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Caenorhabditis elegans as a Biological Model for Multilevel Biomarker Analysis in Environmental Toxicology and Risk Assessment

  • Choi, Jin-Hee (Faculty of Environmental Engineering, College of Urban Science, University of Seoul)
  • Published : 2008.12.01

Abstract

While in some instances, loss of diversity results from acute toxicity (e.g. major pollution incidents), in most cases it results from long-term sub-lethal effects that alter the relative competitive ability and fitness of certain organisms. In such cases the sub-lethal effects will cause a physiological response in the organism that ultimately leads to community level changes. Very sensitive tools are now available to study sub-lethal responses at the molecular level. However, relating such laboratory measurements to ecological effects represents a substantial challenge that can only be met by investigation at all scales (molecular, individual organism and community level) with an appropriate group of organisms. Among the various in vertebrates which can be used as model organisms in such a way, the soil nematode, Caenorhabditis elegans appear to be a promising biological model to diagnose environmental quality. This paper reviews the current status of multilevel biomarkers in environmental toxicology, and C. elegans as promising organisms for this approach.

Keywords

References

  1. Anderson, G.L., Boyd, W.A. and Williams, P.L. (2001). Assessment of sublethal endpoints for toxicity testing with the nematode Caenorhabditis elegans. Environ. Toxicol. Chem., 20, 833-838 https://doi.org/10.1897/1551-5028(2001)020<0833:AOSEFT>2.0.CO;2
  2. Anderson, G.L., Cole, R.D. and Williams, P.L. (2004). Assessing behavioral toxicity with Caenorhabditis elegans. Environ. Toxicol. Chem., 23, 1235-1240 https://doi.org/10.1897/03-264
  3. Antoshechkin, I. and Sternberg, P.W. (2007). The versatile worm: genetic and genomic resources for Caenorhabditis elegans research. Nat. Rev. Genet., 8, 518-532 https://doi.org/10.1038/nrg2105
  4. Ayyadevara, S., Alla, R., Thaden, J.J. and Shmookler Reis, R.J. (2008). Remarkable longevity and stress resistance of nematode PI3K-null mutants. Aging Cell, 7, 13-22 https://doi.org/10.1111/j.1474-9726.2007.00348.x
  5. Ayyadevara, S., Dandapat, A., Singh, S.P., Benes, H., Zimniak, L., Reis, R.J. and Zimniak, P. (2005). Lifespan extension in hypomorphic daf-2 mutants of Caenorhabditis elegans is partially mediated by glutathione transferase CeGSTP2- 2. Aging Cell., 4, 299-307 https://doi.org/10.1111/j.1474-9726.2005.00172.x
  6. Barsyte, D., Lovejoy, D.A. and Lithgow, G.J. (2001). Longevity and heavy metal resistance in daf-2 and age-1 longlived mutants of Caenorhabditis elegans. FASEB J., 15, 627-634 https://doi.org/10.1096/fj.99-0966com
  7. Bettinger, J.C., Carnell, L., Davies, A.G. and McIntire, S.L. (2004). The use of Caenorhabditis elegans in molecular neuropharmacology. Int. Rev. Neurobiol., 62, 195-212 https://doi.org/10.1016/S0074-7742(04)62007-1
  8. Bongers, T. and Ferris, H. (1999). Nematode community structure as a bioindicator in environmental monitoring. Trends Ecol. Evol., 14, 224-228 https://doi.org/10.1016/S0169-5347(98)01583-3
  9. Boyd, W.A. and Williams, P.L. (2003). Comparison of the sensitivity of three nematode species to copper and their utility in aquatic and soil toxicity tests. Environ. Toxicol. Chem., 22, 2768-2774 https://doi.org/10.1897/02-573
