Ecotoxicological effects of the herbicide glyphosate in non-target aquatic species: Transcriptional responses in the mussel Mytilus galloprovincialis

Ackermann, 2014, The influence of glyphosate on the microbiota and production of botulinum neurotoxin during ruminal fermentation, Curr. Microbiol., 70, 374, 10.1007/s00284-014-0732-3 Annett, 2014, Impact of glyphosate and glyphosate-based herbicides on the freshwater environment, J. Appl. Toxicol., 10.1002/jat.2997 Avigliano, 2014, Effects of glyphosate on growth rate, metabolic rate and energy reserves of early juvenile crayfish, Cherax quadricarinatus M, Bull. Environ. Contam. Toxicol., 92, 631, 10.1007/s00128-014-1240-7 Avio, 2015, Pollutants bioavailability and toxicological risk from microplastics to marine mussels, Environ. Pollut., 198, 211, 10.1016/j.envpol.2014.12.021 Barbosa, 2001, Parkinsonism after glycine-derivate exposure, Mov. Disord., 16, 565, 10.1002/mds.1105 Barry, 1992 Battaglin, 2009, The occurrence of glyphosate, atrazine, and other pesticides in vernal pools and adjacent streams in Washington, DC, Maryland, Iowa, and Wyoming, 2005–2006, Environ. Monit. Assess., 155, 281, 10.1007/s10661-008-0435-y Benbrook, 2016, Trends in glyphosate herbicide use in the United States and globally, Environ. Sci. Eur., 28, 3, 10.1186/s12302-016-0070-0 Bevins, 2011, Paneth cells, antimicrobial peptides and maintenance of intestinal homeostasis, Nat. Rev. Microbiol., 9, 356, 10.1038/nrmicro2546 Boutet, 2008, Characterization of reproduction-specific genes in a marine bivalve mollusc: influence of maturation stage and sex on mRNA expression, Gene, 407, 130, 10.1016/j.gene.2007.10.005 Cattani, 2014, Mechanisms underlying the neurotoxicity induced by glyphosate-based herbicide in immature rat hippocampus: involvement of glutamate excitotoxicity, Toxicology, 320, 34, 10.1016/j.tox.2014.03.001 Cavalcante, 2010, Genotoxic effects of Roundup® on the fish Prochilodus lineatus, Mutat. Res. Genet. Toxicol. Environ. Mutagen, 695, 41 Çavaş, 2007, Detection of cytogenetic and DNA damage in peripheral erythrocytes of goldfish (Carassius auratus) exposed to a glyphosate formulation using the micronucleus test and the comet assay, Mutagenesis, 22, 263, 10.1093/mutage/gem012 Cerdeira, 2006, The current status and environmental impacts of glyphosate-resistant crops, J. Environ. Qual., 35, 1633, 10.2134/jeq2005.0378 Chen, 2013, GTPase of the immune-associated nucleotide-binding protein 5 (GIMAP5) regulates calcium influx in T-lymphocytes by promoting mitochondrial calcium accumulation, Biochem. J., 449, 353, 10.1042/BJ20120516 Chew, 2000, The LIM and SH3 domain-containing protein, lasp-1, may link the cAMP signaling pathway with dynamic membrane restructuring activities in ion transporting epithelia, J. Cell Sci., 113, 2035, 10.1242/jcs.113.11.2035 Clark, 2010, Insights into shell deposition in the Antarctic bivalve Laternula elliptica: gene discovery in the mantle transcriptome using 454 pyrosequencing, BMC Genom., 11, 362, 10.1186/1471-2164-11-362 Dallegrave, 2007, Pre- and postnatal toxicity of the commercial glyphosate formulation in Wistar rats, Arch. Toxicol., 81, 665, 10.1007/s00204-006-0170-5 De Castilhos Ghisi, 2013, Genotoxic effects of the herbicide Roundup® in the fish Corydoras paleatus (Jenyns 1842) after short-term, environmentally low concentration exposure, Environ. Monit. Assess., 185, 3201, 10.1007/s10661-012-2783-x de Liz Oliveira Cavalli, 2013, Roundup disrupts male reproductive functions by triggering calcium-mediated cell death in rat testis and Sertoli cells, Free Radic. Biol. Med., 65, 335, 10.1016/j.freeradbiomed.2013.06.043 Dennis, 2003, DAVID: database for annotation, visualization, and integrated discovery, Genome Biol., 4, R60, 10.1186/gb-2003-4-9-r60 