Environmental Science and Pollution Research

, Volume 23, Issue 20, pp 20661–20671 | Cite as

Vitellogenin and vitellogenin receptor gene expression and 20-hydroxyecdysone concentration in Macrobrachium rosenbergii exposed to chlordecone

  • Anne Lafontaine
  • Marc Hanikenne
  • Céline Boulangé-Lecomte
  • Joëlle Forget-Leray
  • Jean-Pierre Thomé
  • Eric Gismondi
Research Article


Chlordecone is a persistent organochlorine pesticide widely used in Guadeloupe (French West Indies) to control the banana weevil Cosmopolites sordidus. Although it was previously highlighted that chlordecone may affect the reproduction and growth of vertebrate species, little information is available on the chlordecone effects in invertebrates. The present study investigated the effects of chlordecone on a hormone and a protein having key roles in reproduction and growth of the decapod crustacean Macrobrachium rosenbergii, by measuring the 20-hydroxyecdysone concentration, vitellogenin, and vitellogenin receptor gene expression, as well as the bioconcentration of chlordecone in exposed prawns. First, the results revealed that chlordecone was accumulated in M. rosenbergii. Then, it was found that Vg and VgR gene expression were increased in male and female M. rosenbergii exposed to chlordecone for 90 and 240 days, while the 20-hydroxyecdysone concentrations were decreased. This work suggests that chlordecone accumulates in prawn tissues and could affect key molecules involved in the reproduction and the growth of the invertebrate M. rosenbergii. However, many questions remain unresolved regarding the impacts of chlordecone on growth and reproduction and the signaling pathways responsible for these effects, as well as the potential role of confounding factors present in in situ studies.


Macrobrachium rosenbergii Chlordecone Vitellogenin Vitellogenin receptor 20-Hydroxyecdysone 



The present study was financially supported by grants from the National Research Agency (MACHLOMA, ANR-10-CESA-014, France) and by Belgium funds under a FNRS-F.R.I.A. grant (Fonds pour la Formation à la Recherche dans l’Industrie et dans l’Agriculture). The authors thank Patrick Boucher and François Herman (OCEAN-SA), Nathalie Dodet (LEAE) and Fanny Caupos (INRA) for their help in the establishment of the experiment, and Catherine Adam (LEAE) for her technical assistance.


  1. Anon. (2008) Arrêté du 30 juin 2008 relatif aux limites maximales applicables aux résidus de chlordécone que ne doivent pas dépasser certaines denrées alimentaires d’origine végétale et animale pour être reconnues propres à la consommation humaine. JORF 4 juillet 2008.Google Scholar
  2. Arukwe A, Goksøyr A (2003) Eggshell and egg yolk proteins in fish: hepatic proteins for the next generation: oogenetic, population, and evolutionary implications of endocrine disruption. Comp Hepatol 2:4. doi: 10.1186/1476-5926-2-4 CrossRefGoogle Scholar
  3. ATSDR, Faroon O, Kueberuwa S, Smith L, Derosa C, U.S. Department of Health and Human Services, P.H.S. (1995) Toxicological profile for mirex and chlordecone. Toxicol Ind Heal 11:1–195. doi: 10.1177/074823379501100601 Google Scholar
  4. Billinghurst Z, Clare AS, Matsumura K, Depledge MH (2000) Induction of cypris major protein in barnacle larvae by exposure to 4-n-nonylphenol and 17β-oestradiol. Aquat Toxicol 47:203–212. doi: 10.1016/S0166-445X(99)00018-1 CrossRefGoogle Scholar
