1-D and 2-D NMR metabolomics of earthworm responses to sub-lethal trifluralin and endosulfan exposure
Jimmy Yuk A , Myrna J. Simpson A and André J. Simpson A B
+ Author Affiliations
- Author Affiliations
A Department of Chemistry, University of Toronto, Scarborough College, 1265 Military Trail, Toronto, ON, M1C 1A4, Canada.
B Corresponding author. Email: andre.simpson@utoronto.ca
Environmental Chemistry 8(3) 281-294 https://doi.org/10.1071/EN11033
Submitted: 16 March 2011 Accepted: 5 May 2011 Published: 22 June 2011
Environmental context. Environmental metabolomics is an emerging field that examines the metabolic changes in organisms in response to potential environmental stressors. In this study, nuclear magnetic resonance spectroscopy is used to investigate earthworm metabolic responses to sub-lethal exposure of environmentally persistent pesticides. The study identifies two toxic modes of action elicited by the pesticides, and highlights the potential of metabolomics for the chemical assessment of persistent environmental contaminants.
Abstract. 1-D and 2-D nuclear magnetic resonance (NMR) spectroscopy is used to examine the metabolic response of the earthworm (Eisenia fetida) after contact test exposure to an organofluorine pesticide, trifluralin, and an organochlorine pesticide, endosulfan. Three sub-lethal concentrations were used for each pesticide (0.1, 0.5 and 1.0 mg cm–2 for trifluralin and 0.5, 1.0 and 2.0 μg cm–2 for endosulfan). Principal component analysis of the trifluralin and endosulfan NMR datasets showed separation between the unexposed and the exposed earthworm groups. Alanine, glycine, maltose and ATP were significant in the highest concentration (1.0 mg cm–2) for trifluralin-exposed earthworms and may result from a non-polar narcosis toxic mode of action (MOA). Leucine, phenylalanine, tryptophan, lysine, glutamate, valine, glycine, isoleucine, methionine, glutamine, alanine, maltose, glucose, meibiose, malate, fumarate and ATP were detected as significant for the two highest concentrations (1.0 and 2.0 μg cm–2) for endosulfan-exposed earthworms and a neurotoxic MOA is postulated. This study highlights the use of 1-D and 2-D metabolomics for understanding the biochemical response of environmental contaminants to model organisms such as earthworms.
Additional keywords: ecotoxicology, Eisenia fetida, metabolic profiling, metabonomics, principal component analysis.
References
[1] P. Jeschke, The unique role of halogen substituents in the design of modern agrochemicals. Pest Manag. Sci. 2010, 66, 10.| The unique role of halogen substituents in the design of modern agrochemicals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFGrsb3K&md5=667115e1f4ce8ec91528532eacb08270CAS | 19701961PubMed |
[2] C. L. Curl, R. A. Fenske, J. C. Kissel, J. H. Shirai, T. F. Moate, W. Griffith, G. Coronado, B. Thompson, Evaluation of take-home organophosphorus pesticide exposure among agricultural workers and their children. Environ. Health Perspect. 2002, 110, a787.
| Evaluation of take-home organophosphorus pesticide exposure among agricultural workers and their children.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtl2lsg%3D%3D&md5=fe6fd75e2e700c18d7f8c04899dd9daaCAS | 12460819PubMed |
[3] V. F. Garry, M. E. Harkins, L. L. Erickson, L. K. Long-Simpson, S. E. Holland, B. L. Burroughs, Birth defects, season of conception, and sex of children born to pesticide applicators living in the Red River Valley of Minnesota, USA. Environ. Health Perspect. 2002, 110, 441..
| 12060842PubMed |
[4] L. E. Gray,, J. Ostby, J. Furr, C. J. Wolf, C. Lambright, L. Parks, D. N. Veeramachaneni, V. Wilson, M. Price, A. Hotchkiss, E. Orlando, L. Guillette, Effects of environmental antiandrogens on reproductive development in experimental animals. Hum. Reprod. Update 2001, 7, 248.
| Effects of environmental antiandrogens on reproductive development in experimental animals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkt1Oktbc%3D&md5=c1e0dae5caf40dd5737f2468ac6a8c6bCAS | 11392371PubMed |
[5] P. Houeto, G. Bindoula, J. R. Hoffman, Ethylenebisdithiocarbamates and ethylenethiourea: possible human health hazards. Environ. Health Perspect. 1995, 103, 568.
| Ethylenebisdithiocarbamates and ethylenethiourea: possible human health hazards.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXmslCntbw%3D&md5=146eef357495aa717a74baa42e4e3073CAS | 7556009PubMed |
[6] N. Masutomi, M. Shibutani, H. Takagi, C. Uneyama, N. Takahashi, M. Hirose, Impact of dietary exposure to methoxychlor, genistein, or diisononyl phthalate during the perinatal period on the development of the rat endocrine/reproductive systems in later life. Toxicology 2003, 192, 149.