  10. Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics., 77, 91-94
  11. Caquet, T., Lagadic, L. and Sheffield, S.R. (2000). Mesocosms in ecotoxicology (1): Outdoor aquatic systems. Rev. Environ. Contam. Toxicol., 165, 1-38
  12. Choi, J., Caquet, T. and Roche, H. (2002). Multilevel effects of sublethal fenitrothion exposure in Chironomus riparius Mg. (Diptera, Chironomidae) larvae. Environ. Toxicol. Chem., 21, 2725-2730 https://doi.org/10.1897/1551-5028(2002)021<2725:MEOSFE>2.0.CO;2
  13. Chu, K.W., Chan, S.K. and Chow, K.L. (2005). Improvement of heavy metal stress and toxicity assays by coupling a transgenic reporter in a mutant nematode strain. Aquat. Toxicol., 74, 320-332 https://doi.org/10.1016/j.aquatox.2005.06.006
  14. Cole, R.D., Anderson, G.L. and Williams, P.L. (2004). The nematode Caenorhabditis elegans as a model of organophosphate- induced mammalian neurotoxicity. Toxicol. Appl. Pharmacol., 194, 248-256 https://doi.org/10.1016/j.taap.2003.09.013
  15. Committee on Developmental Toxicology., Board on Environmental Studies and Toxicology., National Research Council. (2000). Scientific Frontiers in Developmental Toxicology and Risk Assessment. National Research Council, pp. 1- 354
  16. Custodia, N., Won, S.J., Novillo, A., Wieland, M., Li, C. and Callard, I.P. (2001). Caenorhabditis elegans as an environmental monitor using DNA microarray analysis. Ann. N.Y. Acad. Sci., 948, 32-42
  17. Cui, Y., McBride, S.J., Boyd, W.A., Alper, S. and Freedman, J.H. (2007). Toxicogenomic analysis of Caenorhabditis elegans reveals novel genes and pathways involved in the resistance to cadmium toxicity. Genome Biol., 8, R122 https://doi.org/10.1186/gb-2007-8-6-r122
  18. Daitoku, H. and Fukamizu, A. (2007). FOXO transcription factors in the regulatory networks of longevity. J. Biochem., 141, 769-774 https://doi.org/10.1093/jb/mvm104
  19. Dengg, M. and van Meel, J.C. (2004). Caenorhabditis elegans as model system for rapid toxicity assessment of pharmaceutical compounds. J. Pharmacol. Toxicol. Methods, 50, 9-14
  20. Depledge, M.H. (1994). Genotypic toxicity: implications for individuals and populations. Environ. Health Perspect., 12, 101-104
  21. Dhawan, R., Dusenbery, D.B. and Williams, P.L. (1999). Comparison of lethality, reproduction, and behavior as toxicological endpoints in the nematode Caenorhabditis elegans. J. Toxicol. Environ. Health A., 58, 451-462 https://doi.org/10.1080/009841099157179
  22. Dhawan, R., Dusenbery, D.B. and Williams, P.L. (2000). A comparison of metal-induced lethality and behavioral responses in the nematode Caenorhabditis elegans. Environ. Toxicol. Chem., 19, 3061-3067 https://doi.org/10.1897/1551-5028(2000)019<3061:ACOMIL>2.0.CO;2
  23. Dong, J., Boyd, W.A. and Freedman, J.H. (2008). Molecular characterization of two homologs of the Caenorhabditis elegans cadmium-responsive gene cdr-1: cdr-4 and cdr-6. J. Mol. Biol., 376, 621-633 https://doi.org/10.1016/j.jmb.2007.11.094
  24. Dong, J., Song, M.O. and Freedman, J.H. (2005). Identification and characterization of a family of Caenorhabditis elegans genes that is homologous to the cadmiumresponsive gene cdr-1. Biochim. Biophys. Acta., 1727, 16- 26 https://doi.org/10.1016/j.bbaexp.2004.11.007
  25. Forbes, V.E., Palmqvist, A. and Bach, L. (2006). The use and misuse of biomarkers in ecotoxicology. Environ. Toxicol. Chem., 25, 272-280 https://doi.org/10.1897/05-257R.1
