Glyphosate-based herbicides are toxic and endocrine disruptors in human cell lines
Abstract
Glyphosate-based herbicides are the most widely used across the world; they are commercialized in different formulations. Their residues are frequent pollutants in the environment. In addition, these herbicides are spread on most eaten transgenic plants, modified to tolerate high levels of these compounds in their cells. Up to 400 ppm of their residues are accepted in some feed. We exposed human liver HepG2 cells, a well-known model to study xenobiotic toxicity, to four different formulations and to glyphosate, which is usually tested alone in chronic in vivo regulatory studies. We measured cytotoxicity with three assays (Alamar Blue, MTT, ToxiLight), plus genotoxicity (comet assay), anti-estrogenic (on ERalpha, ERbeta) and anti-androgenic effects (on AR) using gene reporter tests. We also checked androgen to estrogen conversion by aromatase activity and mRNA. All parameters were disrupted at sub-agricultural doses with all formulations within 24h. These effects were more dependent on the formulation than on the glyphosate concentration. First, we observed a human cell endocrine disruption from 0.5 ppm on the androgen receptor in MDA-MB453-kb2 cells for the most active formulation (R400), then from 2 ppm the transcriptional activities on both estrogen receptors were also inhibited on HepG2. Aromatase transcription and activity were disrupted from 10 ppm. Cytotoxic effects started at 10 ppm with Alamar Blue assay (the most sensitive), and DNA damages at 5 ppm. A real cell impact of glyphosate-based herbicides residues in food, feed or in the environment has thus to be considered, and their classifications as carcinogens/mutagens/reprotoxics is discussed.
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Roundup concentrations in the range of 10^3 times below the MRL induced endocrine disturbances in human cells and toxic effects thereafter, including in vivo.
“it has been demonstrated that R concentrations in the range of 10 3 times below the MRL induced endocrine disturbances in human cells (Gasnier et al., 2009) and toxic effects thereafter (Benachour and Seralini, 2009), including in vivo (Romano et al., 2012).”
From RETRACTED: Long term toxicity of a Roundup herbicide and a Roundup-tolerant genetically modified maize (2012) · cites this paper as Gasnier et al., 2009
R has been shown to disrupt aromatase which synthesizes estrogens, but also to interfere with estrogen and androgen receptors in cells.
“R has been shown to disrupt aromatase which synthesizes estrogens (Richard et al., 2005), but to also interfere with estrogen and androgen receptors in cells (Gasnier et al., 2009).”
From RETRACTED: Long term toxicity of a Roundup herbicide and a Roundup-tolerant genetically modified maize (2012) · cites this paper as Gasnier et al., 2009
At low contaminating levels, adjuvants may be better candidates than G to explain the toxicity or endocrine disruptive side effects of R on human cells and also in vivo for acute toxicity.
“Even if G has shown to interact directly with the active site of aromatase at high levels [19], at low contaminating levels, adjuvants may be better candidates than G to explain the toxicity or endocrine disruptive side effects of R on human cells [8,20] and also in vivo for acute toxicity [21].”
From Republished study: long-term toxicity of a Roundup herbicide and a Roundup-tolerantgenetically modified maize (2014) · cites this paper as [8]
R concentrations in the range of 103 times below the MRL can induce endocrine disturbances in human cells and toxic effects thereafter.
“Indeed, it has been demonstrated that R concentrations in the range of 103 times below the MRL can induce endocrine disturbances in human cells [8] and toxic effects thereafter [9].”
From Republished study: long-term toxicity of a Roundup herbicide and a Roundup-tolerantgenetically modified maize (2014) · cites this paper as [8]
This is consistent with the well-documented toxic effect of very low dilutions of R on apoptosis, mitochondrial function, and cell membrane degradation, inducing necrosis of hepatocytes, and in other cell lines.
“This is consistent with the well-documented toxic effect of very low dilutions of R on apoptosis, mitochondrial function, and cell membrane degradation, inducing necrosis of hepatocytes, and in other cell lines [8,9,44,45].”
From Republished study: long-term toxicity of a Roundup herbicide and a Roundup-tolerantgenetically modified maize (2014) · cites this paper as [8]
R with adjuvants has been shown to disrupt aromatase, which synthesizes estrogen, and to interfere with estrogen and androgen receptors in cells.
“In addition, R with adjuvants has been shown to disrupt aromatase, which synthesizes estrogen [19], and to interfere with estrogen and androgen receptors in cells [8].”