| Impact of dietary exposure to methoxychlor, genistein, or diisononyl phthalate during the perinatal period on the development of the rat endocrine/reproductive systems in later life.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXot1Kjt7s%3D&md5=b7b7626766e9b8fb2c22c3a8db7db0e6CAS | 14580783PubMed |
[7] D. Neubert, Vulnerability of the endocrine system to xenobiotic influence. Regul. Toxicol. Pharm. 1997, 26, 9.
| Vulnerability of the endocrine system to xenobiotic influence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXms12rtb4%3D&md5=b7fe13ab8294953e7cf32cc81137602fCAS |
[8] F. H. Pierik, A. Burdorf, J. A. Deddens, R. E. Juttmann, R. F. A. Weber, Maternal and paternal risk factors for cryptorchidism and hypospadias: a case-control study in newborn boys. Environ. Health Perspect. 2004, 112, 1570.
| Maternal and paternal risk factors for cryptorchidism and hypospadias: a case-control study in newborn boys.Crossref | GoogleScholarGoogle Scholar | 15531444PubMed |
[9] J. L. Rayner, C. Wood, S. E. Fenton, Exposure parameters necessary for delayed puberty and mammary gland development in Long-Evans rats exposed in utero to atrazine. Toxicol. Appl. Pharmacol. 2004, 195, 23.
| Exposure parameters necessary for delayed puberty and mammary gland development in Long-Evans rats exposed in utero to atrazine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVOksLs%3D&md5=d4cf9200c94b7dd6d84eef9ba23674e9CAS | 14962502PubMed |
[10] L. Ricceri, A. Venerosi, F. Capone, M. F. Cometa, P. Lorenzini, S. Fortuna, G. Calamandrei, Developmental neurotoxicity of organophosphorous pesticides: fetal and neonatal exposure to chlorpyrifos alters sex-specific behaviors at adulthood in mice. Toxicol. Sci. 2006, 93, 105.
| Developmental neurotoxicity of organophosphorous pesticides: fetal and neonatal exposure to chlorpyrifos alters sex-specific behaviors at adulthood in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xotl2ks7g%3D&md5=0bb745dd74236a482c415ab7918d5459CAS | 16760416PubMed |
[11] C. M. Villanueva, G. Durand, M. B. Coutté, C. Chevrier, S. Cordier, Atrazine in municipal drinking water and risk of low birth weight, preterm delivery, and small-for-gestational-age status. Occup. Environ. Med. 2005, 62, 400.
| Atrazine in municipal drinking water and risk of low birth weight, preterm delivery, and small-for-gestational-age status.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXls1aksL8%3D&md5=5925dd3f6de0fd5d89dacf3bda426bc2CAS | 15901888PubMed |
[12] R. M. Whyatt, D. Camann, F. P. Perera, V. A. Rauh, D. Tang, P. L. Kinney, R. Garfinkel, H. Andrews, L. Hoepner, D. B. Barr, Biomarkers in assessing residential insecticide exposures during pregnancy and effects on fetal growth. Toxicol. Appl. Pharmacol. 2005, 206, 246.
| Biomarkers in assessing residential insecticide exposures during pregnancy and effects on fetal growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlsVChsrg%3D&md5=1b0e4737774a773cd403c88bb8eb1343CAS | 15967215PubMed |
[13] K. Naumann, Influence of chlorine substituents on biological activity of chemicals: a review. Pest Manag. Sci. 2000, 56, 3.
| Influence of chlorine substituents on biological activity of chemicals: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhtFersLk%3D&md5=cd466189ce282544ea2a1e61d7b4ee61CAS |
[14] R. Jayashree, N. Vasudevan, Persistence and distribution of endosulfan under field condition. Environ. Monit. Assess. 2007, 131, 475.
| Persistence and distribution of endosulfan under field condition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmvVejsrY%3D&md5=91ae7ab1e7d6d5c86367925385bf7152CAS | 17171258PubMed |
[15] B. D. Key, R. D. Howell, C. S. Criddle, Fluorinated organics in the biosphere. Environ. Sci. Technol. 1997, 31, 2445.
| Fluorinated organics in the biosphere.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXks1Cqsb0%3D&md5=03a8f8fe9d63d82b1d7236810657f2bfCAS |
[16] E. Ebert, K. H. Leist, R. Hack, G. Ehling, Toxicology and hazard potential of trifluralin. Food Chem. Toxicol. 1992, 30, 1031.
