Skip to main content

Invertebrate Model Species in AOP Development

  • Chapter
  • First Online:

Abstract

In this chapter, we present the use of invertebrate model species in the development of adverse outcome pathways (AOPs), its challenges, and the current state of invertebrate toxicity studies. Invertebrates can contribute significantly towards the development of robust AOPs, providing many advantages over the use of vertebrate species. This includes a generally shorter life cycle allowing for chronic and full life cycle toxicity tests, and a wide array of powerful molecular genetic tools such as genome sequences, genomic engineering including gene knock-outs, and comprehensive bioinformatics databases. Currently, the most robustly developed invertebrate model species for toxicity testing include Daphnia, Caenorhabditis elegans, plus members of the Drosophila genus. The potential use of these and other invertebrate organisms for assessing chemical risk for most animals (including vertebrate species) is evaluated via a comparative phylogenetic approach to ecotoxicological testing, seeking to discover the evolutionary origins and distribution of toxicity pathways across the internal branches of the animal phylogeny. Comparative –omics data from cellular and developmental studies suggest a high degree of conservation in regulatory pathways in fly, worm and human. By comparing –omics studies between vertebrates and invertebrate species in toxicology, we begin to also discover coherence in pathway level responses, indicating potentially numerous overlapping responses to specific stressors, even across species that have different physiologies and ecological niches. At present, only a small number of invertebrate AOPs are informed by evidence. Perhaps the most robust of these is the Acetylcholinesterase inhibition (AChE) AOP for pesticides. We present a case study of using the AOP framework for risk assessment and discuss how the use of models, such as those using Dynamic Energy Budget theory linked to populations, can enhance the use of AOPs for understanding and predicting chemical risk.

This is a preview of subscription content, log in via an institution.

References

  • Abdullah AR, Kumar A, Chapman JC (1994) Inhibition of acetylcholinesterase in the Australian freshwater shrimp (Parataya australiensis) by profenofos. Environ Toxicol Chem 13(11):1861–1866

    Article  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215(3):403–410

    Article  PubMed  CAS  Google Scholar 

  • Ankley GT, Bennett RS, Erickson RJ, Hoff DJ, Hornung MW, Johnson RD, Mount DR, Nichols JW, Russom CL, Schmieder PK, Serrano JA, Tietge JE, Villeneuve DL (2010) Adverse outcome pathways: a conceptual framework to support ecotoxicology research and risk assessment. Environ Toxicol Chem 29(3):730–741

    Article  PubMed  CAS  Google Scholar 

  • Ankley GT, Brooks BW, Huggett DB, Sumpter JP (2007) Repeating history: pharmaceuticals in the environment. Environ Sci Technol 41(24):8211–8217

    Article  PubMed  CAS  Google Scholar 

  • Ankley GT, Miracle A, Perkins EJ, Daston GP (eds) (2008) Genomics in regulatory ecotoxicology: applications and challenges. CRC Press, Boca Raton

    Google Scholar 

  • Armitage JM, Wania F, Arnot JA (2014) Application of mass balance models and the chemical activity concept to facilitate the use of in vitro toxicity data for risk assessment. Environ Sci Technol 48:9770–9779

    Article  PubMed  CAS  Google Scholar 

  • Barata C, Markich SJ, Baird DJ, Taylor G, Soares AM (2002) Genetic variability in sublethal tolerance to mixtures of cadmium and zinc in clones of Daphnia magna Straus. Aquat Toxicol 60(1–2):85–99

    Article  PubMed  CAS  Google Scholar 

  • Barata C, Solayan A, Porte C (2004) Role of B-esterases in assessing toxicity of organophosphorus (chlorpyrifos, malathion) and carbamate (carbofuran) pesticides to Daphnia magna. Aquat Toxicol 66(2):125–139

    Article  PubMed  CAS  Google Scholar 

  • Basu N (2015) Applications and implications of neurochemical biomarkers in environmental toxicology. Environ Toxicol Chem 34(1):22–29

    Article  PubMed  CAS  Google Scholar 

  • Bianco K, Yusseppone MS, Otero S, Luquet C, Rios de Molina MC, Kristoff G (2013) Cholinesterases and neurotoxicity as highly sensitive biomarkers for an organophosphate insecticide in freshwater gastropod (Chilina gibbosa) with low sensitivity carboxylesterases. Aquat Toxicol 144–145:26–35