Devine, 1993 Doğramacı, 2015, Glyphosate's impact on vegetative growth in leafy spurge identifies molecular processes and hormone cross-talk associated with increased branching, BMC Genom., 16, 395, 10.1186/s12864-015-1627-9 Dos Santos, 2017, A glyphosate-based herbicide induces histomorphological and protein expression changes in the liver of the female guppy Poecilia reticulata, Chemosphere, 168, 933, 10.1016/j.chemosphere.2016.10.116 Dutra, 2011, Effect of Roundup® (glyphosate formulation) in the energy metabolism and reproductive traits of Hyalella castroi (Crustacea, Amphipoda, Dogielinotidae), Ecotoxicology, 20, 255, 10.1007/s10646-010-0577-x Epelboin, 2015, Energy and antioxidant responses of Pacific oyster exposed to trace levels of pesticides, Chem. Res. Toxicol., 28, 1831, 10.1021/acs.chemrestox.5b00269 Feng, 2014, The machinery of macroautophagy, Cell Res., 24, 24, 10.1038/cr.2013.168 Fleeger, 2003, Indirect effects of contaminants in aquatic ecosystems, Sci. Total Environ., 10.1016/S0048-9697(03)00141-4 Franz, 1997 Ge, 2010, Rapid vacuolar sequestration: the horseweed glyphosate resistance mechanism, Pest Manag. Sci., 66, 345, 10.1002/ps.1911 George, 2013, Emptying of intracellular calcium pool and oxidative stress imbalance are associated with the glyphosate-induced proliferation in human skin keratinocytes HaCaT cells, ISRN Dermatol., 2013, 825180, 10.1155/2013/825180 Glusczak, 2007, Acute effects of glyphosate herbicide on metabolic and enzymatic parameters of silver catfish (Rhamdia quelen), Comp. Biochem. Physiol. C Toxicol. Pharmacol., 146, 519, 10.1016/j.cbpc.2007.06.004 Guilherme, 2010, European eel (Anguilla anguilla) genotoxic and pro-oxidant responses following short-term exposure to Roundup® - a glyphosate-based herbicide, Mutagenesis, 25, 523, 10.1093/mutage/geq038 Guilherme, 2012, Differential genotoxicity of Roundup® formulation and its constituents in blood cells of fish (Anguilla anguilla): considerations on chemical interactions and DNA damaging mechanisms, Ecotoxicology, 21, 1381, 10.1007/s10646-012-0892-5 Hao, 2004, Expression analysis of the human testis-specific serine/threonine kinase (TSSK) homologues. A TSSK member is present in the equatorial segment of human sperm, Mol. Hum. Reprod., 10, 433, 10.1093/molehr/gah052 Hediger, 2004, The ABCs of solute carriers: physiological, pathological and therapeutic implications of human membrane transport proteins, Pflug. Arch. Eur. J. Physiol., 10.1007/s00424-003-1192-y Hokanson, 2007, Alteration of estrogen-regulated gene expression in human cells induced by the agricultural and horticultural herbicide glyphosate, Hum. Exp. Toxicol., 26, 747, 10.1177/0960327107083453 Hou, 2011, Transcriptome sequencing and De Novo analysis for Yesso Scallop (Patinopecten yessoensis) using 454 GS FLX, PLoS One, 6, e21560, 10.1371/journal.pone.0021560 Howe, 2011, RNA-Seq analysis in MeV, Bioinformatics, 27, 3209, 10.1093/bioinformatics/btr490 Huang, 2008, Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources, Nat. Protoc., 4, 44, 10.1038/nprot.2008.211 ISPRA, 2016 Iummato, 2013, Evaluation of biochemical markers in the golden mussel Limnoperna fortunei exposed to glyphosate acid in outdoor microcosms, Ecotoxicol. Environ. Saf., 95, 123, 10.1016/j.ecoenv.2013.05.024 Kakkar, 1999, Calmodulin-dependent cyclic nucleotide phosphodiesterase (PDE1), Cell. Mol. Life Sci., 55, 1164, 10.1007/s000180050364 Kemp, 1983, The decline of submerged vascular plants in Upper Chesapeake Bay: summary of results concercning possible causes, Mar. Technol. Soc. J., 78 Kim, 2013, Mixtures of glyphosate and surfactant TN20 accelerate cell death via mitochondrial damage-induced apoptosis and necrosis, Toxicol. Vitro, 27, 191, 10.1016/j.tiv.2012.09.021 Lee, 2008, Lasp