Differential effects of glyphosate and roundup on human placental cells and aromatase
Open accessAbstract
Roundup is a glyphosate-based herbicide used worldwide, including on most genetically modified plants that have been designed to tolerate it. Its residues may thus enter the food chain, and glyphosate is found as a contaminant in rivers. Some agricultural workers using glyphosate have pregnancy problems, but its mechanism of action in mammals is questioned. Here we show that glyphosate is toxic to human placental JEG3 cells within 18 hr with concentrations lower than those found with agricultural use, and this effect increases with concentration and time or in the presence of Roundup adjuvants. Surprisingly, Roundup is always more toxic than its active ingredient. We tested the effects of glyphosate and Roundup at lower nontoxic concentrations on aromatase, the enzyme responsible for estrogen synthesis. The glyphosate-based herbicide disrupts aromatase activity and mRNA levels and interacts with the active site of the purified enzyme, but the effects of glyphosate are facilitated by the Roundup formulation in microsomes or in cell culture. We conclude that endocrine and toxic effects of Roundup, not just glyphosate, can be observed in mammals. We suggest that the presence of Roundup adjuvants enhances glyphosate bioavailability and/or bioaccumulation.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
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 Richard et al., 2005
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 [19]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
1 retracted
Williams, G. M., Kroes, R., & Munro, I. C. (2000) · Regulatory Toxicology and Pharmacology · doi:10.1006/rtph.1999.1371 · Cited by 864 · see citing works
RetractedBradford, M. M. (1976) · Analytical Biochemistry · doi:10.1016/0003-2697(76)90527-3 · Cited by 255,302 · see citing works
Single-Step Method of RNA Isolation by Acid Guanidinium Thiocyanate–Phenol–Chloroform Extraction
Chomczynski, P., & Sacchi, N. (1987) · Analytical Biochemistry · doi:10.1006/abio.1987.9999 · Cited by 65,240 · see citing works
Mosmann, T. (1983) · Journal of Immunological Methods · doi:10.1016/0022-1759(83)90303-4 · Cited by 56,104 · see citing works
Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction
Chomczyński, P., & Sacchi, N. (1987) · Analytical Biochemistry · doi:10.1016/0003-2697(87)90021-2 · Cited by 47,092 · see citing works
Thompson, E. A., & Siiteri, P. K. (1974) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(20)79735-8 · Cited by 698 · see citing works
Schönbrunn, E., Eschenburg, S., Shuttleworth, W. A., Schloss, J. V., Amrhein, N., Evans, J. N. S., & Kabsch, W. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.98.4.1376 · Cited by 575 · see citing works
Enhanced expression of a glyceraldehyde-3-phosphate dehydrogenase gene in human lung cancers.
Tokunaga, K., Nakamura, Y., Sakata, K., Fujimori, K., Ohkubo, M., Sawada, K., & Sakiyama, S. (1987) · PubMed · Cited by 537 · see citing works
Bulun, S., Sebastian, S., Takayama, K., Suzuki, T., Sasano, H., & Shozu, M. (2003) · Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/s0960-0760(03)00359-5 · Cited by 345 · see citing works
Walsh, L. P., McCormick, C., Martin, C. F., & Stocco, D. (2000) · Environmental Health Perspectives · doi:10.1289/ehp.00108769 · Cited by 339 · see citing works
Acquavella, J., Alexander, B. H., Mandel, J. S., Gustin, C., Baker, B. A., Chapman, P. S., & Bleeke, M. S. (2003) · Environmental Health Perspectives · doi:10.1289/ehp.6667 · Cited by 310 · see citing works
Corbin, C. J., Graham-Lorence, S. E., McPhaul, M. J., Mason, J. I., Mendelson, C. R., & Simpson, E. R. (1988) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.85.23.8948 · Cited by 298 · see citing works
Cytochrome P450 Nomenclature, 2004
Nelson, D. R. (2006) · Humana Press eBooks · doi:10.1385/1-59259-998-2:1 · Cited by 289 · see citing works
Male Pesticide Exposure and Pregnancy Outcome
Savitz, D. A., Arbuckle, T. E., Kaczor, D., & Curtis, K. M. (1997) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a009231 · Cited by 207 · see citing works
Nelson, D. R. (2003) · Humana Press eBooks · doi:10.1385/0-89603-519-0:15 · Cited by 202 · see citing works
Pesticide Roundup Provokes Cell Division Dysfunction at the Level of CDK1/Cyclin B Activation
Marc, J., Mulner‐Lorillon, O., Boulben, S., Hureau, D., Durand, G., & Bellé, R. (2002) · Chemical Research in Toxicology · doi:10.1021/tx015543g · Cited by 131 · see citing works
Effect of the Herbicide Glyphosate on Enzymatic Activity in Pregnant Rats and Their Fetuses
Daruich, J., Zirulnik, F., & Giménez, M. S. (2001) · Environmental Research · doi:10.1006/enrs.2000.4229 · Cited by 124 · see citing works
Aromatase inhibitors: past, present and future
Séralini, G., & Moslemi, S. (2001) · Molecular and Cellular Endocrinology · doi:10.1016/s0303-7207(01)00433-6 · Cited by 121 · see citing works
Self-citationGenetically Modified Organisms in FoodScreening and Specific Detection by Polymerase Chain Reaction