    Article  PubMed  CAS  Google Scholar 

  • Bocquené G, Galgani F (1991) Acetylcholinesterase activity in the common prawn (Palaemon serratus) contaminated by carbaryl and phosalone: choice of a method for detection of effects. Ecotoxicol Environ Saf 22(3):337–344

    Article  PubMed  Google Scholar 

  • Bougas B, Normandeau E, Pierron F, Campbell PGC, Bernatchez L, Couture P (2013) How does exposure to nickel and cadmium affect the transcriptome of yellow perch (Perca flavescens) – results from a 1000 candidate-gene microarray. Aquat Toxicol 142–143:355–364

    Article  PubMed  CAS  Google Scholar 

  • Buikema AL, Cairns J (1980) Aquatic invertebrate bioassays. ASTM International, West Conshohocken

    Book  Google Scholar 

  • Burden N, Sewell F, Andersen ME, Boobis A, Chipman JK, Cronin MTD, Hutchinson TH, Kimber I, Whelan M (2015) Adverse outcome pathways can drive non-animal approaches for safety assessment. J Appl Toxicol 35(9):971–975

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Burgess-Herbert SL, Euling SY (2013) Use of comparative genomics approaches to characterize interspecies differences in response to environmental chemicals: challenges, opportunities, and research needs. Toxicol Appl Pharmacol 271(3):372–385

    Article  PubMed  CAS  Google Scholar 

  • Colbourne JK, Pfrender ME, Gilbert D, Thomas WK, Tucker A, Oakley TH, Tokishita S, Aerts A, Arnold GJ, Basu MK (2011) The ecoresponsive genome of Daphnia pulex. Science 331(6017):555–561

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Council Directive 2010/63/EU of 22 September 2010 on the protection of animals used for scientific purposes [2010] OJ L276/33

    Google Scholar 

  • De Coninck DIM, Asselman J, Glaholt S, Janssen CR, Colbourne JK, Shaw JR, De Schamphelaere KAC (2014) Genome-wide transcription profiles reveal genotype-dependent responses of biological pathways and gene-families in daphnia exposed to single and mixed stressors. Environ Sci Technol 48(6):3513–3522

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dessimoz C, Gabaldón T, Roos DS, Sonnhammer ELL, Herrero J, Altenhoff A, Apweiler R, Ashburner M, Blake J, Boeckmann B, Bridge A, Bruford E, Cherry M, Conte M, Dannie D, Datta R, Domelevo Entfellner J, Ebersberger I, Galperin M, Joseph J, Koestler T, Kriventseva E, Lecompte O, Leunissen J, Lewis S, Linard B, Livstone MS, Lu H-C, Martin M, Mazumder R, Messina D, Miele V, Muffato M, Perrière G, Punta M, Rouard M, Schmitt T, Schreiber F, Silva A, Sjölander K, Škunca N, Stanley E, Szklarczyk R, Thomas P, Uchiyama I, Van Bel M, Vandepoele K, Vilella AJ, Yates A, Zdobnov E (2012) Toward community standards in the quest for orthologs. Bioinformatics 28(6):900–904

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Detra RL, Collins WJ (1991) The relationship of parathion concentration, exposure time, cholinesterase inhibition and symptoms of toxicity in midge larvae (Chironomidae: Diptera). Environ Toxicol Chem 10(8):1089–1095

    Article  CAS  Google Scholar 

  • Dondero F, Banni M, Negri A, Boatti L, Dagnino A, Viarengo A (2011) Interactions of a pesticide/heavy metal mixture in marine bivalves: a transcriptomic assessment. BMC Genomics 12:195

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ellman GL, Courtney KD, Andres V Jr, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7(2):88–90

    Article  PubMed  CAS  Google Scholar 

  • Fang G, Bhardwaj N, Robilotto R, Gerstein MB (2010) Getting started in gene orthology and functional analysis. PLoS Comput Biol 6(3):1–8

    Article  CAS  Google Scholar 

  • Feder ME, Mitchell-Olds T (2003) Evolutionary and ecological functional genomics. Nat Rev Genet 4:649–655

    Article  CAS  Google Scholar 

  • Gabaldón T, Koonin EV (2013) Functional and evolutionary implications of gene orthology. Nat Rev Genet 14:360–366