anchors the Drosophila male stem cell niche and mediates spermatid individualization, Mech. Dev., 125, 768, 10.1016/j.mod.2008.06.012 Matozzo, 2018, Ecotoxicological risk assessment for the herbicide glyphosate to non-target aquatic species: a case study with the mussel Mytilus galloprovincialis, Environ. Pollut., 233, 623, 10.1016/j.envpol.2017.10.100 McDowell, 2016, Multi-species protein similarity clustering reveals novel expanded immune gene families in the eastern oyster Crassostrea virginica, Fish Shellfish Immunol., 10.1016/j.fsi.2016.03.157 McDowell, 2014, Transcriptome of American oysters, Crassostrea virginica, in response to bacterial challenge: insights into potential mechanisms of disease resistance, PLoS One, 9, 10.1371/journal.pone.0105097 Mercurio, 2014, Glyphosate persistence in seawater, Mar. Pollut. Bull., 85, 385, 10.1016/j.marpolbul.2014.01.021 Mesnage, 2015, Transcriptome profile analysis reflects rat liver and kidney damage following chronic ultra-low dose Roundup exposure, Environ. Health, 14, 70, 10.1186/s12940-015-0056-1 Mezzelani, 2016, Transcriptional and cellular effects of Non-Steroidal Anti-Inflammatory Drugs (NSAIDs) in experimentally exposed mussels, Mytilus galloprovincialis, Aquat. Toxicol., 180, 306, 10.1016/j.aquatox.2016.10.006 Milan, 2013, Exploring the effects of seasonality and chemical pollution on the hepatopancreas transcriptome of the Manila clam, Mol. Ecol., 22, 2157, 10.1111/mec.12257 Milan, 2016, Can ecological history influence response to pollutants? Transcriptomomic analysis of Manila clam collected in different Venice lagoon areas and exposed to heavy metal, Aquat. Toxicol., 174, 123, 10.1016/j.aquatox.2016.02.024 Milan, 2015, Transcriptomic resources for environmental risk assessment: a case study in the Venice lagoon, Environ. Pollut., 197, 90, 10.1016/j.envpol.2014.12.005 Milan, 2013, Gene transcription and biomarker responses in the clam Ruditapes philippinarum after exposure to ibuprofen, Aquat. Toxicol., 126, 17, 10.1016/j.aquatox.2012.10.007 Modesto, 2010, Roundup® causes oxidative stress in liver and inhibits acetylcholinesterase in muscle and brain of the fish Prochilodus lineatus, Chemosphere, 78, 294, 10.1016/j.chemosphere.2009.10.047 Moreira, 2015, RNA-Seq in Mytilus galloprovincialis: comparative transcriptomics and expression profiles among different tissues, BMC Genom., 16, 728, 10.1186/s12864-015-1817-5 Motekaitis, 1985, Metal chelate formation by n-phosphonomethylglycine and related ligands, J. Coord. Chem., 14, 139, 10.1080/00958978508073900 Myers, 2016, Concerns over use of glyphosate-based herbicides and risks associated with exposures: a consensus statement, Environ. Health, 15, 19, 10.1186/s12940-016-0117-0 Nazıroğlu, 2012, Role of oxidative stress and Ca2+ signaling on molecular pathways of neuropathic pain in diabetes: focus on TRP channels, Neurochem. Res., 37, 2065, 10.1007/s11064-012-0850-x Nol, 2012, Shikimate leaf disc assay for early detection of glyphosate resistance in Conyza canadensis and relative transcript levels of EPSPS and ABC transporter genes, Weed Res., 52, 233, 10.1111/j.1365-3180.2012.00911.x Peixoto, 2005, Comparative effects of the Roundup and glyphosate on mitochondrial oxidative phosphorylation, Chemosphere, 61, 1115, 10.1016/j.chemosphere.2005.03.044 Robinson, 2009, edgeR: a Bioconductor package for differential expression analysis of digital gene expression data, Bioinformatics, 26, 139, 10.1093/bioinformatics/btp616 Romano, 2010, Prepubertal exposure to commercial formulation of the herbicide glyphosate alters testosterone levels and testicular morphology, Arch. Toxicol., 84, 309, 10.1007/s00204-009-0494-z Samsel, 2015, Glyphosate, pathways to modern diseases III: manganese, neurological diseases, and