| Toxicology and hazard potential of trifluralin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXpsFKgsg%3D%3D&md5=48c74183e9d339c6929028d854ac9811CAS | 1473797PubMed |
[17] D. Kang, S. K. Park, L. Beane-Freeman, C. F. Lynch, C. E. Knott, D. P. Sandler, J. A. Hoppin, M. Dosemeci, J. Coble, J. Lubin, A. Blair, M. Alavanja, Cancer incidence among pesticide applicators exposed to trifluralin in the Agricultural Health Study. Environ. Res. 2008, 107, 271.
| Cancer incidence among pesticide applicators exposed to trifluralin in the Agricultural Health Study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXlslymsbg%3D&md5=e80059e388e73fc6d4fcaaee5327323eCAS | 18342850PubMed |
[18] S. Könen, T. Cavas, Genotoxicity testing of the herbicide trifluralin and its commercial formulation treflan using the piscine micronucleus test. Environ. Mol. Mutagen. 2008, 49, 434.
| Genotoxicity testing of the herbicide trifluralin and its commercial formulation treflan using the piscine micronucleus test.Crossref | GoogleScholarGoogle Scholar | 18449930PubMed |
[19] O. Tiryaki, Ü. Yücel, G. Sezen, Biodegradation of trifluralin in Harran soil. J. Environ. Sci. Health B 2004, 39, 747.
| Biodegradation of trifluralin in Harran soil.Crossref | GoogleScholarGoogle Scholar | 15620083PubMed |
[20] C. Turgut, O. Erdogan, D. Ates, C. Gokbulut, T. J. Cutright, Persistence and behavior of pesticides in cotton production in Turkish soils. Environ. Monit. Assess. 2010, 162, 201.
| Persistence and behavior of pesticides in cotton production in Turkish soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhs1amu7g%3D&md5=181f1ab8e7d2db863ffe56a3fa8be3d3CAS | 19242811PubMed |
[21] J. G. Bundy, J. K. Sidhu, F. Rana, D. J. Spurgeon, C. Svendsen, J. F. Wren, S. R. Stürzenbaum, A. J. Morgan, P. Kille, ‘Systems toxicology’ approach identifies coordinated metabolic responses to copper in a terrestrial non-model invertebrate, the earthworm Lumbricus rubellus. BMC Biol. 2008, 6, 25.
| ‘Systems toxicology’ approach identifies coordinated metabolic responses to copper in a terrestrial non-model invertebrate, the earthworm Lumbricus rubellus.Crossref | GoogleScholarGoogle Scholar | 18522721PubMed |
[22] M. Kroeger, How omics technologies can contribute to the ‘3R’ principles by introducing new strategies in animal testing. Trends Biotechnol. 2006, 24, 343.
| How omics technologies can contribute to the ‘3R’ principles by introducing new strategies in animal testing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XntVymtLw%3D&md5=6f742ff1a4316dbff408c864a7f74a35CAS | 16782220PubMed |
[23] J. O. T. Gibb, C. Svendsen, J. M. Weeks, J. K. Nicholson, H-1 NMR spectroscopic investigations of tissue metabolite biomarker response to CuII exposure in terrestrial invertebrates: identification of free histidine as a novel biomarker of exposure to copper in earthworms. Biomarkers 1997, 2, 295.
| H-1 NMR spectroscopic investigations of tissue metabolite biomarker response to CuII exposure in terrestrial invertebrates: identification of free histidine as a novel biomarker of exposure to copper in earthworms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXmslShs7o%3D&md5=5248d4219bf5a78794a24b610762903fCAS |
[24] M. J. Simpson, J. R. McKelvie, Environmental metabolomics: new insights into earthworm ecotoxicity and contaminant bioavailability in soil. Anal. Bioanal. Chem. 2009, 394, 137.
| Environmental metabolomics: new insights into earthworm ecotoxicity and contaminant bioavailability in soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFWisb0%3D&md5=b57bc5aa80a551588927c245e903630bCAS | 19194697PubMed |
[25] N. W. Xiao, Y. Song, F. Ge, X. H. Liu, Z. Y. Ou-Yang, Biomarkers responses of the earthworm Eisenia fetida to acetochlor exposure in OECD soil. Chemosphere 2006, 65, 907.
| Biomarkers responses of the earthworm Eisenia fetida to acetochlor exposure in OECD soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XpsVKkuro%3D&md5=84667e972f081fdb69932f53f1211d4bCAS | 16682071PubMed |
[26] G. C. Goats, C. A. Edwards, The prediction of field toxicity of chemicals to earthworms by laboratory methods, in Earthworms in Waste and Environmental Assessment (Eds C. A. Edwards, E. F. Neuhauser) 1988, pp. 283–294 (Academic Publishing: The Hague, the Netherlands).
