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

Janiel K Ahkin Chin Tai; Katharine A Horzmann; Thomas L Jenkins; Isabelle N Akoro; Sydney Stradtman; Uma K Aryal; Jennifer L Freeman

doi:10.1016/j.envint.2023.108213

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

Environ Int. 2023 Oct:180:108213. doi: 10.1016/j.envint.2023.108213. Epub 2023 Sep 24.

Authors

Janiel K Ahkin Chin Tai¹, Katharine A Horzmann², Thomas L Jenkins³, Isabelle N Akoro¹, Sydney Stradtman¹, Uma K Aryal⁴, Jennifer L Freeman⁵

Affiliations

¹ School of Health Sciences, Purdue University, West Lafayette, IN, USA.
² School of Health Sciences, Purdue University, West Lafayette, IN, USA; Department of Pathobiology, Auburn University, Auburn, AL, USA.
³ Weldon School of Biomedical Engineering, Purdue University, West Lafayette, IN, USA.
⁴ Department of Comparative Pathobiology, Purdue University, West Lafayette, IN, USA; Bindley Bioscience Center, Discovery Park, Purdue University, West Lafayette, IN, USA.
⁵ School of Health Sciences, Purdue University, West Lafayette, IN, USA. Electronic address: jfreema@purdue.edu.

Abstract

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.

Keywords: Atrazine; Behavior; Multigeneration; Proteomics; Skeletal; Zebrafish.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

MeSH terms

Animals
Atrazine* / metabolism
Atrazine* / toxicity
Embryonic Development
Gene Expression Regulation, Developmental
Herbicides* / metabolism
Herbicides* / toxicity
Proteomics
Zebrafish / metabolism

Substances

Atrazine
Herbicides

Abstract

Publication types

MeSH terms

Substances

Grants and funding