Roundup® disrupts tissue architecture, attenuates Na+/K+-ATPase expression, and induces protein oxidation/nitration, cellular apoptosis, and antioxidant enzyme expressions in the gills of goldfish, Carassius auratus.

Extensive agricultural activities to feed the growing population are one major driving force behind aquatic pollution. Different types of pesticides are used in farmlands to increase crop production and wash up into water bodies. Glyphosate-based herbicide Roundup® is one of the most used pesticides in the United States; however, its effects on teleost species are still poorly understood. This study focused on the effects of environmentally relevant concentrations of Roundup exposure (low- and high-dose: 0.5 and 5 μg/L for 2-week) on Na+/K+-ATPase (NKA, a biomarker for sodium‑potassium ion pump efficacy), cytochrome P450-1A (CYP1A, a monooxygenase enzyme), 2,4-dinitrophenyl protein (DNP, a biomarker for protein oxidation), 3-nitrotyrosine protein (NTP, a biomarker for protein nitration), superoxidase dismutase (SOD, an antioxidant enzyme), catalase (CAT, an antioxidant enzyme) expressions, and cellular apoptosis in the gills of goldfish. Histopathological and in situ TUNEL analyses showed widespread tissue damage, including lamellar fusion, loss of gill architecture, club shape of primary lamellae, mucous formation, and distortion in the epithelium layer, as well as apoptotic nuclei in gills. Immunohistochemical and qRT-PCR analyses provided insights into the expressions of molecular indicators in gills. Fish exposed to Roundup exhibited a significant (P < 0.05) downregulation of NKA expression in gills. Additionally, we observed upregulation of CYP1A, DNP, NTP, SOD, and CAT expressions in the gills of goldfish. Overall, our results suggest that exposure to Roundup causes disruption of gill architecture, induces protein oxidation/nitration and cellular apoptosis, and alters prooxidant-antioxidant homeostasis in tissues, which may lead to reduced fitness and survivability of teleost species.

• Publication year

  2023

• Venue

  Comparative biochemistry and physiology. Toxicology & pharmacology : CBP

• Publication date

  2023-07-01

• Fields of study

  Biology, Medicine, Environmental Science

• Identifiers
  DOI 10.1016/j.cbpc.2023.109710PMID 37532112
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• Combined effects of high temperature and pesticide mixture exposure on free-swimming behaviors and hepatic cytochrome P450 1A expression in goldfish, Carassius auratus

  2023cited by this paper
• Effects of hypoxia and reoxygenation on gill remodeling, apoptosis, and oxidative stress in hypoxia-tolerant new variety blunt snout bream (Megalobrama amblycephala)

  2022cited by this paper
• Effects of the herbicide glyphosate on fish from embryos to adults: a review addressing behavior patterns and mechanisms behind them.

  2022cited by this paper
• 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

  2022cited by this paper
• The effects of low-toxic herbicide Roundup and glyphosate on mitochondria

  2022cited by this paper
• Glyphosate vs. Glyphosate-Based Herbicides Exposure: A Review on Their Toxicity

  2022cited by this paper
• Transient exposure to sublethal concentrations of a pesticide mixture (chlorpyrifos-difenoconazole) caused different responses in fish species from different trophic levels of the same community.

  2021cited by this paper
• Molecular Characterization and Expression of Cytochrome P450 Aromatase in Atlantic Croaker Brain: Regulation by Antioxidant Status and Nitric Oxide Synthase During Hypoxia Stress

  2021cited by this paper
• Acute exposition to Roundup Transorb® induces systemic oxidative stress and alterations in the expression of newly sequenced genes in silverside fish (Odontesthes humensis)

  2021cited by this paper
• Inflammatory, Oxidative Stress, and Apoptosis Effects in Zebrafish Larvae after Rapid Exposure to a Commercial Glyphosate Formulation

  2021cited by this paper
• Effects of chronic glyphosate exposure on antioxdative status, metabolism and immune response in tilapia (GIFT, Oreochromis niloticus).

  2020cited by this paper
• Glyphosate induces lymphocyte cell dysfunction and apoptosis via regulation of miR-203 targeting of PIK3R1 in common carp (Cyprinus carpio L.).

  2020cited by this paper
• Advancements in the Analytical Quantification of Nitroxidative Stress Biomarker 3-Nitrotyrosine in Biological Matrices

  2020cited by this paper
• Toxicological impacts of herbicide paraquat dichloride on histological profile (gills, liver, and kidney) of freshwater fish Channa punctatus (Bloch)

  2020cited by this paper
• Morphological and Immunohistochemical Modifications in Zebrafish (Danio rerio) Gills After Short-Term Exposure to the Fungicide Tebuconazole

  2019cited by this paper
• High temperature aggravates the effects of pesticides in goldfish.

