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Transcriptome Profile Analysis Reflects Rat Liver and Kidney Damage Following Chronic Ultra-Low Dose Roundup Exposure

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Transcriptome Profile Analysis Reflects Rat Liver and Kidney Damage Following Chronic Ultra-Low Dose Roundup Exposure King’s Research Portal DOI: 10.1186/s12940-015-0056-1 Document Version Publisher's PDF, also known as Version of record Link to publication record in King's Research Portal Citation for published version (APA): Mesnage, R., Arno, M., Costanzo, M., Malatesta, M., Séralini, G-E., & Antoniou, M. N. (2015). Transcriptome profile analysis reflects rat liver and kidney damage following chronic ultra-low dose Roundup exposure. Environmental Health, 14, 1-14. [70]. https://doi.org/10.1186/s12940-015-0056-1 Citing this paper Please note that where the full-text provided on King's Research Portal is the Author Accepted Manuscript or Post-Print version this may differ from the final Published version. If citing, it is advised that you check and use the publisher's definitive version for pagination, volume/issue, and date of publication details. 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Download date: 01. Oct. 2021 Mesnage et al. Environmental Health (2015) 14:70 DOI 10.1186/s12940-015-0056-1 RESEARCH Open Access Transcriptome profile analysis reflects rat liver and kidney damage following chronic ultra-low dose Roundup exposure Robin Mesnage1, Matthew Arno2, Manuela Costanzo3, Manuela Malatesta3, Gilles-Eric Séralini4 and Michael N. Antoniou1* Abstract Background: Glyphosate-based herbicides (GBH) are the major pesticides used worldwide. Converging evidence suggests that GBH, such as Roundup, pose a particular health risk to liver and kidneys although low environmentally relevant doses have not been examined. To address this issue, a 2-year study in rats administering 0.1 ppb Roundup (50 ng/L glyphosate equivalent) via drinking water (giving a daily intake of 4 ng/kg bw/day of glyphosate) was conducted. A marked increased incidence of anatomorphological and blood/urine biochemical changes was indicative of liver and kidney structure and functional pathology. In order to confirm these findings we have conducted a transcriptome microarray analysis of the liver and kidneys from these same animals. Results: The expression of 4224 and 4447 transcript clusters (a group of probes corresponding to a known or putative gene) were found to be altered respectively in liver and kidney (p < 0.01, q < 0.08). Changes in gene expression varied from −3.5 to 3.7 fold in liver and from −4.3 to 5.3 in kidneys. Among the 1319 transcript clusters whose expression was altered in both tissues, ontological enrichment in 3 functional categories among 868 genes were found. First, genes involved in mRNA splicing and small nucleolar RNA were mostly upregulated, suggesting disruption of normal spliceosome activity. Electron microscopic analysis of hepatocytes confirmed nucleolar structural disruption. Second, genes controlling chromatin structure (especially histone-lysine N-methyltransferases) were mostly upregulated. Third, genes related to respiratory chain complex I and the tricarboxylic acid cycle were mostly downregulated. Pathway analysis suggests a modulation of the mTOR and phosphatidylinositol signalling pathways. Gene disturbances associated with the chronic administration of ultra-low dose Roundup reflect a liver and kidney lipotoxic condition and increased cellular growth that may be linked with regeneration in response to toxic effects causing damage to tissues. Observed alterations in gene expression were consistent with fibrosis, necrosis, phospholipidosis, mitochondrial membrane dysfunction and ischemia, which correlate with and thus confirm observations of pathology made at an anatomical, histological and biochemical level. Conclusion: Our results suggest that chronic exposure to a GBH in an established laboratory animal toxicity model system at an ultra-low, environmental dose can result in liver and kidney damage with potential significant health implications for animal and human populations. Keywords: Pesticides, Glyphosate, Transcriptome, Chronic toxicity, Liver, Kidney * Correspondence: [email protected] 1Gene Expression and Therapy Group, Faculty of Life Sciences & Medicine, Department of Medical and Molecular Genetics, King’s College London, 8th Floor Tower Wing, Guy’s Hospital, Great Maze Pond, London SE1 9RT, UK Full list of author information is available at the end of the article © 2015 Mesnage et al. Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Mesnage et al. Environmental Health (2015) 14:70 Page 2 of 14 Background Nevertheless, it should be noted that most results from Glyphosate-based herbicides (GBH), such as Roundup, these GBH toxicity studies were obtained at doses far are the major pesticides used worldwide. GBH are cur- greater than general human population exposure. Doses rently applied on at least 24 % of the total global cropland tested were typically over the glyphosate acceptable daily (Benbrook C, personal communication), and also used intake (ADI), which is currently set at 0.3 mg/kg bw/day extensively in domestic and urban environments. Resi- within the European Union and 1.75 mg/kg bw/day in dues of GBH are routinely detected in foodstuffs [1, 2] the USA based on hepatorenal toxicity measurements and also drinking water contaminated via rain, surface after chronic exposure in rats, although GBH toxicity runoff and leaching into groundwater, thereby increasing was not investigated in life-long experiments. possible routes of exposure [3]. Epidemiological data on In order to address this issue, a 2-year study was con- the human body burden of GBH residues is very limited ducted where rats were administered via drinking water but evidence suggests that glyphosate and its metabolites at a concentration of 0.1 ppb Roundup, thus containing are wide-spread [4]. not only glyphosate but also adjuvants [17]. The gly- Glyphosate’s primary perceived mode of herbicidal phosate equivalent concentration was 0.05 μg/L and action is to inhibit 5-enolpyruvylshikimate-3-phosphate corresponds to an admissible concentration within the synthase (EPSPS) of the shikimate aromatic amino acid European Union (0.1 μg/L) and USA (700 μg/L). The biosynthesis pathway present in plants and some bac- results showed that Roundup caused an increased teria. Since this pathway is absent in vertebrates, it is incidence of anatomical signs of pathologies, as well as generally assumed that glyphosate poses minimal health changes in urine and blood biochemical parameters risks to mammals, including humans [5]. However, con- suggestive of liver and kidney functional insufficiency verging evidence suggests that GBH residues pose a par- in both sexes. In an effort to confirm these findings ticular risk to kidney and liver function. Hepatic effects through a more quantitative molecular biological ap- of glyphosate were first observed in the 1980s, including proach and obtain insight into the alterations in gene ex- its ability to disrupt liver mitochondrial oxidative phos- pression profiles associated with the observed increased phorylation [6]. As glyphosate can act as a protonophore signs of kidney and liver anatomorphological pathologies, increasing mitochondrial membrane permeability to pro- we conducted a full transcriptomic analysis of these or- tons and Ca2+ [7], it can trigger the production of react- gans from the female cohort of animals. A large number ive oxygen species resulting in observed oxidative stress of transcript clusters (>4000) were found to be altered in [8]. Elevation in oxidative stress markers is detected in their level of expression in both the liver and kidneys of rat liver and kidney after subchronic exposure to GBH the Roundup treated group relative to controls and to a at the United States permitted glyphosate concentration very high statistical significance. The alterations in gene of 700 μg/L in drinking water [9]. Hepatic histological expression profiles are typical of disturbances measured changes and alterations of clinical biochemistry are de- in cases of fibrosis, necrosis, phospholipidosis, mitochon- tected in rats consuming 4.87 mg/kg body weight (bw) drial membrane dysfunction and ischemia. Therefore our glyphosate every 2 days over 75 days [10].
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