[27] S. A. E. Brown, J. R. McKelvie, A. J. Simpson, M. J. Simpson, 1H NMR metabolomics of earthworm exposure to sub-lethal concentrations of phenanthrene in soil. Environ. Pollut. 2010, 158, 2117.
| 1H NMR metabolomics of earthworm exposure to sub-lethal concentrations of phenanthrene in soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlvVent7w%3D&md5=040d4c79d9b40051a63f9b35826e7b24CAS | 20338676PubMed |
[28] S. A. E. Brown, A. J. Simpson, M. J. Simpson, 1H NMR metabolomics of earthworm responses to sub-lethal PAH exposure. Environ. Chem. 2009, 6, 432.
| 1H NMR metabolomics of earthworm responses to sub-lethal PAH exposure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFSkurnK&md5=ce1e72442ee2dcc90157930d537ca8a4CAS |
[29] J. G. Bundy, H. C. Keun, J. K. Sidhu, D. J. Spurgeon, C. Svendsen, P. Kille, A. J. Morgan, Metabolic profile biomarkers of metal contamination in a sentinel terrestrial species are applicable across multiple sites. Environ. Sci. Technol. 2007, 41, 4458.
| Metabolic profile biomarkers of metal contamination in a sentinel terrestrial species are applicable across multiple sites.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXltVKqs70%3D&md5=676a6197a402726b6f710004b7bef7f8CAS | 17626452PubMed |
[30] J. G. Bundy, D. J. Spurgeon, C. Svendsen, P. K. Hankard, M. A. Warne, D. Osborn, J. C. Lindon, J. K. Nicholson, Environmental metabonomics: applying combination biomarker analysis in earthworms at a metal contaminated site. Ecotoxicology 2004, 13, 797.
| Environmental metabonomics: applying combination biomarker analysis in earthworms at a metal contaminated site.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhslyrs7o%3D&md5=95873eae73546df65733e9f724c0319dCAS | 15736850PubMed |
[31] J. G. Bundy, D. J. Spurgeon, C. Svendsen, P. K. Hankard, D. Osborn, J. C. Lindon, J. K. Nicholson, Earthworm species of the genus Eisenia can be phenotypically differentiated by metabolic profiling. FEBS Lett. 2002, 521, 115.
| Earthworm species of the genus Eisenia can be phenotypically differentiated by metabolic profiling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XksVahsrw%3D&md5=65ad70fd9269c51a1044678567dc378eCAS | 12067738PubMed |
[32] J. G. Bundy, E. M. Lenz, D. Osborn, J. M. Weeks, J. C. Lindon, J. K. Nicholson, Metabolism of 4-fluoroaniline and 4-fluorobiphenyl in the earthworm Eisenia veneta characterized by high-resolution NMR spectroscopy with directly coupled HPLC-NMR and HPLC-MS. Xenobiotica 2002, 32, 479.
| Metabolism of 4-fluoroaniline and 4-fluorobiphenyl in the earthworm Eisenia veneta characterized by high-resolution NMR spectroscopy with directly coupled HPLC-NMR and HPLC-MS.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlsVCltr8%3D&md5=51eb21e8aaa974b2b4d24957d5bb5282CAS | 12160481PubMed |
[33] M. R. Viant, J. G. Bundy, C. A. Pincetich, J. S. de Ropp, R. S. Tjeerdema, NMR-derived developmental metabolic trajectories: an approach for visualizing the toxic actions of trichloroethylene during embryogenesis. Metabolomics 2005, 1, 149.
| NMR-derived developmental metabolic trajectories: an approach for visualizing the toxic actions of trichloroethylene during embryogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1SmsrjE&md5=1a48125c3ed554b0fc8b1e243c54947dCAS |
[34] J. Yuk, J. R. McKelvie, M. J. Simpson, M. Spraul, A. J. Simpson, Comparison of 1-D and 2-D NMR techniques for screening earthworm responses to sub-lethal endosulfan exposure. Environ. Chem. 2010, 7, 524.
| Comparison of 1-D and 2-D NMR techniques for screening earthworm responses to sub-lethal endosulfan exposure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFGrsA%3D%3D&md5=7d9b7bb7dbc1b0ff79e37a3928857114CAS |
[35] Earthworm, Acute Toxicity Tests, Test No, 207, in OECD Guidelines for the Testing of Chemicals 1984, vol. 1, no. 2 (Organisation for Economic Co-operation and Development: Paris).
[36] P. J. Edwards, J. M. Coulson, Choice of earthworm species for laboratory tests, in Ecotoxicology of Earthworms (Eds P. W. Greig-Smith, H. Becker, P. J. Edwards, F. Heimbach) 1992, pp. 36–43. (Intercept) Available at http://www.scopus.com/inward/record.url?eid=2-s2.0-0027064096&partnerID=40 [Verified 8 June 2011].