  2019cited by this paper
• Developmental and epigenetic effects of Roundup and glyphosate exposure on Japanese medaka (Oryzias latipes).

  2019cited by this paper
• Insight into the confusion over surfactant co-formulants in glyphosate-based herbicides.

  2019cited by this paper
• Elevated temperature attenuates ovarian functions and induces apoptosis and oxidative stress in the American oyster, Crassostrea virginica: potential mechanisms and signaling pathways

  2019cited by this paper
• Glutathione reductase and catalase as potential biomarkers for synergistic intoxication of pesticides in fish

  2019cited by this paper
• ROS Generation and Antioxidant Defense Systems in Normal and Malignant Cells

  2019cited by this paper
• Influence of land use and region on glyphosate and aminomethylphosphonic acid in streams in the USA.

  2019cited by this paper
• Short‐term heat stress impairs testicular functions in the American oyster, Crassostrea virginica: Molecular mechanisms and induction of oxidative stress and apoptosis in spermatogenic cells

  2019cited by this paper
• Differential sensitivities to dioxin-like compounds PCB 126 and PeCDF between Tg(cyp1a:gfp) transgenic medaka and zebrafish larvae.

  2018cited by this paper
• The history and current status of glyphosate.

  2018cited by this paper
• Environmental pollution and toxic substances: Cellular apoptosis as a key parameter in a sensible model like fish.

  2018cited by this paper
• Goldfish: an old and new model system to study vertebrate development, evolution and human disease.

  2018cited by this paper
• Why goldfish? Merits and challenges in employing goldfish as a model organism in comparative endocrinology research.

  2017cited by this paper
• Effects of Copper on Hemocyte Apoptosis, ROS Production, and Gene Expression in White Shrimp Litopenaeus vannamei

  2017cited by this paper
• Reactive oxygen species and cancer paradox: To promote or to suppress?

  2017cited by this paper
• High temperature induces apoptosis and oxidative stress in pufferfish (Takifugu obscurus) blood cells.

  2015cited by this paper
• Hepatotoxicity of herbicide Sencor in goldfish may result from induction of mild oxidative stress.

  2015cited by this paper
• Oxidative stress in obstructive sleep apnea and intermittent hypoxia--revisited--the bad ugly and good: implications to the heart and brain.

  2015cited by this paper
• Effects of subchronic exposure to glyphosate in juvenile oysters (Crassostrea gigas): From molecular to individual levels.

  2015cited by this paper
• Immunological and histopathological responses of the kidney of common carp (Cyprinus carpio L.) sublethally exposed to glyphosate.

  2015cited by this paper
• An Overview of Carcinogenic Heavy Metal: Molecular Toxicity Mechanism and Prevention

  2015cited by this paper
• Global transcriptomic profiling demonstrates induction of oxidative stress and of compensatory cellular stress responses in brown trout exposed to glyphosate and Roundup

  2015cited by this paper
• Progression of DNA damage induced by a glyphosate-based herbicide in fish (Anguilla anguilla) upon exposure and post-exposure periods--insights into the mechanisms of genotoxicity and DNA repair.

  2014cited by this paper
• Impact of glyphosate and glyphosate‐based herbicides on the freshwater environment

  2014cited by this paper
• Copper induced upregulation of apoptosis related genes in zebrafish (Danio rerio) gill.

  2013cited by this paper
• 3-Nitrotyrosine: A biomarker of nitrogen free radical species modified proteins in systemic autoimmunogenic conditions.

  2013cited by this paper
• GFP Transgenic Medaka (Oryzias latipes) under the Inducible cyp1a Promoter Provide a Sensitive and Convenient Biological Indicator for the Presence of TCDD and Other Persistent Organic Chemicals

  2013cited by this paper
• Toxic and genotoxic effects of Roundup on tadpoles of the Indian skittering frog (Euflictis cyanophlyctis) in the presence and absence of predator stress.

  2013cited by this paper
• Predicting fish acute toxicity using a fish gill cell line-based toxicity assay.

  2013cited by this paper
• Peroxynitrite, a Stealthy Biological Oxidant*

  2013cited by this paper
• Toxic effects of the herbicide Roundup in the guppy Poecilia vivipara acclimated to fresh water.

