Advertisement

Environmental Science and Pollution Research

, Volume 22, Issue 11, pp 7991–8002 | Cite as

Expression of biotransformation and oxidative stress genes in the giant freshwater prawn Macrobrachium rosenbergii exposed to chlordecone

  • Béatrice Gaume
  • Nathalie Dodet
  • Jean-Pierre Thomé
  • Soazig LemoineEmail author
Crop protection: environment, human health, and biodiversity

Abstract

Chlordecone is a persistent organochlorine pesticide widely used between 1972 and 1993 in the French West Indies to control the root borer in banana fields. Chlordecone use resulted in long-term pollution of soils, contamination of waters, of aquatic organisms, and of fields. Chlordecone is known to be neurotoxic, to increase prostate cancer, and to have negative effects on cognitive and motor development during infancy. In Guadeloupe, most of the freshwater species living in contaminated rivers exceed the French legal limit of 20 μg·kg−1 wet weight. In the present study, we chose a transcriptomic approach to study the cellular effects of chlordecone in the giant freshwater prawn Macrobrachium rosenbergii, an important economical species in Guadeloupe. Quantitative PCR revealed an induction of genes involved in defense mechanism against oxidative stress (catalase and selenium-dependent glutathione peroxidase) in prawns exposed to low environmental concentrations of chlordecone after 12 and 24 h of exposure. In prawns reared in a contaminated farm, transcription of genes involved in the biotransformation process (cytochrome P450 and glutathione-S-transferase (GST)) were induced after 8 days of exposure. Our results provide information on the mechanims of defense induced by chlordecone in aquatic crustacean species. This gene expression study of selected genes should be further strengthened by proteomic analyses and enzymatic activity assays to confirm the response of these biomarkers of stress in crustaceans and to give new insights into the mechanism of toxicity by chlordecone.

Keywords

Chlordecone Macrobrachium rosenbergii Bioconcentration Detoxification Oxidative stress Quantitative PCR Organochlorine Crustaceans 

Notes

Acknowledgments

We are grateful to Yolande Bouchon Navarro, Claude Bouchon, and Félix Bompy for their help in statistical analyses. This work was supported by grants from the National Research Agency (ANR CES MACHLOMA) and the Regional council of Guadeloupe for postdoctoral grant.