  26. Fossi, M.C., Casini, S., Savelli, C., Corbelli, C., Franchi, E., Mattei, N., Sanchez-Hernandez, J.C., Corsi, Bamber, I., Depledge, S. and Depledge, M.H. (2000). Biomarker responses at different levels of biological organisation in crabs (Carcinus aestuarii) experimentally exposed to benzo(alpha)pyrene. Chemosphere, 40, 861-874 https://doi.org/10.1016/S0045-6535(99)00300-8
  27. Gami, M.S., Iser, W.B., Hanselman, K.B. and Wolkow, C.A. (2006). Activated AKT/PKB signaling in C. elegans uncouples temporally distinct outputs of DAF-2/insulin-like signaling. B.M.C. Dev. Biol., 6, 45 https://doi.org/10.1186/1471-213X-6-45
  28. Grad, L.I. and Lemire, B.D. (2004). Mitochondrial complex I mutations in Caenorhabditis elegans produce cytochrome c oxidase deficiency, oxidative stress and vitamin-responsive lactic acidosis. Hum. Mol. Genet., 13, 303-314 https://doi.org/10.1093/hmg/ddh231
  29. Harada, H., Kurauchi, M., Hayashi, R. and Eki, T. (2007). Shortened lifespan of nematode Caenorhabditis elegans after prolonged exposure to heavy metals and detergents. Ecotoxicol. Environ. Saf., 66, 378-383 https://doi.org/10.1016/j.ecoenv.2006.02.017
  30. Heckmann, L.H., Sibly, R.M., Connon, R., Hooper, H.L., Hutchinson, T.H., Maund, S.J., Hill, C.J., Bouetard, A. and Callaghan, A. (2008). Systems biology meets stress ecology: linking molecular and organismal stress responses in Daphnia magna. Genome Biology, 9, R40 https://doi.org/10.1186/gb-2008-9-2-r40
  31. Hollis, R.P., Killham, K. and Glover, L.A. (2000). Design and application of a biosensor for monitoring toxicity of compounds to eukaryotes. Appl. Environ. Microbiol., 66, 1676- 1679 https://doi.org/10.1128/AEM.66.4.1676-1679.2000
  32. Hughes, S. and Stürzenbaum, S.R. (2007). Single and double metallothionein knockout in the nematode C. elegans reveals cadmium dependent and independent toxic effects on life history traits. Environ. Pollut., 145, 395-400 https://doi.org/10.1016/j.envpol.2006.06.003
  33. Ibiam, U. and Grant, A. (2005). RNA/DNA ratios as a sublethal endpoint for large-scale toxicity tests with the nematode Caenorhabditis elegans. Environ. Toxicol. Chem., 24, 1155-1159 https://doi.org/10.1897/04-262R.1
  34. Inoue, H., Hisamoto, N., An, J.H., Oliveira, R.P., Nishida, E., Blackwell, T.K. and Matsumoto, K. (2005). The C. elegans p38 MAPK pathway regulates nuclear localization of the transcription factor SKN-1 in oxidative stress response. Genes Dev., 19, 2278-2283 https://doi.org/10.1101/gad.1324805
  35. Jones, D., Stringham, E.G., Babich, S.L. and Candido, E.P. (1996). Transgenic strains of the nematode C. elegans in biomonitoring and toxicology: Effects of captan and related compounds on the stress response. Toxicology, 109, 119- 127 https://doi.org/10.1016/0300-483X(96)03316-1
  36. Kaletta, T. and Hengartner, M.O. (2006). Finding function in novel targets: C. elegans as a model organism. Nat. Rev. Drug. Discov., 5, 387-398 https://doi.org/10.1038/nrd2031
  37. Kendall, G., Cooper, H.J., Heptinstall, J., Derrick, P.J., Walton, D.J. and Peterson, I.R. (2001). Specific electrochemical nitration of horse heart myoglobin. Arch. Biochem. Biophys., 392, 169-179 https://doi.org/10.1006/abbi.2001.2451
  38. Khanna, N., Cressman, C.P. 3rd., Tatara, C.P. and Williams, P.L. (1997). Tolerance of the nematode Caenorhabditis elegans to pH, salinity, and hardness in aquatic media. Arch. Environ. Contam. Toxicol., 32, 110-114 https://doi.org/10.1007/s002449900162