  5. Bonan H, Prime J-L (2001) Rapport sur la présence de pesticides dans les eaux de consommation humaine en Guadeloupe. Ministère l’aménagement du Territ. l’environnement pp.86.Google Scholar
  6. Bosker T, Munkittrick KR, Maclatchy DL (2010) Challenges and opportunities with the use of biomarkers to predict reproductive impairment in fishes exposed to endocrine disrupting substances. Aquat Toxicol 100:9–16. doi: 10.1016/j.aquatox.2010.07.003 CrossRefGoogle Scholar
  7. Brooks BW, Turner PK, Stanley JK, Weston JJ, Glidewell EA, Foran CM, Slattery M, La Point TW, Huggett DB (2003) Waterborne and sediment toxicity of fluoxetine to select organisms. Chemosphere 52:135–142. doi: 10.1016/S0045-6535(03)00103-6
  8. Cabidoche YM, Lesueur-Jannoyer M (2012) Contamination of harvested organs in root crops grown on chlordecone-polluted soils. Pedosphere 22:562–571. doi: 10.1016/S1002-0160(12)60041-1 CrossRefGoogle Scholar
  9. Cavelier N (1980) Contamination de la Faune par les pesticides organochlorés. In: Kermarrec A (ed) Niveau actuel de la contamination des chaînes biologiques en Guadeloupe : pesticides et métaux lourds. INRA, contrat n° 7883. ministère de l’Environnement et du Cadr, ParisGoogle Scholar
  10. Chang ES, Mykles DL (2011) Regulation of crustacean molting: a review and our perspectives. Gen Comp Endocrinol 172:323–330. doi: 10.1016/j.ygcen.2011.04.003 CrossRefGoogle Scholar
  11. Chung AC-K, Durica DS, Hopkins PM (1998) Tissue-specific patterns and steady-state concentrations of ecdysteroid receptor and retinoid-X-receptor mRNA during the molt cycle of the fiddler crab, Uca pugilator. Gen Comp Endocrinol 109:375–389. doi: 10.1006/gcen.1997.7046 CrossRefGoogle Scholar
  12. Connon RE, Geist J, Werner I (2012) Effect-based tools for monitoring and predicting the ecotoxicological effects of chemicals in the aquatic Environment. Sensors 12:12741–12771. doi: 10.3390/s120912741 CrossRefGoogle Scholar
  13. Costa LG (2015) Chapter 9 - The neurotoxicity of organochlorine and pyrethroid pesticides. In: Handbook of Clinical Neurology. p 135–148. doi: 10.1016/B978-0-444-62627-1.00009-3
  14. Crane M, Babut M (2007) Environmental quality standards for water framework directive priority substances: challenges and opportunities. Integr Environ Assess Manag 3:290. doi: 10.1897/IEAM_2006-045.1 CrossRefGoogle Scholar
  15. Curtis LR, Beyers RJ (1978) Inhibition of oviposition in the teleost oryzias latipes, induced by subacute kepone exposure. Comp Biochem Physiol Part C Comp Pharmacol 61:15–16. doi: 10.1016/0306-4492(78)90103-X CrossRefGoogle Scholar
  16. Debier C, Pomeroy PP, Dupont C, Joiris C, Comblin V, Le Boulengé E, Larondelle Y, Thomé JP (2003) Quantitative dynamics of PCB transfer from mother to pup during lactation in UK grey seals Halichoerus grypus. Mar Ecol Prog Ser 247:237–248. doi: 10.3354/meps247249 CrossRefGoogle Scholar
  17. Dell S, Sedlmeier D, Bocking D, Dauphin-Villemant C (1999) Ecdysteroid biosynthesis in crayfish Y-organs: feedback regulation by circulating ecdysteroids. Arch Insect Biochem Physiol 41:148–155. doi: 10.1002/(SICI)1520-6327(1999)41:3<148::AID-ARCH6>3.0.CO;2-U CrossRefGoogle Scholar
  18. DIREN Guadeloupe (2003) Cartographie de la contamination par les pesticides des eaux superficielles de Guadeloupe - Direction régionale de l’Environnement - Observatoire des résidus phytosanitaires [WWW Document]., URL.,