References

  1. Alnouti Y, Klaassen CD (2008) Tissue distribution, ontogeny, and regulation of aldehyde dehydrogenase (Aldh) enzymes mRNA by prototypical microsomal enzyme inducers in mice. Toxicol Sci 101:51–64. doi: 10.1093/toxsci/kfm280 CrossRefGoogle Scholar
  2. Aruoma OI (1998) Free radicals, oxidative stress, and antioxidants in human health and disease. J Am Oil Chem Soc 75:199–212. doi: 10.1007/s11746-998-0032-9 CrossRefGoogle Scholar
  3. Ballesteros M, Wunderlin D, Bistoni M (2009) Oxidative stress responses in different organs of Jenynsia multidentata exposed to endosulfan. Ecotoxicol Environ Saf 72:199–205. doi: 10.1016/j.ecoenv.2008.01.008 CrossRefGoogle Scholar
  4. Bansal SK, Desaiah D (1985) Chlordecone toxicity: effect of withdrawal of treatment on ATPase inhibition. Neurotoxicology 6:103–107Google Scholar
  5. Bauer M, Greenwood SJ, Clark KF et al (2013) Analysis of gene expression in Homarus americanus larvae exposed to sublethal concentrations of endosulfan during metamorphosis. Comp Biochem Physiol Part D Genomics Proteomics 8:300–308. doi: 10.1016/j.cbd.2013.07.002 CrossRefGoogle Scholar
  6. Belfiore CJ, Yang RSH, Chubb LS et al (2007) Hepatic sequestration of chlordecone and hexafluoroacetone evaluated by pharmacokinetic modeling. Toxicology 234:59–72. doi: 10.1016/j.tox.2007.02.002 CrossRefGoogle Scholar
  7. Birceanu O, Sorensen LA, Henry M et al (2014) The effects of the lampricide 3-trifluoromethyl-4-nitrophenol (TFM) on fuel stores and ion balance in a non-target fish, the rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol C Toxicol Pharmacol 160:30–41. doi: 10.1016/j.cbpc.2013.10.002 CrossRefGoogle Scholar
  8. Blanchette B, Feng X, Singh BR (2007) Marine glutathione S-transferases. Mar Biotechnol 9:513–542. doi: 10.1007/s10126-007-9034-0 CrossRefGoogle Scholar
  9. Bocquené G, Franco A (2005) Pesticide contamination of the coastline of Martinique. Mar Pollut Bull 51:612–619. doi: 10.1016/j.marpolbul.2005.06.026 CrossRefGoogle Scholar
  10. Boucher O, Simard M-N, Muckle G et al (2013) Exposure to an organochlorine pesticide (Chlordecone) and development of 18-month-old infants. Neurotoxicology 35:162–168. doi: 10.1016/j.neuro.2013.01.007 CrossRefGoogle Scholar
  11. Bouétard A, Besnard A-L, Vassaux D et al (2013) Impact of the redox-cycling herbicide diquat on transcript expression and antioxidant enzymatic activities of the freshwater snail Lymnaea stagnalis. Aquat Toxicol 126:256–265. doi: 10.1016/j.aquatox.2012.11.013 CrossRefGoogle Scholar
  12. Cabidoche Y-M, Achard R, Cattan P et al (2009) Long-term pollution by chlordecone of tropical volcanic soils in the French West Indies: a simple leaching model accounts for current residue. Environ Pollut 157:1697–1705. doi: 10.1016/j.envpol.2008.12.015 CrossRefGoogle Scholar
  13. Cannon SB, Veazey JM, Jackson RS et al (1978) Epidemic kepone poisoning in chemical workers. Am J Epidemiol 107:529–537Google Scholar
  14. Capkin E, Altinok I (2013) Effects of chronic carbosulfan exposure on liver antioxidant enzyme activities in rainbow trout. Environ Toxicol Pharmacol 36:80–87. doi: 10.1016/j.etap.2013.03.022 CrossRefGoogle Scholar
  15. Ceyhun SB, Sentürk M, Ekinci D et al (2010) Deltamethrin attenuates antioxidant defense system and induces the expression of heat shock protein 70 in rainbow trout. Comp Biochem Physiol C Toxicol Pharmacol 152:215–223. doi: 10.1016/j.cbpc.2010.04.008 CrossRefGoogle Scholar
  16. Chang C-C, Rahmawaty A, Chang Z-W (2013) Molecular and immunological responses of the giant freshwater prawn, Macrobrachium rosenbergii, to the organophosphorus insecticide, trichlorfon. Aquat Toxicol 130-131C:18–26. doi: 10.1016/j.aquatox.2012.12.024 CrossRefGoogle Scholar
  17. Chen X, Zhou Y, Yang D et al (2012) CYP4 mRNA expression in marine polychaete Perinereis aibuhitensis in response to petroleum hydrocarbon and deltamethrin. Mar Pollut Bull 64:1782–1788. doi: 10.1016/j.marpolbul.2012.05.035 CrossRefGoogle Scholar