  39. Kim, J., Takahashi, M., Shimizu, T., Shirasawa, T., Kajita, M., Kanayama, A. and Miyamoto, Y. (2008). Effects of a potent antioxidant, platinum nanoparticle, on the lifespan of Caenorhabditis elegans. Mech. Ageing. Dev., 129, 322-331 https://doi.org/10.1016/j.mad.2008.02.011
  40. Kipreos, E.T. (2005). Ubiquitin-mediated pathways in C. elegans. WormBook, 1, 1-24
  41. Kurauchi, K., Nakaguchi, Y., Tsutsumi, M., Hori, H., Kurihara, R., Hashimoto, S., Ohnuma, R., Yamamoto, Y., Matsuoka, S., Kawai, S., Hirata, T. and Kinoshita, M. (2005). In vivo visual reporter system for detection of estrogen-like substances by transgenic medaka. Environ. Sci. Technol., 39, 2762-2768 https://doi.org/10.1021/es0486465
  42. Kwon, J.Y., Hong, M., Choi, M.S., Kang, S., Duke, K., Kim, S., Lee, S. and Lee, J. (2004). Ethanol-response genes and their regulation analyzed by a microarray and comparative genomic approach in the nematode Caenorhabditis elegans. Genomics, 83, 600-614 https://doi.org/10.1016/j.ygeno.2003.10.008
  43. Lagadic, L., Caquet, T. and Ramade, F. (1994). The role of biomarkers in environmental assessment (5). Invertebrate populations and communities. Ecotoxicology, 3, 193-208 https://doi.org/10.1007/BF00117084
  44. Lagido, C., Pettitt, J., Porter, A.J., Paton, G.I. and Glover, L.A. (2001). Development and application of bioluminescent Caenorhabditis elegans as multicellular eukaryotic biosensors. FEBS Lett., 23, 36-39
  45. Leacock, S.W. and Reinke, V. (2006). Expression profiling of MAP kinase-mediated meiotic progression in Caenorhabditis elegans. PLoS. Genet., 10, e174
  46. Lee, S.B. and Choi, J. (2006). Multilevel evaluation of nonylphenol toxicity in fourth-instar larvae of Chironomus riparius (Diptera, Chironomidae). Environ. Toxicol. Chem., 25, 3006-3014 https://doi.org/10.1897/05-601R1.1
  47. Lee, S.M., Lee, S.B., Park, C.H. and Choi, J. (2006). Expression of heat shock protein and hemoglobin genes in Chironomus tentans (Diptera, chironomidae) larvae exposed to various environmental pollutants: a potential biomarker of freshwater monitoring. Chemosphere, 65, 1074-1081 https://doi.org/10.1016/j.chemosphere.2006.02.042
  48. Lee, S.W., Park, K., Hong, J. and Choi, J. (2008). Ecotoxicological evaluation of octachlorostyrene in fourth instar larvae of Chironomus riparius (Diptera, Chironomidae). Environ. Toxicol. Chem., 27, 1118-1127 https://doi.org/10.1897/07-219.1
  49. Leiers, B., Kampkotter, A., Grevelding, C.G., Link, C.D., Johnson, T.E. and Henkle-Duhrsen, K. (2003). A stress-responsive glutathione S-transferase confers resistance to oxidative stress in Caenorhabditis elegans. Free Radic Biol. Med., 34, 1405-1415. https://doi.org/10.1016/S0891-5849(03)00102-3
  50. Leung, M.C., Williams, P.L., Benedetto, A., Au, C., Helmcke, K.J., Aschner, M. and Meyer, J.N. (2008). Caenorhabditis elegans: an Emerging Model in Biomedical and Environmental Toxicology. Toxicol. Sci., published
  51. Liao, V.H., Dong, J. and Freedman, J.H. (2002). Molecular characterization of a novel, cadmium-inducible gene from the nematode Caenorhabditis elegans. J. Biol. Chem., 277, 42049-42059 https://doi.org/10.1074/jbc.M206740200
  52. Menzel, R., Rodel, M., Kulas, J. and Steinberg, C.E. (2005). CYP35: Xenobiotically induced gene expression in the nematode Caenorhabditis elegans. Arch. Biochem. Biophys., 438, 93-102 https://doi.org/10.1016/j.abb.2005.03.020