Vollenhofer, S., Burg, K., Schmidt, J., et al. (1999) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf990353l · Cited by 118 · see citing works
Toxic effects of carbofuran and glyphosate on semen characteristics in rabbits
Yousef, M. I., Salem, M. H., Ibrahim, H. Z., Helmi, S., Seehy, M. A., & Bertheussen, K. (1995) · Journal of Environmental Science and Health Part B · doi:10.1080/03601239509372951 · Cited by 114 · see citing works
BREWSTER, D. W. (1991) · Fundamental and Applied Toxicology · doi:10.1016/0272-0590(91)90237-x · Cited by 109 · see citing works
Seibert, H., Mörchel, S., & Gülden, M. (2002) · Toxicology in Vitro · doi:10.1016/s0887-2333(02)00014-0 · Cited by 96 · see citing works
Lioi, M. B., Scarfı̀, M. R., Santoro, A., et al. (1998) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/s0027-5107(98)00010-4 · Cited by 89 · see citing works
Nativelle-Serpentini, C., Richard, S., Séralini, G., et al. (2003) · Toxicology in Vitro · doi:10.1016/s0887-2333(03)00046-8 · Cited by 80 · see citing works
Self-citationAcute toxicity of Roundup® and Rodeo® herbicides to rainbow trout, chinook, and coho salmon
Mitchell, D. G., Chapman, P. M., & Long, T. J. (1987) · Bulletin of Environmental Contamination and Toxicology · doi:10.1007/bf01689594 · Cited by 69 · see citing works
Vigfusson, N. V., & Vyse, E. R. (1980) · Mutation Research/Genetic Toxicology · doi:10.1016/0165-1218(80)90147-0 · Cited by 51 · see citing works
Germ cells: a new source of estrogens in the male gonad
Carreau, S. (2001) · Molecular and Cellular Endocrinology · doi:10.1016/s0303-7207(01)00411-7 · Cited by 50 · see citing works
Lamb, D. C., Kelly, D. E., Hanley, Z., et al. (1998) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1997.7988 · Cited by 46 · see citing works
Studies on a new group of biodegradable surfactants for glyphosate
Haefs, R., Schmitz-Eiberger, M. A., Mainx, H. G., et al. (2002) · Pest Management Science · doi:10.1002/ps.539 · Cited by 44 · see citing works
Androgen and 19-norandrogen aromatization by equine and human placental microsomes
Dintinger, T., Gaillard, J., Moslemi, S., et al. (1989) · Journal of Steroid Biochemistry · doi:10.1016/0022-4731(89)90245-8 · Cited by 32 · see citing works
Self-citationVigfusson, N. V., & Vyse, E. R. (1980) · Mutation Research/Genetic Toxicology and Environmental Mutagenesis · Cited by 31 · see citing works
Auvray, P., Moslemi, S., Sourdaine, P., et al. (1998) · European Journal of Medicinal Chemistry · doi:10.1016/s0223-5234(98)80046-9 · Cited by 29 · see citing works
Self-citationAromatase gene expression in the stallion
Lemazurier, E., Sourdaine, P., Nativelle, C., et al. (2001) · Molecular and Cellular Endocrinology · doi:10.1016/s0303-7207(01)00435-x · Cited by 23 · see citing works
TAKAHASHI, K., Horie, M., & Nobuji, A. O. B. A. (2001) · Food Hygiene and Safety Science (Shokuhin Eiseigaku Zasshi) · doi:10.3358/shokueishi.42.304 · Cited by 21 · see citing works
Moslemi, S., Vibet, A., Papadopoulos, V. D., et al. (1997) · Comparative Biochemistry and Physiology Part B Biochemistry and Molecular Biology · doi:10.1016/s0305-0491(97)00033-3 · Cited by 20 · see citing works
Self-citationWarren, A. J., Ihnat, M. A., Ogdon, S. E., Rowell, E. E., & Hamilton, J. W. (1998) · Environmental and Molecular Mutagenesis · doi:10.1002/(sici)1098-2280(1998)31:1 · Cited by 17 · see citing works
Different in vitro metabolism of 7 α‐methyl‐19‐nortestosterone by human and equine aromatases
Moslemi, S., Dintinger, T., Dehennin, L., et al. (1993) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1993.tb17955.x · Cited by 15 · see citing works
Self-citationMolecular characterization and expression of equine testicular cytochrome P450 aromatase
Séralini, G., Tomilin, A. N., Auvray, P., et al. (2003) · Biochimica et Biophysica Acta (BBA) - Gene Structure and Expression · doi:10.1016/s0167-4781(02)00621-8 · Cited by 12 · see citing works
Estrogen synthetase in the horse
Vibet, A., Dintinger, T., Maboundou, J.-C., et al. (1990) · FEBS Letters · doi:10.1016/0014-5793(90)80629-w · Cited by 11 · see citing works
Moslemi, S., & Séralini, G. (1997) · Journal of enzyme inhibition · doi:10.3109/14756369709035817 · Cited by 11 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Glyphosate-based herbicides are toxic and endocrine disruptors in human cell lines
Gasnier, C., Dumont, C., Benachour, N., Clair, E., Chagnon, M.-C., & Séralini, G.-E. (2009) · Toxicology · doi:10.1016/j.tox.2009.06.006 · Cited by 658 · see citing works
Self-citationFemale reproductive disorders: the roles of endocrine-disrupting compounds and developmental timing
Crain, D. A., Janssen, S. J., Edwards, T. M., Heindel, J., Ho, S.-M., Hunt, P., Iguchi, T., Juul, A., McLachlan, J. A., Schwartz, J., et al. (2008) · Fertility and Sterility · doi:10.1016/j.fertnstert.2008.08.067 · Cited by 465 · see citing works
Benachour, N., & Séralini, G.-E. (2009) · Chemical Research in Toxicology · doi:10.1021/tx800218n · Cited by 428 · see citing works
Self-citationGlyphosate 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
“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.”