  18. Cheung CCC, Zheng GJ, Li AMY et al (2001) Relationships between tissue concentrations of polycyclic aromatic hydrocarbons and antioxidative responses of marine mussels, Perna iridis. Aquat Toxicol 52:189–203CrossRefGoogle Scholar
  19. Coat S, Monti D, Legendre P et al (2011) Organochlorine pollution in tropical rivers (Guadeloupe): role of ecological factors in food web bioaccumulation. Environ Pollut 159:1692–1701. doi: 10.1016/j.envpol.2011.02.036 CrossRefGoogle Scholar
  20. Crupkin AC, Carriquiriborde P, Mendieta J et al (2013) Oxidative stress and genotoxicity in the South American cichlid, Australoheros facetus, after short-term sublethal exposure to endosulfan. Pestic Biochem Physiol 105:102–110. doi: 10.1016/j.pestbp.2012.12.005 CrossRefGoogle Scholar
  21. Dallaire R, Muckle G, Rouget F et al (2012) Cognitive, visual, and motor development of 7-month-old Guadeloupean infants exposed to chlordecone. Environ Res 118:79–85. doi: 10.1016/j.envres.2012.07.006 CrossRefGoogle Scholar
  22. Das SK, Tan J, Johnson DC, Dey SK (1998) Differential spatiotemporal regulation of lactoferrin and progesterone receptor genes in the mouse uterus by primary estrogen, catechol estrogen, and xenoestrogen. Endocrinology 139:2905–2915Google Scholar
  23. Dehn PF, Allen-Mocherie S, Karek J, Thenappan A (2005) Organochlorine insecticides: impacts on human HepG2 cytochrome P4501A, 2B activities and glutathione levels. Toxicol in Vitro 19:261–273. doi: 10.1016/j.tiv.2004.10.002 CrossRefGoogle Scholar
  24. Dubuisson C, Héraud F, Leblanc J-C et al (2007) Impact of subsistence production on the management options to reduce the food exposure of the Martinican population to chlordecone. Regul Toxicol Pharmacol 49:5–16. doi: 10.1016/j.yrtph.2007.04.008 CrossRefGoogle Scholar
  25. Esterbauer H, Schaur RJ, Zollner H (1991) Chemistry and biochemistry of 4-hydroxynonenal malonaldehyde and related aldehydes. Free Radic Biol Med 11:81–128CrossRefGoogle Scholar
  26. Fitzpatrick PJ, Sheehan D, Walsh AR, O’Halloran J (1997) Assessment of a glutathione S-transferase and related proteins in the gill and digestive gland of Mytilus edulis (L.), as potential organic pollution biomarkers. Biomarkers 2:51–56. doi: 10.1080/135475097231977 CrossRefGoogle Scholar
  27. Flouriot G, Pakdel F, Ducouret B, Valotaire Y (1995) Influence of xenobiotics on rainbow trout liver estrogen receptor and vitellogenin gene expression. J Mol Endocrinol 15:143–151. doi: 10.1677/jme.0.0150143 CrossRefGoogle Scholar
  28. Giusti A, Leprince P, Mazzucchelli G et al (2013) Proteomic analysis of the reproductive organs of the hermaphroditic gastropod Lymnaea stagnalis exposed to different endocrine disrupting chemicals. PLoS One 8:e81086. doi: 10.1371/journal.pone.0081086 CrossRefGoogle Scholar
  29. Guldner L, Multigner L, Héraud F et al (2010) Pesticide exposure of pregnant women in Guadeloupe: ability of a food frequency questionnaire to estimate blood concentration of chlordecone. Environ Res 110:146–151. doi: 10.1016/j.envres.2009.10.015 CrossRefGoogle Scholar
  30. Hellemans J, Mortier G, De Paepe A et al (2007) qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol 8:R19. doi: 10.1186/gb-2007-8-2-r19 CrossRefGoogle Scholar
  31. Hui K-M, Hao F-Y, Li W et al (2013) Cloning and identification of four Mu-type glutathione S-transferases from the giant freshwater prawn Macrobrachium rosenbergii. Fish Shellfish Immunol 35:546–552. doi: 10.1016/j.fsi.2013.05.012 CrossRefGoogle Scholar
  32. Jin Y, Zhang X, Shu L et al (2010) Oxidative stress response and gene expression with atrazine exposure in adult female zebrafish (Danio rerio). Chemosphere 78:846–852. doi: 10.1016/j.chemosphere.2009.11.044 CrossRefGoogle Scholar
  33. Jinna RR, Uzodinma JE, Desaiah D (1989) Age-related changes in rat brain ATPases during treatment with chlordecone. J Toxicol Environ Health 27:199–208. doi: 10.1080/15287398909531291 CrossRefGoogle Scholar