[37] C. A. Edwards, P. J. Bohlen, The effects of toxic chemicals on earthworms. Rev. Environ. Contam. Toxicol. 1992, 125, 23..
[38] J. G. Bundy, M. P. Davey, M. R. Viant, Environmental metabolomics: a critical review and future perspectives. Metabolomics 2009, 5, 3.
| Environmental metabolomics: a critical review and future perspectives.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXisFSls7k%3D&md5=f8528d88bc47af243aadb4abbb08cdbbCAS |
[39] J. R. McKelvie, D. M. Wolfe, M. Celejewski, A. J. Simpson, M. J. Simpson, Correlations of Eisenia fetida metabolic responses to extractable phenanthrene concentrations through time. Environ. Pollut. 2010, 158, 2150.
| Correlations of Eisenia fetida metabolic responses to extractable phenanthrene concentrations through time.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlvVent7g%3D&md5=ffa2cdd62741e9824cf9a05c6686ccdbCAS | 20338675PubMed |
[40] T. B. Schock, D. A. Stancyk, L. Thibodeaux, K. G. Burnett, L. E. Burnett, A. F. B. Boroujerdi, D. W. Bearden, Metabolomic analysis of Atlantic blue crab, Callinectes sapidus, hemolymph following oxidative stress. Metabolomics 2010, 6, 250.
| Metabolomic analysis of Atlantic blue crab, Callinectes sapidus, hemolymph following oxidative stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlsFSmu7g%3D&md5=204aa3e4383560f07550f940bc46ec20CAS |
[41] S. A. E. Brown, A. J. Simpson, M. J. Simpson, Evaluation of sample preparation methods for nuclear magnetic resonance metabolic profiling studies with Eisenia fetida. Environ. Toxicol. Chem. 2008, 27, 828.
| Evaluation of sample preparation methods for nuclear magnetic resonance metabolic profiling studies with Eisenia fetida.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXktFGntLg%3D&md5=f8467651471cd45df8ab5ab4160d6142CAS | 18333692PubMed |
[42] F. Heimbach, A comparison of laboratory methods for toxicity testing with earthworms, in Earthworms in Waste and Environmental Management (Eds C. A. Edwards, E. F. Neuhauser) 1988, pp. 329–335 (Academic Publishing: The Hague, the Netherlands).
[43] B. L. Roberts, H. W. Dorough, Relative toxicities of chemicals to the earthworm Eisenia foetida. Environ. Toxicol. Chem. 1984, 3, 67..
[44] A. J. Simpson, S. A. Brown, Purge NMR: effective and easy solvent suppression. J. Magn. Reson. 2005, 175, 340.
| Purge NMR: effective and easy solvent suppression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXls1ygsrY%3D&md5=67f12730c50ea4ae54303eca7e7a36cfCAS | 15964227PubMed |
[45] D. R. Ekman, Q. Teng, D. L. Villeneuve, M. D. Kahl, K. M. Jensen, E. J. Durhan, G. T. Ankley, T. W. Collette, Investigating compensation and recovery of fathead minnow (Pimephales promelas) exposed to 17α-ethynylestradiol with metabolite profiling. Environ. Sci. Technol. 2008, 42, 4188.
| Investigating compensation and recovery of fathead minnow (Pimephales promelas) exposed to 17α-ethynylestradiol with metabolite profiling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXlt1Sks7o%3D&md5=ad652146af4f861f9db0b30febc09dfdCAS | 18589986PubMed |
[46] D. R. Ekman, Q. Teng, D. L. Villeneuve, M. D. Kahl, K. M. Jensen, E. J. Durhan, G. T. Ankley, T. W. Collette, Profiling lipid metabolites yields unique information on sex- and time-dependent responses of fathead minnows (Pimephales promelas) exposed to 17α-ethynylestradiol. Metabolomics 2009, 5, 22.
| Profiling lipid metabolites yields unique information on sex- and time-dependent responses of fathead minnows (Pimephales promelas) exposed to 17α-ethynylestradiol.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXisFSls7Y%3D&md5=c8efcf49af259f8012808abba5505f65CAS |
[47] P. J. Brown, S. M. Long, D. J. Spurgeon, C. Svendsen, P. K. Hankard, Toxicological and biochemical responses of the earthworm Lumbricus rubellus to pyrene, a non-carcinogenic polycyclic aromatic hydrocarbon. Chemosphere 2004, 57, 1675.
| Toxicological and biochemical responses of the earthworm Lumbricus rubellus to pyrene, a non-carcinogenic polycyclic aromatic hydrocarbon.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXpt1arsrg%3D&md5=d5fa0315324825ee1766746b27f1161dCAS | 15519413PubMed |
[48] M. H. Depledge, M. C. Fossi, The role of biomarkers in environmental assessment. (2) Invertebrates. Ecotoxicology 1994, 3, 161.