  19. Donohoe RM, Curtis LR (1996) Estrogenic activity of chlordecone, o, p’-DDT and o, p’-DDE in juvenile rainbow trout: induction of vitellogenesis and interaction with hepatic estrogen binding sites. Aquat Toxicol 36:31–52. doi: 10.1016/S0166-445X(96)00799-0 CrossRefGoogle Scholar
  20. Flouriot G, Pakdel F, Valotaire Y (1996) Transcriptional and post-transcriptional regulation of rainbow trout estrogen receptor and vitellogenin gene expression. Mol Cell Endocrinol 124:173–183. doi: 10.1016/S0303-7207(96)03960-3 CrossRefGoogle Scholar
  21. Forget-Leray J, Landriau I, Minier C, Leboulenger F (2005) Impact of endocrine toxicants on survival, development, and reproduction of the estuarine copepod Eurytemora affinis (Poppe). Ecotoxicol Environ Saf 60:288–294. doi: 10.1016/j.ecoenv.2004.06.008 CrossRefGoogle Scholar
  22. Gaume B, Dodet N, Thomé JP, Lemoine S (2014) Expression of biotransformation and oxidative stress genes in the giant freshwater prawn Macrobrachium rosenbergii exposed to chlordecone. Environ Sci Pollut Res. doi: 10.1007/s11356-014-3134-y Google Scholar
  23. Ghekiere A, Verslycke T, Janssen C (2006) Effects of methoprene, nonylphenol, and estrone on the vitellogenesis of the mysid Neomysis integer. Gen Comp Endocrinol 147:190–5. doi: 10.1016/j.ygcen.2005.12.021 CrossRefGoogle Scholar
  24. Gismondi E, Thomé JP (2014) Effects of two PBDE congeners on the moulting enzymes of the freshwater amphipod Gammarus pulex. Environ Pollut 191:119–125. doi: 10.1016/j.envpol.2014.04.017 CrossRefGoogle Scholar
  25. Giusti A, Lagadic L, Barsi A, Thomé JP, Joaquim-Justo C, Ducrot V (2014) Investigating apical adverse effects of four endocrine active substances in the freshwater gastropod Lymnaea stagnalis. Sci Total Environ 493:147–155. doi: 10.1016/j.scitotenv.2014.05.130 CrossRefGoogle Scholar
  26. Guldner L, Multigner L, Héraud F, Monfort C, Pierre Thomé J, Giusti A, Kadhel P, Cordier S (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
  27. Guzelian PS (1982) Comparative toxicology of chlordecone (Kepone) in humans and experimental animals. Annu Rev Pharmacol Toxicol 22:89–113. doi: 10.1146/ CrossRefGoogle Scholar
  28. Hammond B, Katzenellenbogen BS, Krauthammer N, McConnell J (1979) Estrogenic activity of the insecticide chlordecone (Kepone) and interaction with uterine estrogen receptors. Proc Natl Acad Sci U S A 76:6641–6645. doi: 10.1073/pnas.76.12.6641 CrossRefGoogle Scholar
  29. Hannas BR, Wang YH, Thomson S, Kwon G, Li H, Leblanc GA (2011) Regulation and dysregulation of vitellogenin mRNA accumulation in daphnids (Daphnia magna). Aquat Toxicol 101:351–7. doi: 10.1016/j.aquatox.2010.11.006 CrossRefGoogle Scholar
  30. Hasegawa Y, Hirose E, Katakura Y (1993) Hormonal control of sexual differentiation and reproduction in Crustacea. Am Zool 33:403–411. doi: 10.1093/icb/33.3.403 CrossRefGoogle Scholar
  31. Hellemans J, Mortier G, De Paepe A, Speleman F, Vandesompele J (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
  32. Henry TB, Kwon J-W, Armbrust KL, Black MC (2004) Acute and chronic toxicity of five selective serotonin reuptake inhibitors in Ceriodaphnia dubia. Environ Toxicol Chem 23:2229–2233. doi: 10.1897/03-278
  33. Huang D-J, Chen H-C (2004) Effects of chlordane and lindane on testosterone and vitellogenin levels in green neon shrimp (Neocaridina denticulata). Int J Toxicol 23:91–5. doi: 10.1080/10915810490435604 CrossRefGoogle Scholar