    Article  PubMed  CAS  Google Scholar 

  • Gabaldón T, Dessimoz C, Huxley-Jones J, Vilella AJ, Sonnhammer ELL, Lewis S (2009) Joining forces in the quest for orthologs. Genome Biol 10(9):403. doi:10.1186/gb-2009-10-9-403

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gerstein MB, Rozowsky J, Yan KK, Wang D, Cheng C, Brown JB, Davis CA, Hillier L, Sisu C, Li JJ, Pei B, Harmanci AO, Duff MO, Djebali S, Alexander RP, Alver BH, Auerbach R, Bell K, Bickel PJ, Boeck ME, Boley NP, Booth BW, Cherbas L, Cherbas P, Di C, Dobin A, Drenkow J, Ewing B, Fang G, Fastuca M, Feingold EA, Frankish A, Gao G, Good PJ, Guigó R, Hammonds A, Harrow J, Hoskins RA, Howald C, Hu L, Huang H, Hubbard TJ, Huynh C, Jha S, Kasper D, Kato M, Kaufman TC, Kitchen RR, Ladewig E, Lagarde J, Lai E, Leng J, Lu Z, MacCoss M, May G, McWhirter R, Merrihew G, Miller DM, Mortazavi A, Murad R, Oliver B, Olson S, Park PJ, Pazin MJ, Perrimon N, Pervouchine D, Reinke V, Reymond A, Robinson G, Samsonova A, Saunders GI, Schlesinger F, Sethi A, Slack FJ, Spencer WC, Stoiber MH, Strasbourger P, Tanzer A, Thompson OA, Wan KH, Wang G, Wang H, Watkins KL, Wen J, Wen K, Xue C, Yang L, Yip K, Zaleski C, Zhang Y, Zheng H, Brenner SE, Graveley BR, Celniker SE, Gingeras TR, Waterston R (2014) Comparative analysis of the transcriptome across distant species. Nature 512:445–448

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Giga Community of Scientists (2014) The global invertebrate genomics alliance (GIGA): developing community resources to study diverse invertebrate genomes. J Hered 105(1):1–18

    Article  CAS  Google Scholar 

  • Gong P, Basu N, Scheuhammer AM, Perkins EJ (2010) Neurochemical and electrophysiological diagnosis of reversible neurotoxicity in earthworms exposed to sublethal concentrations of CL-20. Environ Sci Pollut Res 17(1):181–186

    Article  CAS  Google Scholar 

  • Goodman M, Czelusniak J, Moore GW, Romero-Herrera AE, Matsuda G (1979) Fitting the gene lineage into its species lineage, a parsimony strategy illustrated by cladograms constructed from globin sequences. Syst Biol 28(2):132–163

    Article  CAS  Google Scholar 

  • Gorokhova E, Kyle M (2002) Analysis of nucleic acids in Daphnia: development of methods and ontogenetic variations in RNA-DNA content. J Plankton Res 24(5):511–522

    Article  CAS  Google Scholar 

  • Grey KB, Moss BL, Burrell BD (2009) Molecular identification and expression of the NMDA receptor NR1 subunit in the leech. Invertebr Neurosci 9(1):11–20

    Article  CAS  Google Scholar 

  • Groh KJ, Carvalho RN, Chipman JK, Denslow ND, Halder M, Murphy CA, Roelofs D, Rolaki A, Schirmer K, Watanabe KH (2015) Development and application of the adverse outcome pathway framework for understanding and predicting chronic toxicity: I. Challenges and research needs in ecotoxicology. Chemosphere 120:764–777

    Article  PubMed  CAS  Google Scholar 

  • Gunnarsson L, Jauhiainen A, Kristiansson E, Nerman O, Larsson DGJ (2008) Evolutionary conservation of human drug targets in organisms used for environmental risk assessments. Environ Sci Technol 42(15):5807–5813

    Article  PubMed  CAS  Google Scholar 

  • Hammond JI, Jones DK, Stephens PR, Relyea RA (2012) Phylogeny meets ecotoxicology: evolutionary patterns of sensitivity to a common insecticide. Evol Appl 5(6):593–606

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Han M, Kim J (2015) Effect of dietary iron loading on recognition memory in growing rats. PLoS One 10(3):e0120609