associated pathologies, Surg. Neurol. Int., 6, 45, 10.4103/2152-7806.153876 Serrano, 2017, GTPase of the immune-associated nucleotide protein 5 regulates the lysosomal calcium compartment in T lymphocytes, Front. Immunol., 8, 94, 10.3389/fimmu.2017.00094 Shehata, 2013, The effect of glyphosate on potential pathogens and beneficial members of poultry microbiota in vitro, Curr. Microbiol., 66, 350, 10.1007/s00284-012-0277-2 Skeff, 2015, Glyphosate and AMPA in the estuaries of the Baltic Sea method optimization and field study, Mar. Pollut. Bull., 100, 577, 10.1016/j.marpolbul.2015.08.015 Solomon, 2013, Effects of herbicides on fish, Fish Physiol., 33, 369, 10.1016/B978-0-12-398254-4.00007-8 Stewart, 2014, A survey of emerging contaminants in the estuarine receiving environment around Auckland, New Zealand, Sci. Total Environ., 468–469, 202, 10.1016/j.scitotenv.2013.08.039 Struger, 2008, Occurrence of glyphosate in surface waters of southern Ontario, Bull. Environ. Contam. Toxicol., 80, 378, 10.1007/s00128-008-9373-1 Takasuga, 2013, Phosphatidylinositol-3,5-bisphosphate: metabolism and physiological functions, J. Biochem., 10.1093/jb/mvt064 Tanguy, 2005, Molecular identification and expression study of differentially regulated genes in the Pacific oyster Crassostrea gigas in response to pesticide exposure, FEBS J., 272, 390, 10.1111/j.1742-4658.2004.04479.x Tuffnail, 2009, An environmental 1H NMR metabolomic study of the exposure of the marine mussel Mytilus edulis to atrazine, lindane, hypoxia and starvation, Metabolomics, 5, 33, 10.1007/s11306-008-0143-1 Ugarte, 2014, Interaction between glyphosate and mitochondrial succinate dehydrogenase, Comput. Theor. Chem., 1043, 54, 10.1016/j.comptc.2014.05.018 Undabeytia, 2002, FTIR study of glyphosate-copper complexes, J. Agric. Food Chem., 50, 1918, 10.1021/jf010988w Uren Webster, 2014, Effects of glyphosate and its formulation, roundup, on reproduction in zebrafish (Danio rerio), Environ. Sci. Technol., 48, 1271, 10.1021/es404258h Uren Webster, 2015, Global transcriptomic profiling demonstrates induction of oxidative stress and of compensatory cellular stress responses in brown trout exposed to glyphosate and Roundup, BMC Genom., 16, 32, 10.1186/s12864-015-1254-5 Vereecken, 2005, Mobility and leaching of glyphosate: a review, Pest Manag. Sci., 10.1002/ps.1122 Vergne, 2009, Control of autophagy initiation by phosphoinositide 3-phosphatase jumpy, EMBO J., 28, 2244, 10.1038/emboj.2009.159 Wang, 2011, Parkinsonism after chronic occupational exposure to glyphosate, Park. Relat. Disord., 10.1016/j.parkreldis.2011.02.003 Wang, 2016, A simple method for the determination of glyphosate and aminomethylphosphonic acid in seawater matrix with high performance liquid chromatography and fluorescence detection, Talanta, 161, 700, 10.1016/j.talanta.2016.09.023 Wu, 2011, Remote communication through solute carriers and ATP binding cassette drug transporter pathways: an update on the remote sensing and signaling hypothesis, Mol. Pharmacol., 79, 795, 10.1124/mol.110.070607 Yamaguchi, 1999, Stress-associated endoplasmic reticulum protein 1 (SERP1)/ribosome- associated membrane protein 4 (RAMP4) stabilizes membrane proteins during stress and facilitates subsequent glycosylation, J. Cell Biol., 147, 1195, 10.1083/jcb.147.6.1195 Young, 2015, CRISPR/Cas9-mediated rapid generation of multiple mouse lines identified Ccdc63 as essential for spermiogenesis, Int. J. Mol. Sci., 16, 24732, 10.3390/ijms161024732 Yuan, 2007, Non-target-site herbicide resistance: a family business, Trends Plant Sci., 10.1016/j.tplants.2006.11.001 Zhang, 2010, Some single-nucleotide polymorphisms of the TSSK2 gene may be associated with human spermatogenesis impairment, J. Androl., 31, 388, 10.2164/jandrol.109.008466