  34. Huang DJ, Chen HC, Wu JP, Wang SY (2006) Reproduction obstacles for the female green neon shrimp (Neocaridina denticulata) after exposure to chlordane and lindane. Chemosphere 64:11–16. doi: 10.1016/j.chemosphere.2005.12.017 CrossRefGoogle Scholar
  35. Hyne RV (2011) Review of the reproductive biology of amphipods and their endocrine regulation: identification of mechanistic pathways for reproductive toxicants. Environ Toxicol Chem 30:2647–2657. doi: 10.1002/etc.673 CrossRefGoogle Scholar
  36. Jones PD, Tremblay LA, De Coen WM, Glesy JP (2000) Vitellogenin as a biomarker for environmental estrogens. Aust J Ecotoxicol 6:45–58Google Scholar
  37. Jubeaux G, Simon R, Salvador A, Quéau H, Chaumot A, Geffard O (2012) Vitellogenin-like proteins in the freshwater amphipod Gammarus fossarum (Koch, 1835): functional characterization throughout reproductive process, potential for use as an indicator of oocyte quality and endocrine disruption biomarker in males. Aquat Toxicol 112–113:72–82. doi: 10.1016/j.aquatox.2012.01.011 CrossRefGoogle Scholar
  38. Kavlock RJ (1996) Pesticides as endocrine-disrupting chemicals, in: Handbook of pesticide toxicology. U.S. Environmental Protection Agency, Washington DCGoogle Scholar
  39. Keller R, Beyer J (1968) Zur hyperglykämischen Wirkung von Serotonin und Augenstielextrakt beim Flusskrebs Orconectes limosus. Z Vgl Physiol 59:78–85Google Scholar
  40. Kidd KA, Blanchfield PJ, Mills KH, Palace VP, Evans RE, Lazorchak JM, Flick RW (2007) Collapse of a fish population after exposure to a synthetic estrogen. Proc Natl Acad Sci 104:8897–8901. doi: 10.1073/pnas.0609568104 CrossRefGoogle Scholar
  41. Kortenkamp A, Martin O, Faust M, Evans R, Mckinlay R, Orton F, Rosivatz E (2011) State of the art assessment of endocrine disrupters. European Commission, BrusselsGoogle Scholar
  42. Kulkarni G, Glade L (1991) Oogenesis and effects of neuroendocrine tissues on in vitro synthesis of protein by the ovary of the red swamp crayfish Procambarus clarkii (Girard). J Crustac Biol 11(4):513–522CrossRefGoogle Scholar
  43. Kusk KO, Wollenberger L (2007) Towards an internationally harmonized test method for reproductive and developmental effects of endocrine disrupters in marine copepods. Ecotoxicology 16:183–195. doi: 10.1007/s10646-006-0112-2 CrossRefGoogle Scholar
  44. Lafontaine A, Gismondi E, Boulangé-Lecomte C, Geraudie P, Dodet N, Caupos F, Lemoine S, Lagadic L, Thomé J-P, Forget-Leray J (2016) Effects of chlordecone on 20-hydroxyecdysone concentration and chitobiase activity in a decapod crustacean, Macrobrachium rosenbergii. Aquat Toxicol 176:53–63. doi: 10.1016/j.aquatox.2016.04.006 CrossRefGoogle Scholar
  45. LeBlanc G a, Mu X, Rider CV (2000) Embryotoxicity of the alkylphenol degradation product 4-nonylphenol to the crustacean Daphnia magna. Environ Health Perspect 108:1133–1138. doi: 10.1289/ehp.001081133 CrossRefGoogle Scholar
  46. LeBlanc GA (2007) Crustacean endocrine toxicology: a review. Ecotoxicology 16:61–81. doi: 10.1007/s10646-006-0115-z CrossRefGoogle Scholar
  47. Lee K-W, Hwang D-S, Rhee J-S, Ki J-S, Park HG, Ryu J-C, Raisuddin S, Lee J-S (2008) Molecular cloning, phylogenetic analysis and developmental expression of a vitellogenin (Vg) gene from the intertidal copepod Tigriopus japonicus. Comp Biochem Physiol B Biochem Mol Biol 150:395–402. doi: 10.1016/j.cbpb.2008.04.009 CrossRefGoogle Scholar