| The role of biomarkers in environmental assessment. (2) Invertebrates.Crossref | GoogleScholarGoogle Scholar |
[49] H. M. Parsons, D. R. Ekman, T. W. Collette, M. R. Viant, Spectral relative standard deviation: a practical benchmark in metabolomics. Analyst (Lond.) 2009, 134, 478.
| Spectral relative standard deviation: a practical benchmark in metabolomics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXitlGmt78%3D&md5=2375193357ab142c3aed8ccbcef1cbb9CAS |
[50] B. A. Mizock, Alterations in carbohydrate metabolism during stress: a review of the literature. Am. J. Med. 1995, 98, 75.
| Alterations in carbohydrate metabolism during stress: a review of the literature.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2M7is1Wlsw%3D%3D&md5=9b28ebd2dd85b36eb9feaad9e1266447CAS | 7825623PubMed |
[51] E. Ben-Izhak Monselise, A. H. Parola, D. Kost, Low-frequency electromagnetic fields induce a stress effect upon higher plants, as evident by the universal stress signal, alanine. Biochem. Biophys. Res. Commun. 2003, 302, 427.
| Low-frequency electromagnetic fields induce a stress effect upon higher plants, as evident by the universal stress signal, alanine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhsVCgsrg%3D&md5=b88dba7bfb12228593350bc834cf4096CAS | 12604366PubMed |
[52] S. Wera, E. De Schrijver, I. Geyskens, S. Nwaka, J. M. Thevelein, Opposite roles of trehalase activity in heat-shock recovery and heat-shock survival in Saccharomyces cerevisiae. Biochem. J. 1999, 343, 621.
| Opposite roles of trehalase activity in heat-shock recovery and heat-shock survival in Saccharomyces cerevisiae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXntlymtbc%3D&md5=0410efe4bc362ac301a47b7f05696346CAS | 10527941PubMed |
[53] J. J. Blum, Effects of osmotic stress on metabolism, shape, and amino acid content of Leishmania. Biol. Cell 1996, 87, 9.
| Effects of osmotic stress on metabolism, shape, and amino acid content of Leishmania.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhsVOgu7c%3D&md5=e841449a17859eed0f53cb22386d447fCAS | 9026223PubMed |
[54] W. Görner, E. Durchschlag, M. T. Martinez-Pastor, F. Estruch, G. Ammerer, B. Hamilton, H. Ruis, C. Schüller, Nuclear localization of the C2H2 zinc finger protein Msn2p is regulated by stress and protein kinase A activity. Genes Dev. 1998, 12, 586.
| Nuclear localization of the C2H2 zinc finger protein Msn2p is regulated by stress and protein kinase A activity.Crossref | GoogleScholarGoogle Scholar | 9472026PubMed |
[55] D. Ang, K. Liberek, D. Skowyra, M. Zylicz, C. Georgopoulos, Biological role and regulation of the universally conserved heat shock proteins. J. Biol. Chem. 1991, 266, 24233..
| 1761528PubMed |
[56] H. R. B. Pelham, Speculations on the functions of the major heat shock and glucose-regulated proteins. Cell 1986, 46, 959.
| Speculations on the functions of the major heat shock and glucose-regulated proteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28XmtVKlsbg%3D&md5=53ba7025f5a9223357508ebe7cc50f96CAS | 2944601PubMed |
[57] D. Lanneau, G. Wettstein, P. Bonniaud, C. Garrido, Heat shock proteins: cell protection through protein triage. ScientificWorldJournal 2010, 10, 1543..
| 20694452PubMed |
[58] J. McKelvie, J. Yuk, Y. Xu, A. Simpson, M. Simpson, 1H NMR and GC/MS metabolomics of earthworm responses to sub-lethal DDT and endosulfan exposure. Metabolomics 2009, 5, 84.
| 1H NMR and GC/MS metabolomics of earthworm responses to sub-lethal DDT and endosulfan exposure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXisFSls7g%3D&md5=1688328b4ca9fcb0b33fd8ef8867b01bCAS |
[59] I. Nissim, M. Hardy, J. Pleasure, B. States, A mechanism of glycine and alanine cytoprotective action: stimulation of stress-induced HSP70 mRNA. Kidney Int. 1992, 42, 775.
| A mechanism of glycine and alanine cytoprotective action: stimulation of stress-induced HSP70 mRNA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXhvF2hsQ%3D%3D&md5=c6d64244d0a9de09f0a3dab1407616b1CAS | 1405356PubMed |
[60] J. M. Weinberg, M. A. Venkatachalam, R. Garzoquintero, N. F. Roeser, J. A. Davis, Structural requirements for protection by small amino acids against hypoxic injury in kidney proximal tubules. FASEB J. 1990, 4, 3347..