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ishikawa H (1977) Evolution of ribosomal RNA. Comp Biochem Physiol B 58(1):1–7

    Article  PubMed  CAS  Google Scholar 

  • Kano T, Brockie PJ, Sassa T, Fujimoto H, Kawahara Y, Iino Y, Mellem JE, Madsen DM, Hosono R, Maricq AV (2008) Memory in Caenorhabditis elegans is mediated by NMDA-type ionotropic glutamate receptors. Curr Biol 18(13):1010–1015

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kato Y, Shiga Y, Kobayashi K, Tokishita S, Yamagata H, Iguchi T, Watanabe H (2011) Development of an RNA interference method in the cladoceran crustacean Daphnia magna. Dev Genes Evol 220(11–12):337–345

    Article  PubMed  CAS  Google Scholar 

  • Kato Y, Matsuura T, Watanabe H (2012) Genomic integration and germline transmission of plasmid injected into crustacean Daphnia magna eggs. PLoS One 7(9):e45318

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kooijman B (2009) Dynamic energy budget theory for metabolic organisation, 3rd edn. Cambridge University Press, Cambridge, UK

    Book  Google Scholar 

  • Koonin EV (2005) Orthologs, paralogs and evolutionary genomics. Annu Rev Genet 39:309–338

    Article  PubMed  CAS  Google Scholar 

  • Kramer NI, Busser FJM, Oosterwijk MTT, Schirmer K, Escher BI, Hermens JLM (2010) Development of a partition-controlled dosing system for cell assays. Chem Res Toxicol 23:1806–1814

    Article  PubMed  CAS  Google Scholar 

  • Kriventseva EV, Tegenfeldt F, Petty TJ, Waterhouse RM, Simão FA, Pozdnyakov IA, Ioannidis P, Zdobnov EM (2015) OrthoDB v8: update of the hierarchical catalog of orthologs and the underlying free software. Nucleic Acids Res 43(Database issue):D250–D256. doi:10.1093/nar/gku1220

    Article  PubMed  CAS  Google Scholar 

  • LaLone CA, Villeneuve CL, Burgoon LD, Russom CL, Helgen HW, Berninger JP, Tietge JE, Severson MN, Cavallin JE, Ankley GT (2013) Molecular target sequence similarity as a basis for species extrapolation to assess the ecological risk of chemicals with known modes of action. Aquat Toxicol 144–145:141–154

    Article  PubMed  CAS  Google Scholar 

  • Lampert W (2011) In: Kinne O (ed) Daphnia: development of a model organism in ecology and evolution, Excellence in ecology series. International Ecology Institute, Luhe

    Google Scholar 

  • Larras F, Keck F, Montuelle B, Rimet F, Bouchez A (2014) Linking diatom sensitivity to herbicides to phylogeny: a step forward for biomonitoring? Environ Sci Technol 48(3):1921–1930

    Article  PubMed  CAS  Google Scholar 

  • Leung MC, Williams PL, Benedetto A, Au C, Helmcke KJ, Aschner M, Meyer JN (2008) Caenorhabditis elegans: an emerging model in biomedical and environmental toxicology. Toxicol Sci 106(1):5–28

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lu X, Lu H, Zhao L, Yang Y, Lu Z (2010) Genome-wide pathways analysis of nickel ion-induced differential genes expression in fibroblasts. Biomaterials 31(8):1965–1973

    Article  PubMed  CAS  Google Scholar 

  • Lu Y, Park Y, Gao X, Zhang X, Yoo J, Pang Y, Jiang H, Zhu KY (2012) Cholinergic and non-cholinergic functions of two acetylcholinesterase genes revealed by gene-silencing in Tribolium castaneum. Sci Rep 2(288):1–7

    Google Scholar 

  • Martin BT, Jager T, Nisbit RM, Preuss TG, Hammers-Wirtz M, Grimm V (2013) Extrapolating ecotoxicological effects from individuals to populations: a generic approach based on dynamic energy budget theory and individual-based modeling. Ecotoxicology 22(3):574–583

    Article  PubMed  CAS  Google Scholar 

  • Mohamed B, Hajer A, Susanna S, Caterina O, Flavio M, Hamadi B, Aldo V (2014) Transcriptomic responses to heat stress and nickel in the mussel Mytilus galloprovincialis. Aquat Toxicol 148:104–112