  48. Martín-Díaz ML, Villena-Lincoln A, Bamber S, Blasco J, DelValls TA (2005) An integrated approach using bioaccumulation and biomarker measurements in female shore crab, Carcinus maenas. Chemosphere 58:615–26. doi: 10.1016/j.chemosphere.2004.08.072 CrossRefGoogle Scholar
  49. Mattson MP, Spaziani E (1985) Characterization of molt-inhibiting hormone (MIH) action on crustacean Y-organ segments and dispersed cells in culture and a bioassay for MIH activity. J Exp Zool 236:93–101. doi: 10.1002/jez.1402360113
  50. Mazurová E, Hilscherová K, Triebskorn R, Köhler H-R, Maršálek B, Bláha L (2008) Endocrine regulation of the reproduction in crustaceans: Identification of potential targets for toxicants and environmental contaminants. Biologia. 63:139–150. doi: 10.2478/s11756-008-0027-x
  51. Ministère de l’Écologie du Développement durable et de l’Énergie, (2015a). JORF n°0198 28/08/2015 - DEVL1513989A - Arrêté du 27 juillet 2015 modifiant l’arrêté du 25 janvier 2010 relatif aux méthodes et critères d’évaluation de l’état écologique, de l’état chimique et du potentiel écologique des eaux de surface pris en appl.Google Scholar
  52. Ministère de l’Écologie du Développement durable et de l’Énergie (2015a) JORF n°0260 08/11/2015 - DEVL1525745V - Avis relatif aux limites de quantification des couples « paramètre-matrice » de l’agrément des laboratoires effectuant des analyses dans le domaine de l’eau et des milieux aquatiques. Journal Officiel De La République, FRANÇAISEGoogle Scholar
  53. Monti D (2007) Evaluation de la biocontamination en Chlordecone, β-Hexachlorocyclohexane et Cadusaphos de Crustacés et Poissons d’eau douce en Guadeloupe, Ministère de l’Ecologie, du Développement et de l’Aménagement durables. Ministère de l’Ecologie, du Développement et de l’Aménagement durablesGoogle Scholar
  54. Multigner L, Ndong JR, Giusti A, Romana M, Delacroix-Maillard H, Cordier S, Jégou B, Thome JP, Blanchet P (2010) Chlordecone exposure and risk of prostate cancer. J Clin Oncol 28:3457–3462. doi: 10.1200/JCO.2009.27.2153 CrossRefGoogle Scholar
  55. New MB (2002) Farming freshwater prawns: a manual for the culture of the giant river prawn (Macrobrachium Rosenbergii)., Food and Agriculture - Organization of the United NationsGoogle Scholar
  56. Newhouse K, Berner T, Mukerjee D, Rooney A (2009) IRIS toxicological review of chlordecone (Kepone), U.S. Environmental Protection Agency. U.S. Environmental Protection Agency, Washington DCGoogle Scholar
  57. Oberdörster E, Rice CD, Irwin LK (2000) Purification of vitellin from grass shrimp Palaemonetes pugio, generation of monoclonal antibodies, and validation for the detection of lipovitellin in Crustacea. Comp Biochem Physiol Part C Pharmacol Toxicol Endocrinol 127:199–207. doi: 10.1016/S0742-8413(00)00146-8 CrossRefGoogle Scholar
  58. Qiu G-F, Zheng L, Liu P (2008) Transcriptional regulation of ferritin mRNA levels by iron in the freshwater giant prawn, Macrobrachium rosenbergii. Comp Biochem Physiol B Biochem Mol Biol 150:320–5. doi: 10.1016/j.cbpb.2008.03.016 CrossRefGoogle Scholar
  59. Raikhel AS, Dhadialla TS (1992) Accumulation of yolk proteins in insect oocytes. Annu Rev Entomol 37:217–51. doi: 10.1146/annurev.en.37.010192.001245 CrossRefGoogle Scholar
  60. Rodriguez EM, Medesani DA, Fingerman M (2007) Endocrine disruption in crustaceans due to pollutants: a review. Comp Biochem Physiol - A Mol Integr Physiol 146:661–671. doi: 10.1016/j.cbpa.2006.04.030 CrossRefGoogle Scholar
