Biomarkers of metabolic disorders and neurobehavioral diseases in a PCB- exposed population: What we learned and the implications for future research

Simhadri, Jyothirmai J.; Loffredo, Christopher A.; Trnovec, T.; Murínová, Ľubica Palkovičová; Nunlee-Bland, Gail; Koppe, Janna G.; Schoeters, Greet; Jana, Siddhartha S.; Ghosh, Somiranjan

doi:10.1016/j.envres.2020.110211

Cited by 25 publications

(8 citation statements)

References 119 publications

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“…Hepatic steatosis, or lipid accumulation, has been documented in several animals exposed to chlorpyrifos and other organophosphate pesticides (Ojha et al, 2011; Olsvik et al, 2015; Sanden et al, 2018; Søfteland et al, 2014). The disruption of lipids and fatty acids likely contributes to an overall state of metabolic disorder, which has been linked to a number of widespread metabolic diseases in humans exposed to environmental contaminants (see Simhadri et al, 2020). We found several signature biomarkers of metabolic disorder induced from contaminant exposure (Simhadri et al, 2020) in high dose–exposed Japanese quail, including dysregulation of myc protooncogene, paraoxonase 1, AhR , leptin receptor, ectonucleoside triphosphate diphosphohydrolase 5, and integrin subunit beta 3, which, together with enrichment of KEGG pathways related to metabolic disorders (diabetes, renin secretion, pancreatic secretion, insulin secretion), supports the claim that chlorpyrifos exposure in sensitive species can lead to metabolic disease.…”

Section: Discussionmentioning

confidence: 99%

Using Transcriptomics and Metabolomics to Understand Species Differences in Sensitivity to Chlorpyrifos in Japanese Quail and Double‐Crested Cormorant Embryos

Desforges

Legrand

Boulager

et al. 2021

Enviro Toxic and Chemistry

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Modern 21st‐century toxicity testing makes use of omics technologies to address critical questions in toxicology and chemical management. Of interest are questions relating to chemical mechanisms of toxicity, differences in species sensitivity, and translation of molecular effects to observable apical endpoints. Our study addressed these questions by comparing apical outcomes and multiple omics responses in early–life stage exposure studies with Japanese quail (Coturnix japonica) and double‐crested cormorant (Phalacrocorax auritus), representing a model and ecological species, respectively. Specifically, we investigated the dose‐dependent response of apical outcomes as well as transcriptomics and metabolomics in the liver of each species exposed to chlorpyrifos, a widely used organophosphate pesticide. Our results revealed a clear pattern of dose‐dependent disruption of gene expression and metabolic profiles in Japanese quail but not double‐crested cormorant at similar chlorpyrifos exposure concentrations. The difference in sensitivity between species was likely due to higher metabolic transformation of chlorpyrifos in Japanese quail compared to double‐crested cormorant. The most impacted biological pathways after chlorpyrifos exposure in Japanese quail included hepatic metabolism, oxidative stress, endocrine disruption (steroid and nonsteroid hormones), and metabolic disease (lipid and fatty acid metabolism). Importantly, we show consistent responses across biological scales, suggesting that significant disruption at the level of gene expression and metabolite profiles leads to observable apical responses at the organism level. Our study demonstrates the utility of evaluating effects at multiple biological levels of organization to understand how modern toxicity testing relates to outcomes of regulatory relevance, while also highlighting important, yet poorly understood, species differences in sensitivity to chemical exposure. Environ Toxicol Chem 2021;40:3019–3033. © 2021 SETAC

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Section: Discussionmentioning

confidence: 99%

Using Transcriptomics and Metabolomics to Understand Species Differences in Sensitivity to Chlorpyrifos in Japanese Quail and Double‐Crested Cormorant Embryos

Desforges

Legrand

Boulager

et al. 2021

Enviro Toxic and Chemistry

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“…Classified within the most deleterious persistent organic compounds (POPs) for human, animal and ecosystem health (Stockholm Convention on POPs, 2015 ; Hens and Hens, 2017 ), polychlorinated biphenyls (PCBs) are a wide class of 209 congeners containing biphenyl with one up to 10 chlorine atoms. Although their production was banned worldwide in 1979 (Passatore et al ., 2014 ), PCBs still represent a threat for their teratogenic (Berghuis and Roze, 2019 ), carcinogenic (Magoni et al ., 2019 ; Guo et al ., 2020 ), mutagenic potential (Murati et al ., 2020 ), together with their recalcitrance in the environment (Simhadri et al ., 2020 ), persistence and biomagnification in the food web (Amutova et al ., 2021 ). For land reclamation, PCB‐polluted soils should be excavated for off‐site treatment by solvent extraction, thermal alkaline dechlorination, incineration or landfilling (Campanella et al ., 2002 ).…”