  34. Kadhel P, Monfort C, Costet N et al (2014) Chlordecone exposure, length of gestation, and risk of preterm birth. Am J Epidemiol 179:536–544. doi: 10.1093/aje/kwt313 CrossRefGoogle Scholar
  35. Kasai S, Weerashinghe IS, Shono T, Yamakawa M (2000) Molecular cloning, nucleotide sequence and gene expression of a cytochrome P450 (CYP6F1) from the pyrethroid-resistant mosquito, Culex quinquefasciatus Say. Insect Biochem Mol Biol 30:163–171CrossRefGoogle Scholar
  36. Kocarek TA, Schuetz EG, Guzelian PS (1991) Selective induction of cytochrome P450e by kepone (chlordecone) in primary cultures of adult rat hepatocytes. Mol Pharmacol 40:203–210Google Scholar
  37. Li Z-H, Zlabek V, Grabic R et al (2010) Effects of exposure to sublethal propiconazole on intestine-related biochemical responses in rainbow trout, Oncorhynchus mykiss. Chem Biol Interact 185:241–246. doi: 10.1016/j.cbi.2010.02.040 CrossRefGoogle Scholar
  38. Lorenzo MJ, Sanchez J (1989) Toxicity of the organophosphorous insecticide metamidophos (O, S-dimethyl phosphoramidothioate) to larvae of the freshwater prawn Macrobrachium rosenbergii (De Man) and the blue shrimp Penaeus stylirostris Stimpson. Bull Environ Contam Toxicol 43:302–309CrossRefGoogle Scholar
  39. Maier WE, Costa LG (1990) Na+/K(+)-ATPase in rat brain and erythrocytes as a possible target and marker, respectively, for neurotoxicity: studies with chlordecone, organotins and mercury compounds. Toxicol Lett 51:175–188CrossRefGoogle Scholar
  40. Monteiro DA, de Almeida JA, Rantin FT, Kalinin AL (2006) Oxidative stress biomarkers in the freshwater characid fish, Brycon cephalus, exposed to organophosphorus insecticide Folisuper 600 (methyl parathion). Comp Biochem Physiol C Toxicol Pharmacol 143:141–149. doi: 10.1016/j.cbpc.2006.01.004 CrossRefGoogle Scholar
  41. Montes Nieto R, García-Barrera T, Gómez-Ariza J-L, López-Barea J (2010) Environmental monitoring of Domingo Rubio stream (Huelva Estuary, SW Spain) by combining conventional biomarkers and proteomic analysis in Carcinus maenas. Environ Pollut 158:401–408. doi: 10.1016/j.envpol.2009.09.005 CrossRefGoogle Scholar
  42. Monti D, Keith P, Vigneux E (2010) Atlas des poissons et des crustacés d’eau douce de la Guadeloupe. Muséum nat, ParisGoogle Scholar
  43. Multigner L, Ndong JR, Giusti A et al (2010) Chlordecone exposure and risk of prostate cancer. J Clin Oncol 28:3457–3462. doi: 10.1200/JCO.2009.27.2153 CrossRefGoogle Scholar
  44. Nasci C, Nesto N, Monteduro RA, Da Ros L (2002) Field application of biochemical markers and a physiological index in the mussel, Mytilus galloprovincialis: transplantation and biomonitoring studies in the lagoon of Venice (NE Italy). Mar Environ Res 54:811–816CrossRefGoogle Scholar
  45. Natarajan E, Biradar RS, George JP (1992) Acute toxicity of pesticide to giant freshwater prawn Macrobrachium rosenbergii (De Man). J Aquac Trop 7:183–188Google Scholar
  46. Pasquevich MY, Dreon MS, Gutierrez Rivera JN et al (2013) Effect of crude oil petroleum hydrocarbons on protein expression of the prawn Macrobrachium borellii. Comp Biochem Physiol C Toxicol Pharmacol 157:390–396. doi: 10.1016/j.cbpc.2013.03.006 CrossRefGoogle Scholar
  47. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45CrossRefGoogle Scholar
  48. Pujolar JM, Milan M, Marino IAM et al (2013) Detecting genome-wide gene transcription profiles associated with high pollution burden in the critically endangered European eel. Aquat Toxicol 132–133:157–164. doi: 10.1016/j.aquatox.2013.02.012 CrossRefGoogle Scholar
  49. Rajeswari G, Mog S (2002) Effect of pesticides on the survival of Macrobrachium rosenbergii. Pollut Res 21:25–29Google Scholar
  50. Revathi P, Munuswamy N (2010) Effect of tributyltin on the early embryonic development in the freshwater prawn Macrobrachium rosenbergii (De Man). Chemosphere 79:922–927. doi: 10.1016/j.chemosphere.2010.03.023 CrossRefGoogle Scholar