  61. Roth Z, Khalaila I (2012) Identification and characterization of the vitellogenin receptor in Macrobrachium rosenbergii and its expression during vitellogenesis. Mol Reprod Dev 79:478–487. doi: 10.1002/mrd.22055 CrossRefGoogle Scholar
  62. Ruijter JM, Ramakers C, Hoogaars WMH, Karlen Y, Bakker O, van den Hoff MJB, Moorman AFM (2009) Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Res 37:e45. doi: 10.1093/nar/gkp045 CrossRefGoogle Scholar
  63. Ruttanakorn S, Meeratana P, Chetawan K, Hanna P (2014) Induction of ovarian development and sex differentiation in the giant freshwater prawn Macrobrachium rosenbergii, by serotonin, methyl farnesoate, and phytoecdysone. J Sci Technol Humanit 11:77–86Google Scholar
  64. SANCO/12571/2013 European commission, n.d. Guidance document on analytical quality control and validation procedures for pesticide residues analysis in food and feed. Health and Consumer Protection—Safety of the food chain: Chemicals, contaminants, pesticidesGoogle Scholar
  65. Sanders MB, Billinghurst Z, Depledge MH, Clare AS (2005) Larval development and vitellin-like protein expression in Palaemon elegans larvae following xeno-oestrogen exposure. Integr Comp Biol 45:51–60. doi: 10.1093/icb/45.1.51 CrossRefGoogle Scholar
  66. Sappington TW, Raikhel AS (1998) Molecular characteristics of insect vitellogenins and vitellogenin receptors. Insect Biochem Mol Biol 28:277–300. doi: 10.1016/S0965-1748(97)00110-0 CrossRefGoogle Scholar
  67. Schonbaum CP, Lee S, Mahowald AP (1995) The Drosophila yolkless gene encodes a vitellogenin receptor belonging to the low density lipoprotein receptor superfamily. Proc Natl Acad Sci 92:1485–1489. doi: 10.1073/pnas.92.5.1485 CrossRefGoogle Scholar
  68. Scott AP (2013) Do mollusks use vertebrate sex steroids as reproductive hormones? II. Critical review of the evidence that steroids have biological effects. Steroids 78:268–81. doi: 10.1016/j.steroids.2012.11.006 CrossRefGoogle Scholar
  69. Shrivastava S, Princy SA (2014) Crustacean hyperglycemic hormone family neurohormones: a prevailing tool to decipher the physiology of crustaceans. Indian J Mar Sci 43:434–440Google Scholar
  70. Snegaroff J (1977) Les résidus d’insecticides organochlorés dans les sols et les rivières de la région bananière de Guadeloupe. Phytiatr Phytopharm 26:251–268Google Scholar
  71. Snyder MJ, Mulder EP (2001) Environmental endocrine disruption in decapod crustacean larvae: hormone titers, cytochrome P450, and stress protein responses to heptachlor exposure. Aquat Toxicol 55:177–190. doi: 10.1016/s0166-445x(01)00173-4 CrossRefGoogle Scholar
  72. Soroka Y, Milner Y, Sagi A (2000) The hepatopancreas as a site of yolk protein synthesis in the prawn Macrobrachium rosenbergii. Invertebr Reprod Dev 37:61–68. doi: 10.1080/07924259.2000.9652400 CrossRefGoogle Scholar
  73. Subramoniam T (2011) Mechanisms and control of vitellogenesis in crustaceans. Fish Sci 77:1–21. doi: 10.1007/s12562-010-0301-z CrossRefGoogle Scholar
  74. Sumpter JP, Jobling S (1995) Vitellogenesis as a biomarker for estrogenic contamination of the aquatic environment. Environ Health Perspect 103:173–178. doi: 10.1289/ehp.95103s7173 CrossRefGoogle Scholar
  75. Techa S, Chung JS (2015) Ecdysteroids regulate the levels of molt-inhibiting hormone (MIH) expression in the blue crab, Callinectes sapidus. PLoS One 10:e0117278. doi: 10.1371/journal.pone.0117278 CrossRefGoogle Scholar
