Adverse developmental impacts in progeny of zebrafish exposed to the agricultural herbicide atrazine during embryogenesis

Atrazine (ATZ) is an herbicide commonly used on crops in the Midwestern US and other select global regions. The US Environmental Protection Agency ATZ regulatory limit is 3 parts per billion (ppb; µg/L), but this limit is often exceeded. ATZ has a long half-life, is a common contaminant of drinking...

Full description

Bibliographic Details
Main Authors: Janiel K. Ahkin Chin Tai, Katharine A. Horzmann, Thomas L. Jenkins, Isabelle N. Akoro, Sydney Stradtman, Uma K. Aryal, Jennifer L. Freeman
Format: Article
Language:English
Published: Elsevier 2023-10-01
Series:Environment International
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S0160412023004865
_version_ 1827793789426597888
author Janiel K. Ahkin Chin Tai
Katharine A. Horzmann
Thomas L. Jenkins
Isabelle N. Akoro
Sydney Stradtman
Uma K. Aryal
Jennifer L. Freeman
author_facet Janiel K. Ahkin Chin Tai
Katharine A. Horzmann
Thomas L. Jenkins
Isabelle N. Akoro
Sydney Stradtman
Uma K. Aryal
Jennifer L. Freeman
author_sort Janiel K. Ahkin Chin Tai
collection DOAJ
description Atrazine (ATZ) is an herbicide commonly used on crops in the Midwestern US and other select global regions. The US Environmental Protection Agency ATZ regulatory limit is 3 parts per billion (ppb; µg/L), but this limit is often exceeded. ATZ has a long half-life, is a common contaminant of drinking water sources, and is indicated as an endocrine disrupting chemical in multiple species. The zebrafish was used to test the hypothesis that an embryonic parental ATZ exposure alters protein levels leading to modifications in morphology and behavior in developing progeny. Zebrafish embryos (F1) were collected from adults (F0) exposed to 0, 0.3, 3, or 30 ppb ATZ during embryogenesis. Differential proteomics, morphology, and behavior assays were completed with offspring aged 120 or 144 h with no additional chemical treatment. Proteomic analysis identified differential expression of proteins associated with neurological development and disease; and organ and organismal morphology, development, and injury, specifically the skeletomuscular system. Head length and ratio of head length to total length was significantly increased in the F1 of 0.3 and 30 ppb ATZ groups (p < 0.05). Based on molecular pathway alterations, further craniofacial morphology assessment found decreased distance for cartilaginous structures, decreased surface area and distance between saccular otoliths, and a more posteriorly positioned notochord (p < 0.05), indicating delayed ossification and skeletal growth. The visual motor response assay showed hyperactivity in progeny of the 30 ppb treatment group for distance moved and of the 0.3 and 30 ppb treatment groups for time spent moving (p < 0.05). Due to the changes in saccular otoliths, an acoustic startle assay was completed and showed decreased response in the 0.3 and 30 ppb treatments (p < 0.05). These findings suggest that a single embryonic parental exposure alters cellular pathways in their progeny that lead to perturbations in craniofacial development and behavior.
first_indexed 2024-03-11T18:23:35Z
format Article
id doaj.art-f90ccd2e6faa48aaa6ade370ed0ad9c4
institution Directory Open Access Journal
issn 0160-4120
language English
last_indexed 2024-03-11T18:23:35Z
publishDate 2023-10-01
publisher Elsevier
record_format Article
series Environment International
spelling doaj.art-f90ccd2e6faa48aaa6ade370ed0ad9c42023-10-15T04:36:29ZengElsevierEnvironment International0160-41202023-10-01180108213Adverse developmental impacts in progeny of zebrafish exposed to the agricultural herbicide atrazine during embryogenesisJaniel K. Ahkin Chin Tai0Katharine A. Horzmann1Thomas L. Jenkins2Isabelle N. Akoro3Sydney Stradtman4Uma K. Aryal5Jennifer L. Freeman6School of Health Sciences, Purdue University, West Lafayette, IN, USASchool of Health Sciences, Purdue University, West Lafayette, IN, USA; Department of Pathobiology, Auburn University, Auburn, AL, USAWeldon School of Biomedical Engineering, Purdue University, West Lafayette, IN, USASchool of Health Sciences, Purdue University, West Lafayette, IN, USASchool of Health Sciences, Purdue University, West Lafayette, IN, USADepartment of Comparative Pathobiology, Purdue University, West Lafayette, IN, USA; Bindley Bioscience Center, Discovery Park, Purdue University, West Lafayette, IN, USASchool of Health Sciences, Purdue