  51. Routti H, Letcher RJ, Arukwe A et al (2008) Biotransformation of PCBs in relation to phase I and II xenobiotic-metabolizing enzyme activities in ringed seals (Phoca hispida) from Svalbard and the Baltic Sea. Environ Sci Technol 42:8952–8958. doi: 10.1021/es801682f CrossRefGoogle Scholar
  52. Sakuragui MM, Paulino MG, Pereira CDS et al (2013) Integrated use of antioxidant enzymes and oxidative damage in two fish species to assess pollution in man-made hydroelectric reservoirs. Environ Pollut 178:41–51. doi: 10.1016/j.envpol.2013.02.032 CrossRefGoogle Scholar
  53. Sancho E, Ferrando MD, Andreu E (1997) Inhibition of gill Na+/K+-ATPase activity in the eel, Anguilla anguilla, by fenitrothion. Ecotoxicol Environ Saf 38:132–136. doi: 10.1006/eesa.1997.1573 CrossRefGoogle Scholar
  54. Satapornvanit K, Baird DJ, Little DC (2009) Laboratory toxicity test and post-exposure feeding inhibition using the giant freshwater prawn Macrobrachium rosenbergii. Chemosphere 74:1209–1215. doi: 10.1016/j.chemosphere.2008.11.033 CrossRefGoogle Scholar
  55. Shao B, Zhu L, Dong M et al (2012) DNA damage and oxidative stress induced by endosulfan exposure in zebrafish (Danio rerio). Ecotoxicology 21:1533–1540. doi: 10.1007/s10646-012-0907-2 CrossRefGoogle Scholar
  56. Siripatrachai T (1984) Acute toxicity, bioaccumulation and sublethal effects of endrin and carbofuran on the giant freshwater prawns, Macrobrachium rosenbergii De man, p 76Google Scholar
  57. Snell TW, Brogdon SE, Morgan MB (2003) Gene expression profiling in ecotoxicology. Ecotoxicology 12:475–843CrossRefGoogle Scholar
  58. Stara A, Machova J, Velisek J (2012) Effect of chronic exposure to simazine on oxidative stress and antioxidant response in common carp (Cyprinus carpio L.). Environ Toxicol Pharmacol 33:334–343. doi: 10.1016/j.etap.2011.12.019 CrossRefGoogle Scholar
  59. Tanguy A, Boutet I, Laroche J, Moraga D (2005) Molecular identification and expression study of differentially regulated genes in the Pacific oyster Crassostrea gigas in response to pesticide exposure. FEBS J 272:390–403. doi: 10.1111/j.1742-4658.2004.04479.x CrossRefGoogle Scholar
  60. Tu HT, Silvestre F, De Meulder B et al (2012) Combined effects of deltamethrin, temperature and salinity on oxidative stress biomarkers and acetylcholinesterase activity in the black tiger shrimp (Penaeus monodon). Chemosphere 86:83–91. doi: 10.1016/j.chemosphere.2011.09.022 CrossRefGoogle Scholar
  61. Utayopas P (1983) Effect of paraquat, propanil, glyphosate and 2,4-D on the giant freshwater prawn, Macrobrachium rosenbergii De Man 79Google Scholar
  62. Van der Oost R, Beyer J, Vermeulen NPE (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13:57–149CrossRefGoogle Scholar
  63. Vandesompele J, De Preter K, Pattyn F, et al (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:RESEARCH0034Google Scholar
  64. Viarengo A, Lowe D, Bolognesi C et al (2007) The use of biomarkers in biomonitoring: a 2-tier approach assessing the level of pollutant-induced stress syndrome in sentinel organisms. Comp Biochem Physiol C Toxicol Pharmacol 146:281–300. doi: 10.1016/j.cbpc.2007.04.011 CrossRefGoogle Scholar
  65. Willoughby L, Batterham P, Daborn PJ (2007) Piperonyl butoxide induces the expression of cytochrome P450 and glutathione S-transferase genes in Drosophila melanogaster. Pest Manag Sci 63:803–808. doi: 10.1002/ps CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Béatrice Gaume
    • 1
  • Nathalie Dodet
    • 2
  • Jean-Pierre Thomé
    • 2
  • Soazig Lemoine
    • 1
    Email author
  1. 1.DYNECAR-UMR BOREA (MNHN/CNRS 7208/IRD 207/UPMC)Université des Antilles et de la GuyanePointe-à-PitreGuadeloupe
  2. 2.Laboratory of Animal Ecology and Ecotoxicology, CART (Center for Analytical Research and Technology)Université of LiègeSart-TilmanBelgium

Personalised recommendations