Abstract
In this study, we examined the dose-dependent effects of an environmentally relevant pesticide cocktail (metalachlor, linuron, isoproturon, tebucanazole, aclonifen, atrazine, pendimethalin, and azinphos-methyl) and temperature change (22 vs. 32 °C for 4-week exposure) on Na+/K+-ATPase, 3-nitrotyrosine protein (NTP), dinitrophenyl protein (DNP), catalase (CAT), and superoxide dismutase (SOD) expressions in gills of goldfish (Carassius auratus). Histopathological analysis showed widespread damage to gill in elevated temperature (32 °C) and pesticide co-exposure groups, including fusion of secondary lamellae, club-shaped primary lamellae, rupture of epithelial layer, loss of normal architecture, and hemorrhaging. Immunohistochemical and qRT-PCR analyses showed significant decreases in Na+/K+-ATPase protein and mRNA expressions in gills exposed to higher temperature and pesticides; however, combined exposure to heat and pesticides significantly increases NTP, DNP, CAT, and SOD expressions. In situ TUNEL assay revealed elevated levels of apoptotic cells in response to combined exposure. Collectively, our results suggest the combined effects of heat and pesticide stress cause cellular damage, upregulate oxidative/nitrative stress biomarkers, and increase apoptotic cells, downregulate Na+/K+-ATPase expression in gills. This provides new evidence for oxidant/antioxidant-dependent mechanisms for downregulation of Na+/K+-ATPase expression in gills during combined exposure.
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Data availability
All the data generated and analyzed during this study are included in this manuscript and available from the corresponding author upon request.
Abbreviations
- Na+/K+-ATPase:
-
Sodium-potassium ATPase
- NTP:
-
3-Nitrotyrosine protein
- DNP:
-
Dinitrophenyl protein
- CAT:
-
Catalase
- SOD:
-
Superoxide dismutase
- GPx:
-
Glutathione peroxidase
- GST:
-
Glutathione S-transferase
- GR:
-
Glutathione reductase
- 2,4-D:
-
2,4-Dichlorophenoxyacetic acid
- p,p’-DDE:
-
Dichlorodiphenyldichloroethylene
- DDT:
-
Dichlorodiphenyltrichloroethane
- BSA:
-
Bovine serum albumin
- PBS:
-
Phosphate-buffered saline
- qRT-PCR:
-
Quantitative real-time PCR
- TUNEL:
-
Terminal deoxynucleotidyl transferase dUTP nick labeling
- rTdT:
-
Recombinant terminal deoxynucleotidyl transferase
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Acknowledgements
The authors are grateful to Leinady Estrada, Michelle Rivera, Brandon Escareno, and Esmirna Cantu for their valuable input on the revision of the manuscript. We would also like to thank Dr. Aubrey Converse, University of Texas Marine Science Institute and Andrew Lawler, Division of Research, Graduate Studies and New Program Development, University of Texas Rio Grande Valley (UTRGV) for critically reviewing and editing the manuscript.
Funding
This study was funded in part by the start-up fund and University of Texas Rio Grande Valley (UTRGV) College of Science SEED grant (grant no. 210000371) to Md Saydur Rahman, and the UTRGV Presidential Graduate Research Assistant (PGRA) to Brittney Lacy.
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Md Saydur Rahman gave the research idea and supervised research. Brittney Lacy conducted laboratory studies and collected data. Brittney Lacy and Md Saydur Rahman analyzed data. Md Sadequr Rahman helped laboratory sampling and histological and immunohistochemical analyses. Md Saydur Rahman and Brittney Lacy designed the figures. Brittney Lacy drafted manuscript. Brittney Lacy, Md Sadequr Rahman, and Md Saydur Rahman editing and reviewing the manuscript.
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All animal husbandry practices and the following laboratory experimental procedures were approved by the UTRGV Institutional Animal Care and Use Committee (IACUC, protocol# 19–04) and by UTRGV’s consulting veterinarian.
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Lacy, B., Rahman, M.S. & Rahman, M.S. Potential mechanisms of Na+/K+-ATPase attenuation by heat and pesticides co-exposure in goldfish: role of cellular apoptosis, oxidative/nitrative stress, and antioxidants in gills. Environ Sci Pollut Res 29, 57376–57394 (2022). https://doi.org/10.1007/s11356-022-19779-7
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DOI: https://doi.org/10.1007/s11356-022-19779-7