The nematode Caenorhabditis elegans as a tool to predict chemical activity on mammalian development and identify mechanisms influencing toxicological outcome

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Harlow, Philippa H ^a   Perry, Simon J ^a   Widdison, Stephanie ^b   Daniels, Shannon ^c   Bondo, Eddie ^c   Lamberth, Clemens ^d   Currie, Richard A ^a   Flemming, Anthony J ^a  

^a JEALOTT S HILL INTERNATIONAL RESEARCH CENTRE   (United Kingdom)

^b General Bioinformatics   (United Kingdom)

^c SYNGENTA BIOTECHNOLOGY INC   (United States)

^d SYNGENTA CROP PROTECTION AG   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CAENORHABDITIS ELEGANS PROTEIN; CYTOCHROME P450; PESTICIDE;

ANIMAL; ANIMAL MODEL; CAENORHABDITIS ELEGANS; CHEMISTRY; DRUG EFFECTS; GENE INACTIVATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; MAMMAL; METABOLISM; STRUCTURE ACTIVITY RELATION; TOXICITY TESTING;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CYTOCHROME P-450 ENZYME SYSTEM; GENE KNOCKOUT TECHNIQUES; HUMANS; MAMMALS; MODELS, ANIMAL; PESTICIDES; STRUCTURE-ACTIVITY RELATIONSHIP; TOXICITY TESTS;

EID: 84961827459     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep22965     Document Type: Article

References (55)

