[en] The present work is the first study investigating the impacts
of chlordecone, an organochlorine insecticide, on the proteome of the
decapod crustacean Macrobrachium rosenbergii, by gel-free proteomic
analysis of the hepatopancreas protein expression variations in organisms
exposed to three environmental relevant concentrations of chlordecone
(i.e. 0.2, 2 and 20 μg/L). Results revealed that 62 proteins were
significantly up- or down-regulated in exposed prawns compared to
controls. Most of these proteins are involved in important physiological
processes such as ion transport, defense mechanisms and immune system,
cytoskeleton dynamics, or protein synthesis and degradation. Moreover, it
appears that 6% of the deregulated protein are involved in the endocrine
system and in the hormonal control of reproduction or development
processes of M. rosenbergii (e.g. vitellogenin, farnesoic acid omethyltransferase).
These results indicate that chlordecone is
potentially an endocrine disruptor compound for decapods, as already
observed in vertebrates. These protein modifications could lead to
disruptions of growth and reproduction of M. rosenbergii, and therefore
of the fitness population on the long-term. Besides, these disrupted
proteins could be suggested as biomarkers of exposure for endocrine
disruptions in invertebrates. However, further investigations are needed
to complete understanding of action mechanisms of chlordecone on proteome
and endocrine system of crustaceans.
Disciplines :
Environmental sciences & ecology
Author, co-author :
Lafontaine, Anne ; Université de Liège > Département de Biologie, Ecologie et Evolution > Ecologie animale et écotoxicologie
Abdu, U., Takac, P., Laufer, H., Sagi, A., Effect of methyl farnesoate on late larval development and metamorphosis in the prawn macrobrachium rosenbergii (Decapoda, Palaemonidae): a juvenoid-like effect?. Biol. Bull. 195 (1998), 1112–1119.
Ankley, G.T., Bencic, D.C., Breen, M.S., Collette, T.W., Conolly, R.B., Denslow, N.D., Edwards, S.W., Ekman, D.R., Garcia-Reyero, N., Jensen, K.M., Lazorchak, J.M., Martinović, D., Miller, D.H., Perkins, E.J., Orlando, E.F., Villeneuve, D.L., Wang, R.-L., Watanabe, K.H., Endocrine disrupting chemicals in fish: developing exposure indicators and predictive models of effects based on mechanism of action. Aquat. Toxicol. 92 (2009), 168–178, 10.1016/j.aquatox.2009.01.013.
Baggerman, G., Vierstraete, E., De Loof, A., Schoofs, L., Gel-based versus gel-free proteomics: a review. Comb. Chem. High. Throughput Screen. 8 (2005), 669–677, 10.2174/138620705774962490.
Bai, H., Qiao, H., Li, F., Fu, H., Jiang, S., Zhang, W., Yan, Y., Xiong, Y., Sun, S., Jin, S., Gong, Y., Wu, Y., Molecular and functional characterization of the vitellogenin receptor in oriental river prawn, Macrobrachium nipponense. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 194 (2016), 45–55, 10.1016/j.cbpa.2015.12.008.
Bansal, S.K., Desaiah, D., Chlordecone toxicity: effect of withdrawal of treatment on ATPase inhibition. Neurotoxicology 6 (1985), 103–107.
Billinghurst, Z., Clare, A.S., Matsumura, K., Depledge, M.H., Induction of cypris major protein in barnacle larvae by exposure to 4-n-nonylphenol and 17β-oestradiol. Aquat. Toxicol. 47 (2000), 203–212, 10.1016/S0166-445X(99)00018-1.
Boulangé-Lecomte, C., Rocher, B., Cailleaud, K., Cosette, P., Legrand, E., Devreker, D., Budzinski, H., Souissi, S., Forget-Leray, J., Differential protein expression in the estuarine copepod Eurytemora affinis after diuron and alkylphenol exposures. Environ. Toxicol. Chem. 35 (2016), 1860–1871, 10.1002/etc.3343.
Cabidoche, Y.M., Lesueur-Jannoyer, M., Contamination of harvested organs in root crops grown on chlordecone-polluted soils. Pedosphere 22 (2012), 562–571, 10.1016/S1002-0160(12)60041-1.
Cao, A., Fuentes, J., Comesaña, P., Casas, S.M., Villalba, A., A proteomic approach envisaged to analyse the bases of oyster tolerance/resistance to bonamiosis. Aquaculture 295 (2009), 149–156, 10.1016/j.aquaculture.2009.06.044.
Cao, J.X., Dai, J.Q., Dai, Z.M., Yin, G.L., Yang, W.J., A male reproduction-related Kazal-type peptidase inhibitor gene in the prawn, Macrobrachium rosenbergii: molecular characterization and expression patterns. Mar. Biotechnol. 9 (2007), 45–55, 10.1007/s10126-006-6026-4.
Cavelier, N., Contamination de la Faune par les pesticides organochlorés. Kermarrec, A., (eds.) Niveau actuel de la contamination des chaînes biologiques en Guadeloupe: pesticides et métaux lourds. INRA, contrat n° 7883., 1980, Ministère de l′Environnement et du Cadr, Paris.
Chan, S.-M., Mak, A.S.C., Choi, C.L., Ma, T.H.T., Hui, J.H.L., Tiu, S.H.K., Vitellogenesis in the red crab, Charybdis feriatus: contributions from small vitellogenin transcripts (CfVg) and farnesoic acid stimulation of CfVg expression. Ann. N. Y. Acad. Sci. 1040 (2005), 74–79, 10.1196/annals.1327.008.
