A toxicity pathway-oriented approach to develop adverse outcome pathway: AHR activation as a case study.

With numerous new chemicals introduced into the environment everyday, identification of their potential hazards to the environment and human health is a considerable challenge. Developing adverse outcome pathway (AOP) framework is promising in helping to achieve this goal as it can bring In Vitro testing into toxicity measurement and understanding. To explore the toxic mechanism underlying environmental chemicals via the AOP approach, an integration of adequate experimental data with systems biology understanding is preferred. Here, we describe a novel method to develop reliable and sensible AOPs that relies on chemical-gene interactions, toxicity pathways, molecular regulations, phenotypes, and outcomes information obtained from comparative toxicogenomics database (CTD) and Ingenuity Pathway Analysis (IPA). Using Benzo(a)pyrene (BaP), a highly studied chemical as a stressor, we identified the pivotal IPA toxicity pathways, the molecular initiating event (MIE), and candidate key events (KEs) to structure AOPs in the liver and lung, respectively. Further, we used the corresponding CTD information of multiple typical AHR-ligands, including 2,3,7,8-tetrachlorodibenzoparadioxin (TCDD), valproic acid, quercetin, and particulate matter, to validate our AOP networks. Our approach is likely to speed up AOP development as providing a time- and cost-efficient way to collect all fragmented bioinformation in published studies. It also facilitates a better understanding of the toxic mechanism of environmental chemicals, and potentially brings new insights into the screening of critical paths in the AOP network.

[1]  Melvin E Andersen,et al.  Defining and modeling known adverse outcome pathways: Domoic acid and neuronal signaling as a case study , 2011, Environmental toxicology and chemistry.

[2]  Andreas Krämer,et al.  Causal analysis approaches in Ingenuity Pathway Analysis , 2013, Bioinform..

[3]  Stephen W. Edwards,et al.  Integrating Publicly Available Data to Generate Computationally Predicted Adverse Outcome Pathways for Fatty Liver. , 2016, Toxicological sciences : an official journal of the Society of Toxicology.

[4]  Stephen W. Edwards,et al.  Creating a Structured AOP Knowledgebase via Ontology-Based Annotations. , 2017, Applied in vitro toxicology.

[5]  Anne Gourmelon,et al.  The Adverse Outcome Pathway Concept: A Basis for Developing Regulatory Decision-making Tools , 2016, Alternatives to laboratory animals : ATLA.

[6]  Béatrice Desvergne,et al.  RXR: from partnership to leadership in metabolic regulations. , 2007, Vitamins and hormones.

[7]  Y Fujii-Kuriyama,et al.  Molecular mechanisms of AhR functions in the regulation of cytochrome P450 genes. , 2005, Biochemical and biophysical research communications.

[8]  D. Krewski,et al.  Toxicity testing in the 21st century: progress in the past decade and future perspectives , 2019, Archives of Toxicology.

[9]  Karine Audouze,et al.  Linking Bisphenol S to Adverse Outcome Pathways Using a Combined Text Mining and Systems Biology Approach , 2019, Environmental health perspectives.

[10]  Georgia Tsiliki,et al.  A Data Fusion Pipeline for Generating and Enriching Adverse Outcome Pathway Descriptions , 2017, Toxicological sciences : an official journal of the Society of Toxicology.

[11]  Mustapha Kandouz,et al.  Oltipraz is a bifunctional inducer activating both phase I and phase II drug-metabolizing enzymes via the xenobiotic responsive element. , 2003, Molecular pharmacology.

[12]  Melvin E. Andersen,et al.  Temporal concordance between apical and transcriptional points of departure for chemical risk assessment. , 2013, Toxicological sciences : an official journal of the Society of Toxicology.

[13]  Paul A. Schulte,et al.  The Next Generation of Risk Assessment Multi-Year Study—Highlights of Findings, Applications to Risk Assessment, and Future Directions , 2016, Environmental health perspectives.

[14]  Sharon Munn,et al.  Adverse outcome pathway networks II: Network analytics , 2018, Environmental toxicology and chemistry.

[15]  Division on Earth Using 21st Century Science to Improve Risk-Related Evaluations , 2017 .

[16]  C. Guerreiro,et al.  Benzo(a)pyrene in Europe: Ambient air concentrations, population exposure and health effects. , 2016, Environmental pollution.

[17]  William Bourguet,et al.  Modulation of RXR function through ligand design. , 2012, Biochimica et biophysica acta.

[18]  Gerald Batist,et al.  Transcriptional Regulation of NF-E2 p45-related Factor (NRF2) Expression by the Aryl Hydrocarbon Receptor-Xenobiotic Response Element Signaling Pathway , 2005, Journal of Biological Chemistry.

[19]  Andrew Worth,et al.  Assessment of developmental neurotoxicity induced by chemical mixtures using an adverse outcome pathway concept , 2020, Environmental Health.

[20]  Taigang He,et al.  Integrated genomic approaches identify major pathways and upstream regulators in late onset Alzheimer’s disease , 2015, Scientific Reports.

[21]  Thomas C. Wiegers,et al.  The Comparative Toxicogenomics Database: update 2019 , 2018, Nucleic Acids Res..

[22]  M. Denison,et al.  Activation of the aryl hydrocarbon receptor by structurally diverse exogenous and endogenous chemicals. , 2003, Annual review of pharmacology and toxicology.

[23]  Masutaka Furue,et al.  Perillaldehyde Inhibits AHR Signaling and Activates NRF2 Antioxidant Pathway in Human Keratinocytes , 2018, Oxidative medicine and cellular longevity.

[24]  Stephen W. Edwards,et al.  An integrative data mining approach to identifying adverse outcome pathway signatures. , 2016, Toxicology.

[25]  Mathieu Vinken,et al.  Taking adverse outcome pathways to the next level. , 2018, Toxicology in vitro : an international journal published in association with BIBRA.

[26]  Jaeseong Jeong,et al.  Development of AOP relevant to microplastics based on toxicity mechanisms of chemical additives using ToxCast™ and deep learning models combined approach. , 2020, Environment international.

[27]  Jan G. Hengstler,et al.  Adverse outcome pathways: a concise introduction for toxicologists , 2017, Archives of Toxicology.