes (LECO), Cadarache, 13115 Saint-Paul-lez-Durance, FranceUniv. Rennes, Inserm, EHESP, Irset (Institut de Recherche en Santé, Environnement et Travail), UMR_S 1085, 35000 Rennes, FranceInstitut de Radioprotection et de Sûreté Nucléaire (IRSN), Pôle Santé Environnement-Santé (PSE-Santé)/Service de Recherche en Dosimétrie (SDOS)/Laboratoire de Micro-Irradiation, de Métrologie et de Dosimétrie des Neutrons (LMDN), Cadarache, 13115 Saint-Paul-lez-Durance, FranceMARBEC, Univ. Montpellier, CNRS, Ifremer, IRD, INRAE, 34250 Palavas Les Flots, FranceInstitut de Radioprotection et de Sûreté Nucléaire (IRSN), Pôle Santé Environnement-Environnement (PSE-ENV)/Service de Recherche sur les Transferts et les Effets des Radionucléides sur les Ecosystèmes (SRTE)/Laboratoire de Recherche sur les Effets des Radionucléides sur les Ecosystèmes (LECO), Cadarache, 13115 Saint-Paul-lez-Durance, FranceHigh levels of ionizing radiation (IR) are known to induce neurogenesis defects with harmful consequences on brain morphogenesis and cognitive functions, but the effects of chronic low to moderate dose rates of IR remain largely unknown. In this study, we aim at defining the main molecular pathways impacted by IR and how these effects can translate to higher organizational levels such as behavior. Adult zebrafish were exposed to gamma radiation for 36 days at 0.05 mGy/h, 0.5 mGy/h and 5 mGy/h. RNA sequencing was performed on the telencephalon and completed by RNA in situ hybridization that confirmed the upregulation of oxytocin and cone rod homeobox in the parvocellular preoptic nucleus. A dose rate-dependent increase in differentially expressed genes (DEG) was observed with 27 DEG at 0.05 mGy/h, 200 DEG at 0.5 mGy/h and 530 DEG at 5 mGy/h. Genes involved in neurotransmission, neurohormones and hypothalamic-pituitary-interrenal axis functions were specifically affected, strongly suggesting their involvement in the stress response behavior observed after exposure to dose rates superior or equal to 0.5 mGy/h. At the individual scale, hypolocomotion, increased freezing and social stress were detected. Together, these data highlight the intricate interaction between neurohormones (and particularly oxytocin), neurotransmission and neurogenesis in response to chronic exposure to IR and the establishment of anxiety-like behavior.https://www.mdpi.com/2072-6694/14/15/3793gamma irradiationteleostanxiety-like behaviorsociabilityneurotransmitter systemneurohormone
spellingShingle Elsa Cantabella
Virginie Camilleri
Isabelle Cavalie
Nicolas Dubourg
Béatrice Gagnaire
Thierry D. Charlier
Christelle Adam-Guillermin
Xavier Cousin
Oliver Armant
Revealing the Increased Stress Response Behavior through Transcriptomic Analysis of Adult Zebrafish Brain after Chronic Low to Moderate Dose Rates of Ionizing Radiation
Cancers
gamma irradiation
teleost
anxiety-like behavior
sociability
neurotransmitter system
neurohormone
title Revealing the Increased Stress Response Behavior through Transcriptomic Analysis of Adult Zebrafish Brain after Chronic Low to Moderate Dose Rates of Ionizing Radiation
title_full Revealing the Increased Stress Response Behavior through Transcriptomic Analysis of Adult Zebrafish Brain after Chronic Low to Moderate Dose Rates of Ionizing Radiation
title_fullStr Revealing the Increased Stress Response Behavior through Transcriptomic Analysis of Adult Zebrafish Brain after Chronic Low to Moderate Dose Rates of Ionizing Radiation
title_full_unstemmed Revealing the Increased Stress Response Behavior through Transcriptomic Analysis of Adult Zebrafish Brain after Chronic Low to Moderate Dose Rates of Ionizing Radiation
title_short Revealing the Increased Stress Response Behavior through Transcriptomic Analysis of Adult Zebrafish Brain after Chronic Low to Moderate Dose Rates of Ionizing Radiation
title_sort revealing the increased stress response behavior through transcriptomic analysis of adult zebrafish brain after chronic low to moderate dose rates of ionizing radiation
topic gamma irradiation
teleost
anxiety-like behavior
sociability
neurotransmitter system
neurohormone
url https://www.mdpi.com/2072-6694/14/15/3793
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