| 2253849PubMed |
[61] J. Ahlers, I. Cascorbi, M. Foret, A. Gies, M. Kohler, W. Pauli, E. Rosick, Interaction with functional membrane proteins – a common mechanism of toxicity for lipophilic environmental chemicals? Comp. Biochem. Physiol. C Pharmacol. Toxicol. Endocrinol. 1991, 100, 111.
| Interaction with functional membrane proteins – a common mechanism of toxicity for lipophilic environmental chemicals?Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3Mzit12rsQ%3D%3D&md5=eace6949086150358352e16b2111257bCAS |
[62] N. P. Franks, W. R. Lieb, Is membrane expansion relevant to anaesthesia? Nature 1981, 292, 248.
| Is membrane expansion relevant to anaesthesia?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXmtFGht7o%3D&md5=1dd960d6bcf87742f32ea143c5feb4f3CAS | 7254317PubMed |
[63] T. A. A. Rocha-e-Silva, B. Farley, K. O. Nonaka, H. S. Selistre-de-Araujo, F. T. Rantin, I. A. Degterev, Spectral characteristics of a compound altering cytochrome P450 spectra from vertebrate microsomes suggest that it is a functional protein. Comp. Biochem. Physiol. C: Toxicol. Pharmacol. 2001, 130, 53.
| Spectral characteristics of a compound altering cytochrome P450 spectra from vertebrate microsomes suggest that it is a functional protein.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MvpsFelsg%3D%3D&md5=2e07e9ac56a0f2a85d66858764d1d0cbCAS | 11544143PubMed |
[64] M. Saint-Denis, J. F. Narbonne, C. Arnaud, E. Thybaud, D. Ribera, Biochemical responses of the earthworm Eisenia fetida andrei exposed to contaminated artificial soil: effects of benzo(a)pyrene. Soil Biol. Biochem. 1999, 31, 1837.
| Biochemical responses of the earthworm Eisenia fetida andrei exposed to contaminated artificial soil: effects of benzo(a)pyrene.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmslGjtLs%3D&md5=b3fde7c598787852b3aab0d06ca1471bCAS |
[65] M. E. Hahn, The aryl hydrocarbon receptor: a comparative perspective. Comp. Biochem. Physiol. C Pharmacol. Toxicol. Endocrinol. 1998, 121, 23.
| The aryl hydrocarbon receptor: a comparative perspective.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1M7jvVeqtA%3D%3D&md5=db75310b925331f45450f3269510b840CAS | 9972449PubMed |
[66] W. Zhang, Y. F. Song, P. Gong, T. H. Sun, Q. X. Zhou, M. Liu, Earthworm cytochrome P450 determination and application as a biomarker for diagnosing PAH exposure. J. Environ. Monit. 2006, 8, 963.
| Earthworm cytochrome P450 determination and application as a biomarker for diagnosing PAH exposure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XovFKlt7Y%3D&md5=b573a277fda5fa52daf2a21687de8587CAS | 16951757PubMed |
[67] R. K. Achazi, C. Flenner, D. R. Livingstone, L. D. Peters, K. Schaub, E. Scheiwe, Cytochrome P450 and dependent activities in unexposed and PAH-exposed terrestrial annelids. Comp. Biochem. Physiol. C Pharmacol. Toxicol. Endocrinol. 1998, 121, 339.
| Cytochrome P450 and dependent activities in unexposed and PAH-exposed terrestrial annelids.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1M7jvVChsQ%3D%3D&md5=e8e5db2f0c114424cb2f6be627e04db4CAS | 9972476PubMed |
[68] J. Bierkens, G. Klein, P. Corbisier, R. Van Den Heuvel, L. Verschaeve, R. Weltens, G. Schoeters, Comparative sensitivity of 20 bioassays for soil quality. Chemosphere 1998, 37, 2935.
| Comparative sensitivity of 20 bioassays for soil quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXns1Snt74%3D&md5=b9645c272c14d92cfbe26955d6cbed92CAS | 9839407PubMed |
[69] K. L. Behar, D. L. Rothman, In vivo nuclear magnetic resonance studies of glutamate-γ-aminobutyric acid–glutamine cycling in rodent and human cortex: the central role of glutamine. J. Nutr. 2001, 131, 2498S..
| 11533301PubMed |
[70] K. Ukena, T. Oumi, O. Matsushima, T. Ikeda, T. Fujita, H. Minakata, K. Nomoto, Effects of annetocin, an oxytocin-related peptide isolated from the earthworm Eisenia foetida, and some putative neurotransmitters on gut motility of the earthworm. J. Exp. Zool. 1995, 272, 184.