  2013cited by this paper
• Origin of first cells at terrestrial, anoxic geothermal fields

  2012cited by this paper
• S-Glutathionylation of the Na,K-ATPase Catalytic α Subunit Is a Determinant of the Enzyme Redox Sensitivity*

  2012cited by this paper
• NIH Image to ImageJ: 25 years of image analysis

  2012cited by this paper
• Acute exposure of a glyphosate-based herbicide affects the gills and liver of the Neotropical fish, Piaractus mesopotamicus.

  2012cited by this paper
• Histopathological changes and antioxidant response in brain and kidney of common carp exposed to atrazine and chlorpyrifos.

  2012cited by this paper
• Perinatal outcomes, mitochondrial toxicity and apoptosis in HIV-treated pregnant women and in-utero-exposed newborn

  2012cited by this paper
• Environmental chemical exposures and human epigenetics.

  2012cited by this paper
• Gestational Cadmium Exposure-Induced Ovotoxicity Delays Puberty through Oxidative Stress and Impaired Steroid Hormone Levels

  2011cited by this paper
• Role of oxidative stress and DNA damage in human carcinogenesis.

  2011cited by this paper
• Roundup Effects on Oxidative Stress Parameters and Recovery Pattern of Rhamdia quelen

  2011cited by this paper
• Identification of oxidized serum albumin in the cerebrospinal fluid of ischaemic stroke patients

  2011cited by this paper
• Embryonic exposure to cypermethrin induces apoptosis and immunotoxicity in zebrafish (Danio rerio).

  2011cited by this paper
• Accelerated apoptosis contributes to aging-related hyperinflammation in endotoxemia.

  2010cited by this paper
• Roundup causes oxidative stress in liver and inhibits acetylcholinesterase in muscle and brain of the fish Prochilodus lineatus.

  2010cited by this paper
• Na+, K+-ATPase: Ubiquitous Multifunctional Transmembrane Protein and its Relevance to Various Pathophysiological Conditions

  2010cited by this paper
• Herbicide Formulation with Glyphosate Affects Growth, Acetylcholinesterase Activity, and Metabolic and Hematological Parameters in Piava (Leporinus obtusidens)

  2010cited by this paper
• Effects of Roundup Transorb on fish: hematology, antioxidant defenses and acetylcholinesterase activity.

  2010cited by this paper
• CYP1A Expression in Caged Rainbow Trout Discriminates Among Sites with Various Degrees of Polychlorinated Biphenyl Contamination

  2010cited by this paper
• Inorganic mercury exposure: toxicological effects, oxidative stress biomarkers and bioaccumulation in the tropical freshwater fish matrinxã, Brycon amazonicus (Spix and Agassiz, 1829)

  2010cited by this paper
• Oxidative stress, DNA damage and antioxidant enzyme gene expression in the Pacific white shrimp, Litopenaeus vannamei when exposed to acute pH stress.

  2009cited by this paper
• An evaluation of the cytochrome P450 inhibition potential of selected pesticides in human hepatic microsomes

  2009cited by this paper
• Pollution induced nitrative stress and heat shock protein 70 overexpression in fish liver mitochondria.

  2009cited by this paper
• Low toxic herbicide Roundup induces mild oxidative stress in goldfish tissues.

  2009cited by this paper
• Glyphosate-based herbicides are toxic and endocrine disruptors in human cell lines.

  2009cited by this paper
• Toxicity and effects of a glyphosate-based herbicide on the Neotropical fish Prochilodus lineatus.

  2008cited by this paper
• The goldfish (Carassius auratus) as a model for neuroendocrine signaling.

  2008cited by this paper
• Levels of glyphosate in surface waters, sediments and soils associated with direct sowing soybean cultivation in north pampasic region of Argentina.

  2008cited by this paper
• Acute toxicity impacts of hexavalent chromium on behavior and histopathology of gill, kidney and liver of the freshwater fish, Channa punctatus (Bloch).

  2008cited by this paper
• Protein tyrosine nitration--functional alteration or just a biomarker?

  2008cited by this paper
• A complex barcode underlies the heterogeneous response of p53 to stress

  2008cited by this paper
• Genotoxic effects of Roundup on the fish Prochilodus lineatus.

  2008cited by this paper
• Time- and Dose-Dependent Effects of Roundup on Human Embryonic and Placental Cells

  2007cited by this paper
• Free radicals and antioxidants in normal physiological functions and human disease.

  2007cited by this paper
• Peroxynitrite: biochemistry, pathophysiology and development of therapeutics

  2007cited by this paper
• Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants.

  2006cited by this paper
• Molecular Biomarkers: Their significance and application in marine pollution monitoring

  2006cited by this paper
• Protein carbonyls: novel biomarkers of exposure to oxidative stress-inducing pesticides in freshwater fish Channa punctata (Bloch).

