Toxicity by descent: A comparative approach for chemical hazard assessment

John K. Colbourne; Joseph R. Shaw; Elena Sostare; Claudia Rivetti; Romain Derelle; Rosemary Barnett; Bruno Campos; Carlie LaLone; Mark R. Viant; Geoff Hodges

doi:10.1016/j.envadv.2022.100287

Toxicity by descent: A comparative approach for chemical hazard assessment

John K. Colbourne^*, Joseph R. Shaw, Elena Sostare, Claudia Rivetti, Romain Derelle, Rosemary Barnett, Bruno Campos, Carlie LaLone, Mark R. Viant, Geoff Hodges

^*Corresponding author for this work

Biosciences

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Abstract

Toxicology is traditionally divided between human and eco-toxicology. In the shared pursuit of environmental health, this separation does not account for discoveries made in the comparative studies of animal genomes. Here, we provide evidence on the feasibility of understanding the health impact of chemicals on all animals, including ecological keystone species and humans, based on a significant number of conserved genes and their functional associations to health-related outcomes across much of animal diversity. We test four conditions to understand the value of comparative genomics data to inform mechanism-based human and environmental hazard assessment: (1) genes that are most fundamental for health evolved early during animal evolution; (2) the molecular functions of pathways are better conserved among distantly related species than the individual genes that are members of these pathways; (3) the most conserved pathways among animals are those that cause adverse health outcomes when disrupted; (4) gene sets that serve as molecular signatures of biological processes or disease-states are largely enriched by evolutionarily conserved genes across the animal phylogeny. The concept of homology is applied in a comparative analysis of gene families and pathways among invertebrate and vertebrate species compared with humans. Results show that over 70% of gene families associated with disease are shared among the greatest variety of animal species through evolution. Pathway conservation between invertebrates and humans is based on the degree of conservation within vertebrates and the number of interacting genes within the human network. Human gene sets that already serve as biomarkers are enriched by evolutionarily conserved genes across the animal phylogeny. By implementing a comparative method for chemical hazard assessment, human and eco-toxicology converge towards a more holistic and mechanistic understanding of toxicity disrupting biological processes that are important for health and shared among animals (including humans).

Original language	English
Article number	100287
Journal	Environmental Advances
Volume	9
DOIs	https://doi.org/10.1016/j.envadv.2022.100287
Publication status	Published - 15 Sept 2022

Bibliographical note

Funding Information:
We thank Don Gilbert (Indiana University) for his contributions to advancing the science of annotating genomes of both model and emerging model species. Thanks also to James (Ben) Brown (Laurence Berkeley National Laboratory) for his ideas reflected in the paper. This work was partly funded by a research framework contract to MHS from the European Chemicals Agency ( ECHA/2018/135 ). It is also part of the PrecisionTox project that has received funding from the European Union's Horizon 2020 research and innovation programme under grant agreement No 965406 . The views expressed in this work are those of the authors and do not necessarily reflect the views or policies of the US EPA, nor does the mention of trade names or commercial products constitute endorsement or recommendation for use.

Funding Information:
We thank Don Gilbert (Indiana University) for his contributions to advancing the science of annotating genomes of both model and emerging model species. Thanks also to James (Ben) Brown (Laurence Berkeley National Laboratory) for his ideas reflected in the paper. This work was partly funded by a research framework contract to MHS from the European Chemicals Agency (ECHA/2018/135). It is also part of the PrecisionTox project that has received funding from the European Union's Horizon 2020 research and innovation programme under grant agreement No 965406. The views expressed in this work are those of the authors and do not necessarily reflect the views or policies of the US EPA, nor does the mention of trade names or commercial products constitute endorsement or recommendation for use.

Publisher Copyright:
© 2022 The Authors

Keywords

Biomarkers
Comparative toxicology
Cross-species extrapolation
Evolutionary toxicology
Genomics
Model species

ASJC Scopus subject areas

Global and Planetary Change
Environmental Chemistry
Environmental Science (miscellaneous)

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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Cite this

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title = "Toxicity by descent: A comparative approach for chemical hazard assessment",

abstract = "Toxicology is traditionally divided between human and eco-toxicology. In the shared pursuit of environmental health, this separation does not account for discoveries made in the comparative studies of animal genomes. Here, we provide evidence on the feasibility of understanding the health impact of chemicals on all animals, including ecological keystone species and humans, based on a significant number of conserved genes and their functional associations to health-related outcomes across much of animal diversity. We test four conditions to understand the value of comparative genomics data to inform mechanism-based human and environmental hazard assessment: (1) genes that are most fundamental for health evolved early during animal evolution; (2) the molecular functions of pathways are better conserved among distantly related species than the individual genes that are members of these pathways; (3) the most conserved pathways among animals are those that cause adverse health outcomes when disrupted; (4) gene sets that serve as molecular signatures of biological processes or disease-states are largely enriched by evolutionarily conserved genes across the animal phylogeny. The concept of homology is applied in a comparative analysis of gene families and pathways among invertebrate and vertebrate species compared with humans. Results show that over 70% of gene families associated with disease are shared among the greatest variety of animal species through evolution. Pathway conservation between invertebrates and humans is based on the degree of conservation within vertebrates and the number of interacting genes within the human network. Human gene sets that already serve as biomarkers are enriched by evolutionarily conserved genes across the animal phylogeny. By implementing a comparative method for chemical hazard assessment, human and eco-toxicology converge towards a more holistic and mechanistic understanding of toxicity disrupting biological processes that are important for health and shared among animals (including humans).",

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note = "Funding Information: We thank Don Gilbert (Indiana University) for his contributions to advancing the science of annotating genomes of both model and emerging model species. Thanks also to James (Ben) Brown (Laurence Berkeley National Laboratory) for his ideas reflected in the paper. This work was partly funded by a research framework contract to MHS from the European Chemicals Agency ( ECHA/2018/135 ). It is also part of the PrecisionTox project that has received funding from the European Union's Horizon 2020 research and innovation programme under grant agreement No 965406 . The views expressed in this work are those of the authors and do not necessarily reflect the views or policies of the US EPA, nor does the mention of trade names or commercial products constitute endorsement or recommendation for use. Funding Information: We thank Don Gilbert (Indiana University) for his contributions to advancing the science of annotating genomes of both model and emerging model species. Thanks also to James (Ben) Brown (Laurence Berkeley National Laboratory) for his ideas reflected in the paper. This work was partly funded by a research framework contract to MHS from the European Chemicals Agency (ECHA/2018/135). It is also part of the PrecisionTox project that has received funding from the European Union's Horizon 2020 research and innovation programme under grant agreement No 965406. The views expressed in this work are those of the authors and do not necessarily reflect the views or policies of the US EPA, nor does the mention of trade names or commercial products constitute endorsement or recommendation for use. Publisher Copyright: {\textcopyright} 2022 The Authors",

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AU - Viant, Mark R.

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Toxicity by descent: A comparative approach for chemical hazard assessment

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

UN SDGs

Access to Document

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Cite this