University, West Lafayette, IN, USA; Corresponding author at: School of Health Sciences, 550 Stadium Mall Drive, West Lafayette, IN 47907, USA.Atrazine (ATZ) is an herbicide commonly used on crops in the Midwestern US and other select global regions. The US Environmental Protection Agency ATZ regulatory limit is 3 parts per billion (ppb; µg/L), but this limit is often exceeded. ATZ has a long half-life, is a common contaminant of drinking water sources, and is indicated as an endocrine disrupting chemical in multiple species. The zebrafish was used to test the hypothesis that an embryonic parental ATZ exposure alters protein levels leading to modifications in morphology and behavior in developing progeny. Zebrafish embryos (F1) were collected from adults (F0) exposed to 0, 0.3, 3, or 30 ppb ATZ during embryogenesis. Differential proteomics, morphology, and behavior assays were completed with offspring aged 120 or 144 h with no additional chemical treatment. Proteomic analysis identified differential expression of proteins associated with neurological development and disease; and organ and organismal morphology, development, and injury, specifically the skeletomuscular system. Head length and ratio of head length to total length was significantly increased in the F1 of 0.3 and 30 ppb ATZ groups (p < 0.05). Based on molecular pathway alterations, further craniofacial morphology assessment found decreased distance for cartilaginous structures, decreased surface area and distance between saccular otoliths, and a more posteriorly positioned notochord (p < 0.05), indicating delayed ossification and skeletal growth. The visual motor response assay showed hyperactivity in progeny of the 30 ppb treatment group for distance moved and of the 0.3 and 30 ppb treatment groups for time spent moving (p < 0.05). Due to the changes in saccular otoliths, an acoustic startle assay was completed and showed decreased response in the 0.3 and 30 ppb treatments (p < 0.05). These findings suggest that a single embryonic parental exposure alters cellular pathways in their progeny that lead to perturbations in craniofacial development and behavior.http://www.sciencedirect.com/science/article/pii/S0160412023004865AtrazineBehaviorMultigenerationProteomicsSkeletalZebrafish
spellingShingle Janiel K. Ahkin Chin Tai
Katharine A. Horzmann
Thomas L. Jenkins
Isabelle N. Akoro
Sydney Stradtman
Uma K. Aryal
Jennifer L. Freeman
Adverse developmental impacts in progeny of zebrafish exposed to the agricultural herbicide atrazine during embryogenesis
Environment International
Atrazine
Behavior
Multigeneration
Proteomics
Skeletal
Zebrafish
title Adverse developmental impacts in progeny of zebrafish exposed to the agricultural herbicide atrazine during embryogenesis
title_full Adverse developmental impacts in progeny of zebrafish exposed to the agricultural herbicide atrazine during embryogenesis
title_fullStr Adverse developmental impacts in progeny of zebrafish exposed to the agricultural herbicide atrazine during embryogenesis
title_full_unstemmed Adverse developmental impacts in progeny of zebrafish exposed to the agricultural herbicide atrazine during embryogenesis
title_short Adverse developmental impacts in progeny of zebrafish exposed to the agricultural herbicide atrazine during embryogenesis
title_sort adverse developmental impacts in progeny of zebrafish exposed to the agricultural herbicide atrazine during embryogenesis
topic Atrazine
Behavior
Multigeneration
Proteomics
Skeletal
Zebrafish
url http://www.sciencedirect.com/science/article/pii/S0160412023004865
work_keys_str_mv AT janielkahkinchintai adversedevelopmentalimpactsinprogenyofzebrafishexposedtotheagriculturalherbicideatrazineduringembryogenesis
AT katharineahorzmann adversedevelopmentalimpactsinprogenyofzebrafishexposedtotheagriculturalherbicideatrazineduringembryogenesis
AT thomasljenkins adversedevelopmentalimpactsinprogenyofzebrafishexposedtotheagriculturalherbicideatrazineduringembryogenesis
AT isabellenakoro adversedevelopmentalimpactsinprogenyofzebrafishexposedtotheagriculturalherbicideatrazineduringembryogenesis
AT sydneystradtman adversedevelopmentalimpactsinprogenyofzebrafishexposedtotheagriculturalherbicideatrazineduringembryogenesis
AT umakaryal adversedevelopmentalimpactsinprogenyofzebrafishexposedtotheagriculturalherbicideatrazineduringembryogenesis
AT jenniferlfreeman adversedevelopmentalimpactsinprogenyofzebrafishexposedtotheagriculturalherbicideatrazineduringembryogenesis