  76. Techa S, Chung JS (2013) Ecdysone and retinoid-X receptors of the blue crab, Callinectes sapidus: cloning and their expression patterns in eyestalks and Y-organs during the molt cycle. Gene 527:139–153. doi: 10.1016/j.gene.2013.05.035 CrossRefGoogle Scholar
  77. Thomson SA, Baldwin WS, Wang YH, Kwon G, LeBlanc GA (2009) Annotation, phylogenetics, and expression of the nuclear receptors in Daphnia pulex. BMC Genomics 10:500. doi: 10.1186/1471-2164-10-500 CrossRefGoogle Scholar
  78. Thornton J, Need E, Crews D (2003) Resurrecting the ancestral steroid receptor: ancient origin of estrogen signaling. Science 301:1714–7. doi: 10.1126/science.1086185 CrossRefGoogle Scholar
  79. Tinikul Y, Joffre Mercier A, Soonklang N, Sobhon P (2008) Changes in the levels of serotonin and dopamine in the central nervous system and ovary, and their possible roles in the ovarian development in the giant freshwater prawn, Macrobrachium rosenbergii. Gen Comp Endocrinol 158:250–258. doi: 10.1016/j.ygcen.2008.07.009 CrossRefGoogle Scholar
  80. Tiu SHK, Benzie J, Chan S-M (2008) From hepatopancreas to ovary: molecular characterization of a shrimp vitellogenin receptor involved in the processing of vitellogenin. Biol Reprod 79:66–74. doi: 10.1095/biolreprod.107.066258 CrossRefGoogle Scholar
  81. Tokishita S-I, Kato Y, Kobayashi T, Nakamura S, Ohta T, Yamagata H (2006) Organization and repression by juvenile hormone of a vitellogenin gene cluster in the crustacean, Daphnia magna. Biochem Biophys Res Commun 345:362–70. doi: 10.1016/j.bbrc.2006.04.102 CrossRefGoogle Scholar
  82. Tyler CR, van der Eerden B, Jobling S, Panter G, Sumpter JP (1996) Measurement of vitellogenin, a biomarker for exposure to oestrogenic chemicals, in a wide variety of cyprinid fish. J Comp Physiol B 166:418–426. doi: 10.1007/BF02337886 CrossRefGoogle Scholar
  83. Young NJ, Webster SG, Rees HH (1993) Ecdysteroid profiles and vitellogenesis in Penaeus monodon (Crustacea: Decapoda). Invertebr Reprod Dev 24:107–117. doi: 10.1080/07924259.1993.9672340 CrossRefGoogle Scholar
  84. Zhong L, Yuan L, Rao Y, Li Z, Zhang X, Liao T, Xu Y, Dai H (2014) Distribution of vitellogenin in zebrafish (Danio rerio) tissues for biomarker analysis. Aquat Toxicol 149:1–7. doi: 10.1016/j.aquatox.2014.01.022 CrossRefGoogle Scholar
  85. Zou E (2005) Impacts of xenobiotics on crustacean molting: the invisible endocrine disruption. Integr Comp Biol 45:33–38. doi: 10.1093/icb/45.1.33 CrossRefGoogle Scholar
  86. Zou E, Fingerman M (1999) Effects of exposure to diethyl phthalate, 4-(tert)-octylphenol, and 2,4,5-trichlorobiphenyl on activity of chitobiase in the epidermis and hepatopancreas of the fiddler crab, Uca pugilator. Comp Biochem Physiol Part C Pharmacol Toxicol Endocrinol 122:115–120CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Anne Lafontaine
    • 1
  • Marc Hanikenne
    • 2
    • 3
  • Céline Boulangé-Lecomte
    • 4
  • Joëlle Forget-Leray
    • 4
  • Jean-Pierre Thomé
    • 1
  • Eric Gismondi
    • 1
  1. 1.Laboratory of Animal Ecology and Ecotoxicology (LEAE), Centre of Analytical Research and Technology (CART)University of LiègeLiègeBelgium
  2. 2.Center for Protein Engineering, Functional Genomics and Plant Molecular ImagingUniversity of LiègeLiègeBelgium
  3. 3.PhytoSYSTEMSUniversity of LiègeLiègeBelgium
  4. 4.Normandie University, ULH, UMR I-02 SEBIO, FR CNRS 3730 SCALELe HavreFrance

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