Section: The ‘Cry‐for‐help’ Hypothesis Is Poorly Investigated In Polluted Environmentsmentioning

confidence: 99%

‘Cry‐for‐help’ in contaminated soil: a dialogue among plants and soil microbiome to survive in hostile conditions

Rolli

Vergani

Ghitti

et al. 2021

Environmental Microbiology

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Summary An open question in environmental ecology regards the mechanisms triggered by root chemistry to drive the assembly and functionality of a beneficial microbiome to rapidly adapt to stress conditions. This phenomenon, originally described in plant defence against pathogens and predators, is encompassed in the ‘cry‐for‐help’ hypothesis. Evidence suggests that this mechanism may be part of the adaptation strategy to ensure the holobiont fitness in polluted environments. Polychlorinated biphenyls (PCBs) were considered as model pollutants due to their toxicity, recalcitrance and poor phyto‐extraction potential, which lead to a plethora of phytotoxic effects and rise environmental safety concerns. Plants have inefficient detoxification processes to catabolize PCBs, even leading to by‐products with a higher toxicity. We propose that the ‘cry‐for‐help’ mechanism could drive the exudation‐mediated recruitment and sustainment of the microbial services for PCBs removal, exerted by an array of anaerobic and aerobic microbial degrading populations working in a complex metabolic network. Through this synergistic interaction, the holobiont copes with the soil contamination, releasing the plant from the pollutant stress by the ecological services provided by the boosted metabolism of PCBs microbial degraders. Improving knowledge of root chemistry under PCBs stress is, therefore, advocated to design rhizoremediation strategies based on plant microbiome engineering.

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“…A wide range of human health effects have been observed in PCBs exposure: higher serum levels are associated with blood and immune cells reduction [ 83 ]. Metabolic disorders include type 2 diabetes, insulin resistance and obesity [ 84 ]. Neurobehavioral disorders include neuropathies, cognitive, motor, and sensory impairments [ 84 ].…”

Section: Endocrine Disruptorsmentioning

confidence: 99%

“…Metabolic disorders include type 2 diabetes, insulin resistance and obesity [ 84 ]. Neurobehavioral disorders include neuropathies, cognitive, motor, and sensory impairments [ 84 ]. Other severe effects include endocrine disruption and direct activity of the pollutants against sex hormone receptors [ 84 , 85 ].…”

Section: Endocrine Disruptorsmentioning

confidence: 99%

Integrated Genomic and Bioinformatics Approaches to Identify Molecular Links between Endocrine Disruptors and Adverse Outcomes

Verga

Huff

Owens

et al. 2022

IJERPH

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Exposure to Endocrine Disrupting Chemicals (EDC) has been linked with several adverse outcomes. In this review, we examine EDCs that are pervasive in the environment and are of concern in the context of human, animal, and environmental health. We explore the consequences of EDC exposure on aquatic life, terrestrial animals, and humans. We focus on the exploitation of genomics technologies and in particular whole transcriptome sequencing. Genome-wide analyses using RNAseq provides snap shots of cellular, tissue and whole organism transcriptomes under normal physiological and EDC perturbed conditions. A global view of gene expression provides highly valuable information as it uncovers gene families or more specifically, pathways that are affected by EDC exposures, but also reveals those that are unaffected. Hypotheses about genes with unknown functions can also be formed by comparison of their expression levels with genes of known function. Risk assessment strategies leveraging genomic technologies and the development of toxicology databases are explored. Finally, we review how the Adverse Outcome Pathway (AOP) has exploited this high throughput data to provide a framework for toxicology studies.

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Biomarkers of metabolic disorders and neurobehavioral diseases in a PCB- exposed population: What we learned and the implications for future research

Cited by 25 publications

References 119 publications

Using Transcriptomics and Metabolomics to Understand Species Differences in Sensitivity to Chlorpyrifos in Japanese Quail and Double‐Crested Cormorant Embryos

Using Transcriptomics and Metabolomics to Understand Species Differences in Sensitivity to Chlorpyrifos in Japanese Quail and Double‐Crested Cormorant Embryos

‘Cry‐for‐help’ in contaminated soil: a dialogue among plants and soil microbiome to survive in hostile conditions

Integrated Genomic and Bioinformatics Approaches to Identify Molecular Links between Endocrine Disruptors and Adverse Outcomes

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