BackgroundSelf-citationRetractedMajor 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-citationTime- and dose-dependent effects of Roundup on human embryonic and placental cells
Benachour, N., Sipahutar, H., Moslemi, S., Gasnier, C., Travert, C., & Séralini, G. E. (2007) · Archives of Environmental Contamination and Toxicology · doi:10.1007/s00244-006-0154-8 · Cited by 226 · see citing works
Self-citationSéralini, G.-E., Cellier, D., & de Vendomois, J. S. (2007) · Archives of Environmental Contamination and Toxicology · doi:10.1007/s00244-006-0149-5 · Cited by 222 · see citing works
Meftaul, 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
Romano, R. M., Romano, M. A., Bernardi, M. M., Furtado, P. V., & Oliveira, C. A. (2010) · Archives of Toxicology · doi:10.1007/s00204-009-0494-z · Cited by 204 · see citing works
Glyphosate 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
A long-term study on female mice fed on a genetically modified soybean: effects on liver ageing
Malatesta, M., Boraldi, F., Annovi, G., Baldelli, B., Battistelli, S., Biggiogera, M., & Quaglino, D. (2008) · Histochemistry and Cell Biology · doi:10.1007/s00418-008-0476-x · Cited by 88 · 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
Seralini, G.-E., & Jungers, G. (2021) · Toxicology Reports · doi:10.1016/j.toxrep.2021.07.014 · Cited by 57 · see citing works
Malatesta, M., Perdoni, F., Santin, G., Battistelli, S., Muller, S., & Biggiogera, M. (2008) · Toxicology in Vitro · doi:10.1016/j.tiv.2008.09.006 · Cited by 50 · see citing works
Down the River: Glyphosate Use in Agriculture and Birth Outcomes of Surrounding Populations
Dias, M., Rocha, R., & Soares, R. R. (2023) · Review of Economic Studies · doi:10.1093/restud/rdad011 · Cited by 50 · 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
- Richard, S., Moslemi, S., Sipahutar, H., Benachour, N., & Seralini, G.-E.
- Affiliations
- Université de Caen Normandie (FR)
- ORCID
- Sipahutar, Herbert
- Venue
- Environmental Health Perspectives
- Publisher
- American Chemical Society (ACS)
- Published
- 2005-02-25
- Volume
- 113
- Issue
- 6
- Pages
- 716-720
- ISSN
- 0091-6765 (ISSN-L)
- 1552-9924
- PMC
- PMC1257596
- OpenAlex
- W2147373429
- Cited by
- 619
- References
- 40
- Citations by year
- 2026: 9 · 2025: 22 · 2024: 34 · 2023: 34 · 2022: 39 · 2021: 44 · 2020: 36 · 2019: 48 · 2018: 56 · 2017: 39 · 2016: 29 · 2015: 20 · 2014: 32 · 2013: 20 · 2012: 33
- FWCI
- 19.98
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- public-domain
- creativecommons.org/licenses/by/4.0/ (vor, 4690 d)
- Locations
- Environmental Health Perspectives (publishedVersion, public-domain)
- Europe PMC (PubMed Central) (publishedVersion, public-domain)
- PubMed Central (publishedVersion, public-domain)
- PubMed (publishedVersion)
- HAL (submittedVersion, cc-by)
- 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
- Physical Sciences › Environmental Science › Pollution › Pesticide and Herbicide Environmental Studies
- Keywords
- glyphosate, Roundup, herbicide toxicity, placental cells, JEG-3 cells, aromatase, estrogen synthesis, endocrine disruption, bioavailability, bioaccumulation, placental toxicity, genetically modified crops
- MeSH terms
- Glyphosate, Adjuvants, Pharmaceutic, Aromatase, Cell Survival, Drug Synergism, Female, Glycine, Herbicides, Humans, Microsomes, Oxidoreductases, RNA, Messenger, Gene Expression Regulation, Enzymologic, Cell Line, Tumor
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review