    Article  PubMed  CAS  Google Scholar 

  • Moreira EG, Yu X, Robinson JF, Griffith W, Hong SW, Beyer RP, Bammler TK, Faustman EM (2010) Toxicogenomic profiling in maternal and fetal rodent brains following gestational exposure to chlorpyrifos. Toxicol Appl Pharmacol 245(3):310–325

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nakanishi T, Kato Y, Matsuura T, Watanabe H (2014) CRISPR/Cas-mediated targeted mutagenesis in Daphnia magna. PLoS One 9(5):e98363

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nookaew I, Papini M, Pornputtpong N, Scalcinati G, Fagerberg L, Uhlen M, Nielsen J (2012) A comprehensive comparison of RNA-Seq-based transcriptome analysis from reads to differential gene expression and cross-comparison with microarrays: a case study in Saccharomyces cerevisiae. Nucleic Acids Res 2012:1–14

    Google Scholar 

  • Oetken M, Bachmann J, Schulte-Oehlmann U, Oehlmann J (2004) Evidence for endocrine disruption in invertebrates. Int Rev Cytol 236:1–44

    Article  PubMed  CAS  Google Scholar 

  • Patwardhan V, Ghaskadbi S (2013) Invertebrate alternatives for toxicity testing: hydra stakes its claim. Proceedings of animal alternatives in teaching, toxicity testing, and medicine, Bhubaneswar, 2012: 69–76

    Google Scholar 

  • Paul RJ, Colmorgen M, Pirow R, Chen YH, Tsai MC (1998) Systemic and metabolic responses in Daphnia magna to anoxia. Comp Biochem Physiol Part A 120(3):519–530

    Article  Google Scholar 

  • Perkins EJ, Antczak P, Burgoon L, Falciani F, Garcia-Reyero N, Gutsell S, Hodges G, Kienzler A, Knapen D, McBride M, Willett C (2015) Adverse outcome pathways for regulatory applications: examination of four case studies with different degrees of completeness and scientific confidence. Toxicol Sci 148(1):14–25

    Article  PubMed  CAS  Google Scholar 

  • Quinn DM (1987) Acetylcholinesterase: enzyme structure, reaction dynamics, and virtual transition states. Chem Rev 87(5):955–979

    Article  CAS  Google Scholar 

  • Rajini PS, Melstrom P, Williams PL (2008) A comparative study on the relationship between various toxicological endpoints in Caenorhabditis elegans exposed to organophsophorus insecticides. J Toxicol Environ Health A 71(15):1043–1050

    Article  PubMed  CAS  Google Scholar 

  • Raymond-Delpech V, Matsuda K, Sattelle BM, Rauh JJ, Sattelle DB (2005) Ion channels: molecular targets of neuroactive insecticides. Invertebr Neurosci 5(3–4):119–133

    Article  CAS  Google Scholar 

  • REACH (2006). Regulation (EC) No 1907/2006 of The European Parliament and of The Council In Registration, Evaluation, Authorisation and Restriction of Chemicals (REACH), establishing a European Chemicals Agency, amending Directive 1999/45/EC and repealing Council Regulation (EEC) No 793/93 and Commission Regulation (EC) No 1488/94 as well as Council Directive 76/769/EEC and Commission Directives 91/155/EEC, 93/67/EEC, 93/105/EC and 2000/21/EC. The European Parliament and The Council of The European Union

    Google Scholar 

  • Reddy MS, Jayaprada P, Rao KVR (1990) Impact of methyl parathion and malathion on cholinergic and non-cholinergic enzyme systems of penaeid prawn, Metpenaeus monoceros. Biochem Int 22:769–780

    PubMed  CAS  Google Scholar 

  • Reddy NC, Rao JV (2008) Biological response of earthworm, Eisenia foetida (Savigny) to an organophosphorus pesticide, profenofos. Ecotoxicol Environ Saf 71(2):574–582

    Article  CAS  Google Scholar 

  • Reddy TBK, Thomas A, Stamatis D, Bertsch J, Isbandi M, Jansson J, Mallajosyula J, Pagani I, Lobos E, Kyrpides N (2014) The genomes OnLine database (GOLD) v.5: a metadata management system based on a four level (meta)genome project classification. Nucl Acids Res. doi:10.1093/nar/gku950