  53. Menzel, R., Yeo, H.L., Rienau, S., Li, S., Steinberg, C.E. and Sturzenbaum, S.R. (2007). Cytochrome P450s and shortchain dehydrogenases mediate the toxicogenomic response of PCB52 in the nematode Caenorhabditis elegans. J. Mol. Biol., 370, 1-13 https://doi.org/10.1016/j.jmb.2007.04.058
  54. Newman, M.C. and Jagoe, C.H. (1996). Ecotoxicology: a hierarchical treatment, Savannah River series on environmental sciences, Boca Raton, pp. 411
  55. Peredney, C.L. and Williams, P.L. (2000). Utility of Caenorhabditis elegans for assessing heavy metal contamination in artificial soil. Arch. Environ. Contam. Toxicol., 39, 113-118
  56. Paton, G.I., Rattray, E.A.S., Campbell, C.D., Menssen, H., Cresser, M.S., Glover, L.A. and Killham, K. (1997). In: Bioindicators of Soil Health (Pankhurst, C.S., Doube, B. and Gupta, V., Eds.), Wallingford, UK: CAB Intermonitor, pp. 397-418
  57. Power, R.S. and de Pomerai, D.I. (1999). Effect of single and paired metal inputs in soil on a stress-inducible transgenic nematode. Arch. Environ. Contam. Toxicol., 37, 503- 511 https://doi.org/10.1007/s002449900545
  58. Poynton, H.C., Varshavsky, J.R., Chang, B., Cavigiolio, G., Chan, S., Holman, P.S., Loguinov, A.V., Bauer, D.J., Komachi, K., Theil, E.C., Perkins, E.J., Hughes, O. and Vulpe, C.D. (2007). Daphnia magna ecotoxicogenomics provides mechanistic insights into metal toxicity. Environ. Sci. Technol., 41, 1044-1050 https://doi.org/10.1021/es0615573
  59. Reichert, K. and Menzel, R. (2005). Expression profiling of five different xenobiotics using a Caenorhabditis elegans whole-genome microarray. Chemosphere, 61, 229-237 https://doi.org/10.1016/j.chemosphere.2005.01.077
  60. Risso-de Faverney, C., Devaux, A., Lafaurie, M., Girard, J.P. and and Rahmani, R. (2001). Toxic effects of wastewaters collected at upstream and downstream sites of a purification station in cultures of rainbow trout hepatocytes. Arch. Environ. Contam. Toxicol., 41, 129-141 https://doi.org/10.1007/s002440010230
  61. Roesijadi, G. (1994). Metallothionein induction as a measure of response to metal exposure in aquatic animal. Environ. Health Perspect, 12, 91-95
  62. Roh, J.Y. and Choi, J. (2008). Ecotoxicological evaluation of chlorpyrifos exposure on the nematode Caenorhabditis elegans. Ecotoxicol. Environ. Saf., doi:10.1016
  63. Roh, J.Y., Jung, I.H., Lee, J.Y. and Choi, J. (2007). Toxic effects of di(2-ethylhexyl)phthalate on mortality, growth, reproduction and stress-related gene expression in the soil nematode Caenorhabditis elegans. Toxicology, 237, 126-133 https://doi.org/10.1016/j.tox.2007.05.008
  64. Roh, J.Y., Lee, J. and Choi, J. (2006). Assessment of stressrelated gene expression in the heavy metal-exposed nematode Caenorhabditis elegans: a potential biomarker for metal-induced toxicity monitoring and environmental risk assessment. Environ. Toxicol. Chem., 25, 2946-2956 https://doi.org/10.1897/05-676R.1
  65. Russo, J. and Lagadic, L. (2000). Effects of parasitism and pesticide exposure on characteristics and functions of hemocyte populations in the freshwater snail Lymnaea palustris (Gastropoda, Pulmonata). Cell Biol. Toxicol., 16, 15-30 https://doi.org/10.1023/A:1007640519746
  66. Schafer, W.R. (2006). Neurophysiological methods in C. elegans: an introduction. WormBook, 2, 1-4