  2005cited by this paper
• Is oxidative stress the mechanism of blue sac disease in retene‐exposed trout larvae?

  2005cited by this paper
• Differential Effects of Glyphosate and Roundup on Human Placental Cells and Aromatase

  2005cited by this paper
• The basics about nitric oxide.

  2005cited by this paper
• Oxidants and asthma

  2004cited by this paper
• The role of oxidative damage and stress in aging.

  2004cited by this paper
• Cadmium-induced apoptosis through the mitochondrial pathway in rainbow trout hepatocytes: involvement of oxidative stress.

  2004cited by this paper
• Tissue-specific oxidative stress responses in fish exposed to 2,4-D and azinphosmethyl.

  2004cited by this paper
• Na(+)+K(+)-ATPase in gills of aquatic crustacea.

  2003cited by this paper
• Apoptotic insults impair Na+, K+-ATPase activity as a mechanism of neuronal death mediated by concurrent ATP deficiency and oxidant stress

  2003cited by this paper
• Ecological Risk Assessment for Aquatic Organisms from Over-Water Uses of Glyphosate

  2003cited by this paper
• Apoptosis in the development and maintenance of the immune system

  2003cited by this paper
• Hypoxia-induced endocytosis of Na,K-ATPase in alveolar epithelial cells is mediated by mitochondrial reactive oxygen species and PKC-zeta.

  2003cited by this paper
• Protein carbonyl groups as biomarkers of oxidative stress.

  2003cited by this paper
• Biochemistry of Na,K-ATPase.

  2002cited by this paper
• The use of the oxidative stress responses as biomarkers in Nile tilapia (Oreochromis niloticus) exposed to in vivo cadmium contamination.

  2002cited by this paper
• Role of Free Radicals in the Neurodegenerative Diseases

  2001cited by this paper
• Oxidative stress in chronic renal failure.

  2001cited by this paper

• Synergistic effect of chlorogenic acid and Saccharomyces boulardii on growth and health performance in Goldfish (Carassius auratus).

  2026cites this paper
• Network-based investigation of norfloxacin-induced nasal immune-related inflammatory responses in carp (Cyprinus carpio) and its cross-species implications for olfactory immune disturbance.

  2025cites this paper
• Sex-specific hepatotoxicity in zebrafish (Danio rerio) induced by Roundup WG® exposure

  2025influential citation
• Toxic effects of a glyphosate-based herbicide on tetra (Astyanax lacustris)

  2025cites this paper
• Mechanistic Biomarker Integration Reveals Oxidative and Osmoregulatory Disruption by S-Metolachlor in Rainbow Trout.

  2025cites this paper
• Effects of heat stress on HSP70 and Na+/K+-ATPase expressions in the gills of juvenile goldfish: Focus on tissue architecture, mucus secretion and protein nitration.

  2025cites this paper
• Immunohistochemical examination of HSP70, PCNA, 8-OHdG, iNOS and apoptosis in the gills of Lake Van fish (Alburnus tarichi (Güldenstädt, 1814)) after esfenvalerate exposure

  2025cites this paper
• Evaluation of histological architecture, cellular apoptosis, dinitrophenyl protein and superoxide dismutase expressions in the gills of goldfish exposed to environmentally relevant pesticide mixtures: Potential mechanisms to disrupt osmoregulation.

  2025cites this paper
• Combined effects of cold plasma and Laurus nobilis essential oil on stress and flavor in hybrid grouper (Epinephelus fuscoguttatus♀ × Epinephelus lanceolatus♂) during live transport

  2025cites this paper
• Adverse Effects of Glyphosate and Microcystin-LR on Fish Health: Evidence from Structural and Functional Impairments in Zebrafish Gills

  2025cites this paper
• Effects of Lactobacillus acidophilus AC on the growth, intestinal flora and metabolism of zebrafish (Danio rerio).

  2024cites this paper
• Histological, biochemical and immunohistochemical assessments of Roundup®, atrazine, and 2,4-D mixtures on tissue architecture, body fluid conditions, nitrotyrosine protein and Na+/K+-ATPase expressions in the American oyster, Crassostera virginica.

  2024cites this paper
• Assessing the negative impact of chlorantraniliprole, isoxaflutole, and simazine pesticides on phospholipid membrane models and tilapia gill tissues.

  2024cites this paper
• Biological-based techniques for real-time water-quality studies: Assessment of non-invasive (swimming consistency and respiration) and toxicity (antioxidants) biomarkers of zebrafish.

  2024cites this paper