  • Rodriguez-Serrano M, Romero-Puertas MC, Pazmino DM, Testillano PS, Risueno MC, del Rio LA, Sandalio LM (2009) Cellular response of pea plants to cadmium toxicity: cross talk between reactive oxygen species, nitric oxide, and calcium. Plant Physiol 150(1):229–243

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Russom CL, Bradbury SP, Broderius SJ, Hammermeister DE, Drummond RA (1997) Predicting modes of toxic action from chemical structure: acute toxicity in the fathead minnow (Pimephales promelas). Environ Toxicol Chem 16(5):948–967

    Article  CAS  Google Scholar 

  • Russom CL, Lalone CA, Villeneuve DL, Ankley GT (2014) Development of an adverse outcome pathway for acetylcholinesterase inhibition leading to acute mortality. Environ Toxicol Chem 33(10):2157–2169

    Article  PubMed  CAS  Google Scholar 

  • Santiago-Vázquez LZ, Ranzer LK, Kerr RG (2006) Comparison of two total RNA extraction protocols using the marine gorgonian coral Pseudopterogorgia elisabethae and its symbiont Symbiodinium sp. Electron J Biotechnol 9(5):598–603

    Article  CAS  Google Scholar 

  • Schreiber R, Gündel U, Franz S, Küster A, Rechenberg B, Altenburger R (2011) Using the fish plasma model for comparative hazard identification for pharmaceuticals in the environment by extrapolation from human therapeutic data. Regul Toxicol Pharmacol 61(3):261–275

    Article  PubMed  CAS  Google Scholar 

  • Seyfert AL, Cristescu ME, Frisse L, Schaack S, Thomas WK, Lynch M (2008) The rate and spectrum of microsatellite mutation in Caenorhabditis elegans and Daphnia pulex. Genetics 178(4):2113–2121

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shaw JR, Pfrender ME, Eads BD, Klaper R, Callaghan A, Sibly RM, Colson I, Jansen B, Gilbert D, Colbourne JK (2008) Daphnia as an emerging model for toxicological genomics. In: Hogstrand C, Kille P (eds) Comparative Toxicogenomics, vol 2. Elsevier Science, Amsterdam, pp 165–219

    Chapter  Google Scholar 

  • Smith TF, Waterman MS (1981) Identification of common molecular subsequences. J Mol Biol 147:195–197

    Article  PubMed  CAS  Google Scholar 

  • Smyth GK (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3(1):3

    Article  Google Scholar 

  • Spade DJ, Griffitt RJ, Liu L, Brown-Peterson NJ, Kroll KJ, Feswick A, Glazer RA, Barber DS, Denslow ND (2010) Queen conch (Strombus gigas) testis regresses during the reproductive season at nearshore sites in the Florida keys. PLoS One 5(9):e12737

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Stevanik DJ, Wolenski FS, Friedman LE, Gilmore TD, Finnerty JR (2013) Isolation of DNA, RNA and protein from the starlet sea anemone Nematostella vectensis. Nat Protoc 8(5):892–899

    Article  CAS  Google Scholar 

  • Stilwell GE, Saraswati S, Littleton JT, Chouinard SW (2006) Development of a Drosophila seizure model for in vivo high-throughput drug screening. Eur J Neurosci 24(8):2211–2222

    Article  PubMed  Google Scholar 

  • Subramanian A, Tamayo P, Mootha VK, Mukherjee EBL, Gillette MA, Paulovic A, Pomeroy SL, Golub TR, Lander ES, Mesirov JP (2005) Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci 102(43):15545–15550

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Svendsen C, Spurgeon DJ, Hankard PK, Weeks JM (2004) A review of lysosomal membrane stability measured by neutral red retention: is it a workable earthworm biomarker? Ecotoxicol Environ Saf 57(1):20–29

    Article  PubMed  CAS  Google Scholar 

  • Swain S, Wren JF, Stürzenbaum SR, Kille P, Morgan AJ, Jager T, Jonker MJ, Hankard PK, Svendsen C, Owen J, Hedley BA, Blaxter M, Spurgeon DJ (2010) Linking toxicant physiological mode of action with induced gene expression changes in Caenorhabditis elegans. BMC Syst Biol 4:32

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tagu D, Colbourne JK, Nègre N (2014) Genomic data integration for ecological and evolutionary traits in non-model organisms. BMC Genomics 15:490