1. Hewitt, M., Ellison, C. M., Enoch, S. J., Madden, J. C., Cronin, M. T. Integrating (Q)SAR models, expert systems and read-across approaches for the prediction of developmental toxicity. Reprod Toxicol 30, 147-160, doi: 10.1016/j.reprotox.2009.12.003 (2010).
2. Li, H. et al. Use of the ES-D3 cell differentiation assay, combined with the BeWo transport model, to predict relative in vivo developmental toxicity of antifungal compounds. Toxicol In Vitro 29, 320-328, doi: 10.1016/j.tiv.2014.11.012 (2015).
3. Ball, J. S. et al. Fishing for teratogens: a consortium effort for a harmonized zebrafish developmental toxicology assay. Toxicol Sci 139, 210-219, doi: 10.1093/toxsci/kfu017 (2014).
4. Boyd, W. A. et al. Developmental Effects of the ToxCast Phase I and II Chemicals in and Corresponding Responses in Zebrafish, Rats, and Rabbits. Environ Health Perspect, doi: 10.1289/ehp.1409645 (2015).
5. Allard, P., Kleinstreuer, N. C., Knudsen, T. B., Colaiacovo, M. P. A C. Elegans screening platform for the rapid assessment of chemical disruption of germline function. Environ Health Perspect 121, 717-724, doi: 10.1289/ehp.1206301 (2013).
6. Meyer, D., Williams, P. L. Toxicity Testing of Neurotoxic Pesticides in Caenorhabditis elegans. J Toxicol Environ Health B Crit Rev 17, 284-306, doi: 10.1080/10937404.2014.933722 (2014).
7. Cui, Y., McBride, S. J., Boyd, W. A., Alper, S., Freedman, J. H. Toxicogenomic analysis of Caenorhabditis elegans reveals novel genes and pathways involved in the resistance to cadmium toxicity. Genome Biol 8, R122, doi: 10.1186/gb-2007-8-6-r122 (2007).
8. Wolozin, B., Saha, S., Guillily, M., Ferree, A., Riley, M. Investigating convergent actions of genes linked to familial Parkinson's disease. Neurodegener Dis 5, 182-185, doi: 10.1159/000113697 (2008).
9. Kitagawa, N. et al. The role of the presenilin-1 homologue gene sel-12 of Caenorhabditis elegans in apoptotic activities. J Biol Chem 278, 12130-12134, doi: 10.1074/jbc.M212058200 (2003).
10. Wang, S. et al. Cadmium-induced germline apoptosis in Caenorhabditis elegans: the roles of HUS1, p53, and MAPK signaling pathways. Toxicol Sci 102, 345-351, doi: 10.1093/toxsci/kfm220 (2008).
11. Leung, M. C. et al. Caenorhabditis elegans: an emerging model in biomedical and environmental toxicology. Toxicol Sci 106, 5-28, doi: 10.1093/toxsci/kfn121 (2008).
12. Cole, R. D., Anderson, G. L., Williams, P. L. The nematode Caenorhabditis elegans as a model of organophosphate-induced mammalian neurotoxicity. Toxicol Appl Pharmacol 194, 248-256, doi: 10.1016/j.taap.2003.09.013 (2004).
13. Mitchell, P. et al. A differential role for neuropeptides in acute and chronic adaptive responses to alcohol: behavioural and genetic analysis in Caenorhabditis elegans. PLoS One 5, e10422, doi: 10.1371/journal.pone.0010422 (2010).
14. Kayser, E. B., Morgan, P. G., Sedensky, M. M. GAS-1: a mitochondrial protein controls sensitivity to volatile anesthetics in the nematode Caenorhabditis elegans. Anesthesiology 90, 545-554 (1999).
15. de Boer, R. et al. Caenorhabditis elegans as a Model System for Studying Drug Induced Mitochondrial Toxicity. PLoS One 10, e0126220, doi: 10.1371/journal.pone.0126220 (2015).
16. Kullyev, A. et al. A genetic survey of fluoxetine action on synaptic transmission in Caenorhabditis elegans. Genetics 186, 929-941, doi: 10.1534/genetics.110.118877 (2010).
17. Ward, A., Walker, V. J., Feng, Z., Xu, X. Z. Cocaine modulates locomotion behavior in C. Elegans. PLoS One 4, e5946, doi: 10.1371/journal.pone.0005946 (2009).
18. Sulston, J. E., Horvitz, H. R. Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev Biol 56, 110-156 (1977).
19. Sulston, J. E., Schierenberg, E., White, J. G., Thomson, J. N. The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev Biol 100, 64-119 (1983).
20. Priess, J. Notch signaling in the C. Elegans embryo, In WormBook, (ed. The C. Elegans Research Community) doi: 10.1895/wormbook.1.4.1 (2005).
21. Pellegatti, M. Preclinical in vivo ADME studies in drug development: a critical review. Expert Opin Drug Metab Toxicol 8, 161-172, doi: 10.1517/17425255.2012.652084 (2012).
22. Lindblom, T. H., Dodd, A. K. Xenobiotic detoxification in the nematode Caenorhabditis elegans. J Exp Zool A Comp Exp Biol 305, 720-730, doi: 10.1002/jez.a.324 (2006).
23. The-C.elegans-sequencing-consortium. Genome sequence of the nematode C. Elegans: a platform for investigating biology. Science 282, 2012-2018 (1998).
24. Knudsen, T. B. et al. Profiling the activity of environmental chemicals in prenatal developmental toxicity studies using the U.S. EPA's ToxRefDB. Reprod Toxicol 28, 209-219, doi: 10.1016/j.reprotox.2009.03.016 (2009).
25. Lofstedt, R. Communicating food risks in an era of growing public distrust: three case studies. Risk Anal 33, 192-202, doi: 10.1111/j.1539-6924.2011.01722.x (2013).
26. Dekant, W., Kehrer, J. P. Scientifically unfounded precaution drives European Commission's recommendations on EDC regulation, while defying common sense, well-established science and risk assessment principles. Toxicol Lett 223, A1-4, doi: 10.1016/j. toxlet.2013.07.010 (2013).
27. Knudsen, T. B. et al. Activity profiles of 309 ToxCast chemicals evaluated across 292 biochemical targets. Toxicology 282, 1-15, doi: 10.1016/j.tox.2010.12.010 (2011).