| Effects of annetocin, an oxytocin-related peptide isolated from the earthworm Eisenia foetida, and some putative neurotransmitters on gut motility of the earthworm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXnt1eru78%3D&md5=7929cc78c280375349a40a7a50180d54CAS | 7790842PubMed |
[71] C. Vale, E. Fonfra, J. Bujons, A. Messeguer, E. Rodrguez-Farr, C. Suol, The organochlorine pesticides γ-hexachlorocyclohexane (lindane), α-endosulfan and dieldrin differentially interact with GABA and glycine-gated chloride channels in primary cultures of cerebellar granule cells. Neuroscience 2003, 117, 397.
| The organochlorine pesticides γ-hexachlorocyclohexane (lindane), α-endosulfan and dieldrin differentially interact with GABA and glycine-gated chloride channels in primary cultures of cerebellar granule cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhsVChs7c%3D&md5=808820a2095de32cbd5732845791c03bCAS | 12614680PubMed |
[72] S. Ribeiro, J. P. Sousa, A. J. A. Nogueira, A. M. V. M. Soares, Effect of endosulfan and parathion on energy reserves and physiological parameters of the terrestrial isopod Porcellio dilatatus. Ecotoxicol. Environ. Saf. 2001, 49, 131.
| Effect of endosulfan and parathion on energy reserves and physiological parameters of the terrestrial isopod Porcellio dilatatus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjvFKjtLs%3D&md5=28bb76bb5493b5a4b4b5aed925c310d6CAS | 11386726PubMed |
[73] O. A. H. Jones, D. J. Spurgeon, C. Svendsen, J. L. Griffin, A metabolomics based approach to assessing the toxicity of the polyaromatic hydrocarbon pyrene to the earthworm Lumbricus rubellus. Chemosphere 2008, 71, 601.
| A metabolomics based approach to assessing the toxicity of the polyaromatic hydrocarbon pyrene to the earthworm Lumbricus rubellus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXisVWjsbY%3D&md5=7445330843c7108859a9b535664969dfCAS | 17928029PubMed |
[74] C. D. Drewes, E. P. Vining, In vivo neurotoxic effects of dieldrin on giant nerve fibers and escape reflex function in the earthworm, Eisenia foetida. Pestic. Biochem. Physiol. 1984, 22, 93.
| In vivo neurotoxic effects of dieldrin on giant nerve fibers and escape reflex function in the earthworm, Eisenia foetida.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXltVGntr8%3D&md5=775ada6b77d0b5e4e16f9e914e04490cCAS |
[75] W. Liu, L. S. Zhu, J. Wang, J. H. Wang, H. Xie, Y. Song, Assessment of the genotoxicity of endosulfan in earthworm and white clover plants using the comet assay. Arch. Environ. Contam. Toxicol. 2009, 56, 742.
| Assessment of the genotoxicity of endosulfan in earthworm and white clover plants using the comet assay.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXktFCkurY%3D&md5=673a1fde74334064f92b7096e4eea785CAS | 19306081PubMed |
[76] Y. Y. Mosleh, S. Paris-Palacios, M. Couderchet, G. Vernet, Acute and sublethal effects of two insecticides on earthworms (Lumbricus terrestris L.) under laboratory conditions. Environ. Toxicol. 2003, 18, 1.
| Acute and sublethal effects of two insecticides on earthworms (Lumbricus terrestris L.) under laboratory conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtFKjsLc%3D&md5=67f840669273a3a24eb9a5b6c050c319CAS | 12539138PubMed |
[77] J. Weber, C. J. Halsall, D. Muir, C. Teixeira, J. Small, K. Solomon, M. Hermanson, H. Hung, T. Bidleman, Endosulfan, a global pesticide: a review of its fate in the environment and occurrence in the Arctic. Sci. Total Environ. 2010, 408, 2966.
| Endosulfan, a global pesticide: a review of its fate in the environment and occurrence in the Arctic.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXntV2isLo%3D&md5=d424d9336d48cd27f8e330ff12ebb4ccCAS | 19939436PubMed |
[78] H. Li, G. Sheng, W. Sheng, O. Xu, Uptake of trifluralin and lindane from water by ryegrass. Chemosphere 2002, 48, 335.
| Uptake of trifluralin and lindane from water by ryegrass.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XktVCnt7Y%3D&md5=0b882dd5b0c029599e076964e02a6e17CAS | 12146622PubMed |
[79] W. J. Doucette, Quantitative structure-activity relationships for predicting soil-sediment sorption coefficients for organic chemicals. Environ. Toxicol. Chem. 2003, 22, 1771.
| Quantitative structure-activity relationships for predicting soil-sediment sorption coefficients for organic chemicals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXotF2gsrk%3D&md5=70347898037af220d6eb13f69e86725eCAS | 12924577PubMed |