    Article  PubMed  PubMed Central  Google Scholar 

  • Taylor EM, Lehmann AR (1998) Conservation of eukaryotic DNA repair mechanisms. Int J Radiat Biol 74(3):277–286

    Article  PubMed  CAS  Google Scholar 

  • Taylor NS, Weber RJM, White TA, Viant MR (2010) Discriminating between different acute chemical toxicities via changes in the daphnid metabolome. Toxicol Sci 118(1):307–317

    Article  PubMed  CAS  Google Scholar 

  • The C. elegans Sequencing Consortium (1998) Genome sequence of the Nematode C. elegans: a platform for investigating biology. Science 282(5396): 2012–2018

    Google Scholar 

  • Thomas P, Dawick J, Lampi M, Lemaire P, Presow S, van Egmond R, Arnot JA, Mackay D, Mayer P, Burgos MG (2015) Application of the activity framework for assessing aquatic ecotoxicology data for organic chemicals. Environ Sci Technol 49(20):12289–12296

    Article  PubMed  CAS  Google Scholar 

  • Tilton FA, Tilton SC, Bammler TK, Beyer RP, Stapleton PL, Scholz NL, Gallagher EP (2011) Transcriptional impact of organophosphate and metal mixtures on olfaction: copper dominates the chlorpyrifos-induced response in adult zebrafish. Aquat Toxicol 102(3–4):205–215

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Toyota K, Miyakawa H, Yamaguchi K, Shigenobu S, Ogino Y, Tatarazako N, Miyagawa S, Iguchi T (2015) NMDA receptor activation upstream of methyl farnesoate signaling for short day-induced male offspring production in the water flea, Daphnia pulex. BMC Genomics 16(1):186

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tushers VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci 98(9):5116–5121

    Article  Google Scholar 

  • USEPA (2015) ToxCast & Tox21 summary files from invitrodb_v2. Retrieved from http://www2.Epa.Gov/chemical-research/toxicity-forecaster-toxcasttm-data on October 28, 2015. Data released. October 2015

  • Van Wezel AP, de Vries DA, Sijm D, Opperhuizen A (1996) Use of the lethal body burden in the evaluation of mixture toxicity. Ecotoxicol Environ Saf 35(3):236–241

    Article  PubMed  Google Scholar 

  • Vanderbrouck T, Soetaert A, van der Ven K, Blust R, de Coen W (2009) Nickel and binary metal mixture responses in Daphnia magna: molecular fingerprints and (sub)organismal effects. Aquat Toxicol 92(1):18–29

    Article  CAS  Google Scholar 

  • Verhaar HJM, Van Leeuwen CJ, Hermens JLM (1992) Classifying environmental pollutants 1: structure-activity relationships for prediction of aquatic toxicity. Chemosphere 25(4):471–491

    Article  CAS  Google Scholar 

  • Verslycke T, Ghekiere A, Raimondo S, Janssen C (2007) Mysid crustaceans as standard models for the screening and testing of endocrine-disrupting chemicals. Ecotoxicology 16(1):205–219

    Article  PubMed  CAS  Google Scholar 

  • Viñuela A, Snoek LB, Riksen JAG, Kammenga JE (2010) Genome-wide gene expression analysis in response to organophosphorus pesticide chlorpyrifos and diazinon in C. elegans. PLoS One 5(8):e12145

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev 10(1):57–63

    Article  CAS  Google Scholar 

  • Williams EG, Auwerx J (2015) The convergence of systems and reductionist approaches in complex trait analysis. Cell 162(1):23–32

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wren JF, Kille P, Spurgeon DJ, Swain S, Sturzenbaum SR, Jager T (2011) Application of physiologically based modelling and trascriptomics to probe the systems toxicology of aldicarb for Caenorhabditis elegans (Maupas 1900). Ecotoxicology 20(2):397–408

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Geoff Hodges .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer International Publishing AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Hodges, G. et al. (2018). Invertebrate Model Species in AOP Development. In: Garcia-Reyero, N., Murphy, C. (eds) A Systems Biology Approach to Advancing Adverse Outcome Pathways for Risk Assessment. Springer, Cham. https://doi.org/10.1007/978-3-319-66084-4_5

Download citation

Publish with us

Policies and ethics