28. Lamberth, C. et al. Synthesis and fungicidal activity of tubulin polymerisation promoters. Part 2: pyridazines. Bioorg Med Chem 20, 2803-2810, doi: 10.1016/j.bmc.2012.03.035 (2012).
29. Lamberth, C. et al. Synthesis and fungicidal activity of tubulin polymerisation promoters. Part 3: imidazoles. Bioorg Med Chem 21, 127-134, doi: 10.1016/j.bmc.2012.10.052 (2013).
30. Driscoll, M., Dean, E., Reilly, E., Bergholz, E., Chalfie, M. Genetic and molecular analysis of a Caenorhabditis elegans beta-tubulin that conveys benzimidazole sensitivity. J Cell Biol 109, 2993-3003 (1989).
31. Jones, L. M., Flemming, A. J., Urwin, P. E. NHR-176 regulates cyp-35d1 to control hydroxylation-dependent metabolism of thiabendazole in Caenorhabditis elegans. Biochem J 466, 37-44, doi: 10.1042/bj20141296 (2015).
32. Jones, L. M., Rayson, S. J., Flemming, A. J., Urwin, P. E. Adaptive and specialised transcriptional responses to xenobiotic stress in Caenorhabditis elegans are regulated by nuclear hormone receptors. PLoS One 8, e69956, doi: 10.1371/journal.pone.0069956 (2013).
33. Schafer, P., Muller, M., Kruger, A., Steinberg, C. E. W., Menzel, R. Cytochrome P450-dependent metabolism of PCB52 in the nematode Caenorhabditis elegans. Arch. Biochem. Biophys. 488, 60-68 (2009).
34. Johnston, W. L., Krizus, A., Dennis, J. W. The eggshell is required for meiotic fidelity, polar-body extrusion and polarization of the C. Elegans embryo. BMC Biol 4, 35, doi: 10.1186/1741-7007-4-35 (2006).
35. Brenner, S. The genetics of Caenorhabditis elegans. Genetics 77, 71-94 (1974).
36. Menzel, R. et al. Cytochrome P450s and short-chain dehydrogenases mediate the toxicogenomic response of PCB52 in the nematode Caenorhabditis elegans. J Mol Biol 370, 1-13, doi: 10.1016/j.jmb.2007.04.058 (2007).
37. Menzel, R., Rodel, M., Kulas, J., Steinberg, C. E. CYP35: xenobiotically induced gene expression in the nematode Caenorhabditis elegans. Arch Biochem Biophys 438, 93-102, doi: 10.1016/j.abb.2005.03.020 (2005).
38. Menzel, R., Bogaert, T., Achazi, R. A systematic gene expression screen of Caenorhabditis elegans cytochrome P450 genes reveals CYP35 as strongly xenobiotic inducible. Arch Biochem Biophys 395, 158-168, doi: 10.1006/abbi.2001.2568 (2001).
39. Lewis, J. A., Szilagyi, M., Gehman, E., Dennis, W. E., Jackson, D. A. Distinct patterns of gene and protein expression elicited by organophosphorus pesticides in Caenorhabditis elegans. BMC Genomics 10, 202, doi: 10.1186/1471-2164-10-202 (2009).
40. Chakrapani, B. P., Kumar, S., Subramaniam, J. R. Development and evaluation of an in vivo assay in Caenorhabditis elegans for screening of compounds for their effect on cytochrome P450 expression. J Biosci 33, 269-277 (2008).
41. Farnham, A. W. In Piperonyl Butoxide (ed Jones, D. G.) Ch. 12, 199-214 (Academic Press, 1998).
42. Roh, J. Y., Choi, J. Cyp35a2 gene expression is involved in toxicity of fenitrothion in the soil nematode Caenorhabditis elegans. Chemosphere 84, 1356-1361, doi: 10.1016/j.chemosphere.2011.05.010 (2011).
43. Aarnio, V. et al. Caenorhabditis elegans Mutants Predict Regulation of Fatty Acids and Endocannabinoids by the CYP-35A Gene Family. Front Pharmacol 2, 12, doi: 10.3389/fphar.2011.00012 (2011).
44. Ashrafi, K. et al. Genome-wide RNAi analysis of Caenorhabditis elegans fat regulatory genes. Nature 421, 268-272 (2003).
45. Meskar, A., Plee-Gautier, E., Amet, Y., Berthou, F., Lucas, D. [Alcohol-xenobiotic interactions. Role of cytochrome P450 2E1]. Pathol Biol (Paris) 49, 696-702 (2001).
46. Preskorn, S. H. Debate resolved: there are differential effects of serotonin selective reuptake inhibitors on cytochrome P450 enzymes. J Psychopharmacol 12, S89-97 (1998).
47. Waring, M. J. et al. An analysis of the attrition of drug candidates from four major pharmaceutical companies. Nat Rev Drug Discov 14, 475-486, doi: 10.1038/nrd4609 (2015).
48. Rodriguez-Ruiz, A., Marigomez, I., Boatti, L., Viarengo, A. Dictyostelium discoideum developmental cycle (DDDC) assay: a tool for Hg toxicity assessment and soil health screening. Sci Total Environ 450-451, 39-50, doi: 10.1016/j.scitotenv.2013.01.060 (2013).
49. Guengerich, F. P. Cytochrome P450 and Chemical Toxicology. Chemical Research in Toxicology 21, 70-83, doi: 10.1021/tx700079z (2007).
50. Stiernagle, T. Maintenance of C. Elegans, In WormBook, (ed. The C. Elegans Research Community) doi: 10.1895/wormbook.1.101.1 (2006).
51. R. Core Team R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/(2013).
52. Gautier, L., Cope, L., Bolstad, B. M., Irizarry, R. A. affy-analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 20, 307-315, doi: 10.1093/bioinformatics/btg405 (2004).
53. MacDonald, J. W. Afycoretools: Functions useful for those doing repetitive analyses with Affymetrix GeneChips. Bioconductor, Fred Hutchinson Cancer Research Center, Seattle, U. S. A. URL http://www.bioconductor.org/packages/release/bioc/html/affycoretools. html (2008).
54. Smyth, G. K. In Bioinformatics and Computational Biology Solutions using R and Bioconductor (ed Carey, V., Gentleman, R., Dudoit, S., Irizarry, R., Huber, W.) Ch. 5, 397-420 (Springer, 2005).
55. Hochberg, Y., Benjamini, Y. More powerful procedures for multiple significance testing. Stat Med 9, 811-818 (1990).