  67. Scholz, S., Kurauchi, K., Kinoshita, M., Oshima, Y., Ozato, K., Schirmer, K. and Wakamatsu, Y. (2005). Analysis of estrogenic effects by quantification of green fluorescent protein in juvenile fish of a transgenic medaka. Environ. Toxicol. Chem., 24, 2553-2561 https://doi.org/10.1897/04-525R.1
  68. Schroeder, F.C. (2006). Small molecule signaling in Caenorhabditis elegans. ACS Chem Biol., 1, 198-200. Snell, T.W., Brogdon, S.E. and Morgan, M.B. (2003). Gene expression profiling in ecotoxicology. Ecotoxicology, 12, 475-483 https://doi.org/10.1023/B:ECTX.0000003033.09923.a8
  69. Snell, T.W., Brogdon, S.E. and Morgan, M.B. (2003). Gene expression profiling in ecotoxicology. Ecotoxicology, 12, 475-483 https://doi.org/10.1023/B:ECTX.0000003033.09923.a8
  70. Steinberg, C.E., Sturzenbaum, S.R. and Menzel. R. (2008). Genes and environment - Striking the fine balance between sophisticated biomonitoring and true functional environmental genomics. Sci. Total Environ. pp. 142-161
  71. Stringham, E.G. and Candido, E.P. (1994). Transgenic hsp16- lacZ strains of the soil nematode Caenorhabditis elegans as biological monitors of environmental stress. Environ. Toxicol. Chem., 13, 1211-1220 https://doi.org/10.1897/1552-8618(1994)13[1211:THLSOT]2.0.CO;2
  72. Swain, S.C., Keusekotten, K., Baumeister, R. and Sturzenbaum, S.R. (2004). C. elegans metallothioneins: new insights into the phenotypic effects of cadmium toxicosis. J. Mol. Biol., 341, 951-959 https://doi.org/10.1016/j.jmb.2004.06.050
  73. Tullet, J.M., Hertweck, M., An, J.H., Baker, J., Hwang, J.Y., Liu, S., Oliveira, R.P., Baumeister, R. and Blackwell, T.K. (2008). Direct inhibition of the longevity-promoting factor SKN-1 by insulin-like signaling in C. elegans. Cell, 132, 1025-1038 https://doi.org/10.1016/j.cell.2008.01.030
  74. Ura, K., Kai, T., Sakata, S., Iguchi, T. and Arizono, K. (2002). Aquatic acute toxicity testing using the nematode Caenorhabditis elegans. J. Health Sci., 48, 583-586 https://doi.org/10.1248/jhs.48.583
  75. Wang, D.Y. and Wang, Y. (2008). Phenotypic and behavioral defects caused by barium exposure in nematode Caenorhabditis elegans. Arch. Environ. Contam. Toxicol., 54, 447-453 https://doi.org/10.1007/s00244-007-9050-0
  76. Wang, Y.M., Pu, P. and Le, W.D. (2007). ATP depletion is the major cause of MPP+ induced dopamine neuronal death and worm lethality in alpha-synuclein transgenic C. elegans. Neurosci Bull., 23, 329-335 https://doi.org/10.1007/s12264-007-0049-3
  77. Williams, P.L., Anderson, G.L., Johnstone, J.L., Nunn, A.D., Tweedle, M.F. and Wedeking, P. (2000). Caenorhabditis elegans as an alternative animal species. J. Toxicol. Environ. Health A., 61, 641-647 https://doi.org/10.1080/00984100050195125
  78. Williams, P.L. and Dusenbery, D.B. (1988). Using the nematode Caenorhabditis elegans to predict mammalian acute lethality to metallic salts. Toxicol. Ind. Health, 4, 469-478 https://doi.org/10.1177/074823378800400406
  79. Williams, P.L. and Dusenbery, D.B. (1990). Aquatic toxicity testing using the nematode Caenorhabditis elegans. Environ. Toxicol. Chem., 9, 1285-1290 https://doi.org/10.1897/1552-8618(1990)9[1285:ATTUTN]2.0.CO;2
  80. Yoshimi, T., Minowa, K., Karouna-Renier, N.K., Watanabe, C., Sugaya, Y. and Miura, T. (2002). Activation of stressinduced gene by insecticides in the midge, Chironomus yoshimatsui. J. Biochem. Mol. Toxicol., 16, 10-17 https://doi.org/10.1002/jbt.10018