From Republished study: long-term toxicity of a Roundup herbicide and a Roundup-tolerantgenetically modified maize (2014) · cites this paper as [8]
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Glyphosate induces human breast cancer cells growth via estrogen receptors
Thongprakaisang, S., Thiantanawat, A., Rangkadilok, N., Suriyo, T., & Satayavivad, J. (2013) · Food and Chemical Toxicology · doi:10.1016/j.fct.2013.05.057 · Cited by 424 · see citing works
Ethoxylated adjuvants of glyphosate-based herbicides are active principles of human cell toxicity
Mesnage, R., Bernay, B., & Séralini, G.-E. (2013) · Toxicology · doi:10.1016/j.tox.2012.09.006 · Cited by 424 · see citing works
Self-citationSéralini, G.-E., Clair, E., Mesnage, R., Gress, S., Defarge, N., Malatesta, M., Hennequin, D., & de Vendômois, J. S. (2012) · Food and Chemical Toxicology · doi:10.1016/j.fct.2012.08.005 · Cited by 397 · see citing works
Self-citationRetractedPesticide exposure in children
Roberts, J. R., Karr, C. J., COUNCIL ON ENVIRONMENTAL HEALTH, Paulson, J. A., Brock-Utne, A. C., Brumberg, H. L., Campbell, C. C., Lanphear, B. P., Osterhoudt, K. C., Sandel, M. T., et al. (2012) · Pediatrics · doi:10.1542/peds.2012-2758 · Cited by 351 · see citing works
Major Pesticides Are More Toxic to Human Cells Than Their Declared Active Principles
Mesnage, R., Defarge, N., Spiroux de Vendômois, J., & Séralini, G.-E. (2014) · BioMed Research International · doi:10.1155/2014/179691 · Cited by 342 · see citing works
Self-citationSéralini, G.-E., Clair, E., Mesnage, R., Gress, S., Defarge, N., Malatesta, M., Hennequin, D., & de Vendômois, J. S. (2014) · Environmental Sciences Europe · doi:10.1186/s12302-014-0014-5 · Cited by 299 · see citing works
Self-citationMeftaul, I. M., Venkateswarlu, K., Dharmarajan, R., Annamalai, P., Asaduzzaman, M., Parven, A., & Megharaj, M. (2020) · Environmental Pollution · doi:10.1016/j.envpol.2020.114372 · Cited by 218 · see citing works
Defarge, N., Takács, E., Lozano, V., Mesnage, R., Spiroux de Vendômois, J., Séralini, G.-E., & Székács, A. (2016) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph13030264 · Cited by 205 · see citing works
Self-citationGlyphosate impairs male offspring reproductive development by disrupting gonadotropin expression
Romano, M. A., Romano, R. M., Santos, L. D., Wisniewski, P., Campos, D. A., de Souza, P. B., Viau, P., Bernardi, M. M., Nunes, M. T., & de Oliveira, C. A. (2012) · Archives of Toxicology · doi:10.1007/s00204-011-0788-9 · Cited by 196 · see citing works
Environmental Toxin Screening Using Human-Derived 3D Bioengineered Liver and Cardiac Organoids
Forsythe, S. D., Devarasetty, M., Shupe, T., Bishop, C., Atala, A., Soker, S., & Skardal, A. (2018) · Frontiers in Public Health · doi:10.3389/fpubh.2018.00103 · Cited by 112 · see citing works
Glyphosate: too much of a good thing?
Cuhra, M., Bøhn, T., & Cuhra, P. (2016) · Frontiers in Environmental Science · doi:10.3389/fenvs.2016.00028 · Cited by 106 · see citing works
Genetically modified crops safety assessments: present limits and possible improvements
Séralini, G.-E., Mesnage, R., Clair, E., Gress, S., de Vendômois, J. S., & Cellier, D. (2011) · Environmental Sciences Europe · doi:10.1186/2190-4715-23-10 · Cited by 82 · see citing works
Self-citationDebate on GMOs health risks after statistical findings in regulatory tests
de Vendômois, J. S., Cellier, D., Vélot, C., Clair, E., Mesnage, R., & Séralini, G.-E. (2010) · International Journal of Biological Sciences · doi:10.7150/ijbs.6.590 · Cited by 64 · see citing works
Self-citationSeralini, G.-E., & Jungers, G. (2021) · Toxicology Reports · doi:10.1016/j.toxrep.2021.07.014 · Cited by 57 · see citing works
Dig1 protects against cell death provoked by glyphosate-based herbicides in human liver cell lines
Gasnier, C., Benachour, N., Clair, E., Travert, C., Langlois, F., Laurant, C., Decroix-Laporte, C., & Séralini, G.-E. (2010) · Journal of Occupational Medicine and Toxicology · doi:10.1186/1745-6673-5-29 · Cited by 49 · see citing works
Self-citationDefined plant extracts can protect human cells against combined xenobiotic effects
Gasnier, C., Laurant, C., Decroix-Laporte, C., Mesnage, R., Clair, E., Travert, C., & Séralini, G.-E. (2011) · Journal of Occupational Medicine and Toxicology · doi:10.1186/1745-6673-6-3 · Cited by 31 · see citing works
Self-citation
- Authors
- Gasnier, C., Dumont, C., Benachour, N., Clair, E., Chagnon, M.-C., & Séralini, G.-E.
- Affiliations
- Université de Caen Normandie (FR)
- Université de Bourgogne (FR)
- Venue
- Toxicology
- Publisher
- Elsevier BV
- Published
- 2009-08
- Volume
- 262
- Issue
- 3
- Pages
- 184-191
- ISSN
- 0300-483X (ISSN-L)
- OpenAlex
- W2120475447
- Cited by
- 658
- References
- 95
- Citations by year
- 2026: 22 · 2025: 35 · 2024: 41 · 2023: 37 · 2022: 38 · 2021: 65 · 2020: 61 · 2019: 60 · 2018: 59 · 2017: 46 · 2016: 44 · 2015: 23 · 2014: 31 · 2013: 25 · 2012: 27
- FWCI
- 26.51
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Toxicology (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- Funders
- Fondation Denis Guichard
- Topics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Pesticide Exposure and Toxicity
- Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Effects and risks of endocrine disrupting chemicals
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Carcinogens and Genotoxicity Assessment
- Keywords
- glyphosate-based herbicides, endocrine disruption, cytotoxicity, genotoxicity, estrogen receptor alpha, estrogen receptor beta, androgen receptor, aromatase, herbicide formulation, genetically modified crops, HepG2 cells, DNA damage
- MeSH terms
- Glyphosate, Adolescent, Aromatase, DNA Damage, Dose-Response Relationship, Drug, Glycine, Herbicides, Humans, Male, Pesticide Residues, Receptors, Androgen, RNA, Messenger, Transcription, Genetic, Genes, Reporter, Toxicity Tests, Comet Assay, Cell Line, Tumor, Estrogen Receptor alpha, Estrogen Receptor beta, Endocrine Disruptors
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