Chang, E., Bruce, M., Tamone, S., Regulation of crustacean molting: a multi-hormonal system. Am. Zool., 1993.
Chang, E.S., Physiological and biochemical changes during the molt cycle in decapod crustaceans: an overview. J. Exp. Mar. Biol. Ecol. 193 (1995), 1–14, 10.1016/0022-0981(95)00106-9.
Clostre, F., Woignier, T., Rangon, L., Fernandes, P., Soler, A., Lesueur-Jannoyer, M., Field validation of chlordecone soil sequestration by organic matter addition. J. Soils Sediment. 14 (2013), 23–33, 10.1007/s11368-013-0790-3.
Curtis, L.R., Beyers, R.J., Inhibition of oviposition in the teleost Oryzias latipes, induced by subacute kepone exposure. Comp. Biochem. Physiol. Part C. Comp. Pharmacol. 61 (1978), 15–16, 10.1016/0306-4492(78)90103-X.
Desaiah, D., Koch, R.B., Inhibition of ATPases activity in channel catfish brain by Kepone and its reduction product. Bull. Environ. Contam. Toxicol. 13 (1975), 153–158, 10.1007/BF01721729.
Donohoe, R.M., Curtis, L.R., 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 (1996), 31–52, 10.1016/S0166-445X(96)00799-0.
Duan, Y., Liu, P., Li, J., Wang, Y., Li, J., Chen, P., A farnesoic acid O-methyltransferase (FAMeT) from Exopalaemon carinicauda is responsive to Vibrio anguillarum and WSSV challenge. Cell Stress Chaperon-. 19 (2014), 367–377, 10.1007/s12192-013-0464-5.
Eroschenko, V.P., Estrogenic activity of the insecticide chlordecone in the reproductive tract of birds and mammals. J. Toxicol. Environ. Health 8 (1981), 731–742, 10.1080/15287398109530109.
Fercha, A., Capriotti, A.L., Caruso, G., Cavaliere, C., Gherroucha, H., Samperi, R., Stampachiacchiere, S., Lagana, A., Gel-free proteomics reveal potential biomarkers of priming-induced salt tolerance in durum wheat. J. Proteom. 91 (2013), 486–499, 10.1016/j.jprot.2013.08.010.
Flouriot, G., Pakdel, F., Valotaire, Y., Transcriptional and post-transcriptional regulation of rainbow trout estrogen receptor and vitellogenin gene expression. Mol. Cell. Endocrinol. 124 (1996), 173–183, 10.1016/S0303-7207(96)03960-3.
Gaume, B., Dodet, N., Thomé, J.P., Lemoine, S., Expression of biotransformation and oxidative stress genes in the giant freshwater prawn Macrobrachium rosenbergii exposed to chlordecone. Environ. Sci. Pollut. Res., 2014, 10.1007/s11356-014-3134-y.
Ghekiere, A., Verslycke, T., Janssen, C., Effects of methoprene, nonylphenol, and estrone on the vitellogenesis of the mysid Neomysis integer. Gen. Comp. Endocrinol. 147 (2006), 190–195, 10.1016/j.ygcen.2005.12.021.
Gismondi, E., Mazzucchelli, G., De Pauw, E., Joaquim-Justo, C., Thomé, J.P., Gender differences in responses in Gammarus pulex exposed to BDE-47: a gel-free proteomic approach. Ecotoxicol. Environ. Saf. 122 (2015), 205–213, 10.1016/j.ecoenv.2015.07.038.
Giusti, A., Leprince, P., Mazzucchelli, G., Thomé, J.P., Lagadic, L., Ducrot, V., Joaquim-Justo, C., Proteomic analysis of the reproductive organs of the hermaphroditic gastropod Lymnaea stagnalis exposed to different endocrine disrupting chemicals. PLoS One, 2013, 8, 10.1371/journal.pone.0081086.
Giusti, A., Lagadic, L., Barsi, A., Thomé, J.P., Joaquim-Justo, C., Ducrot, V., Investigating apical adverse effects of four endocrine active substances in the freshwater gastropod Lymnaea stagnalis. Sci. Total Environ. 493 (2014), 147–155, 10.1016/j.scitotenv.2014.05.130.
Gomiero, A., Pampanin, D.M., Bjørnstad, A., Larsen, B.K., Provan, F., Lyng, E., Andersen, O.K., An ecotoxicoproteomic approach (SELDI-TOF mass spectrometry) to biomarker discovery in crab exposed to pollutants under laboratory conditions. Aquat. Toxicol. 78 (2006), S34–S41, 10.1016/j.aquatox.2006.02.013.
Görg, A., Weiss, W., Dunn, M.J., Current two-dimensional electrophoresis technology for proteomics. Proteomics 4 (2004), 3665–3685, 10.1002/pmic.200401031.
GREPP, 2004. Rapport d′activités 2001–2004. Programme d′actions 2005.
Guzelian, P.S., Comparative toxicology of chlordecone (Kepone) in humans and experimental animals. Annu. Rev. Pharmacol. Toxicol. 22 (1982), 89–113, 10.1146/annurev.pa.22.040182.000513.
Hammond, B., Katzenellenbogen, B.S., Krauthammer, N., McConnell, J., Estrogenic activity of the insecticide chlordecone (Kepone) and interaction with uterine estrogen receptors. Proc. Natl. Acad. Sci. USA 76 (1979), 6641–6645, 10.1073/pnas.76.12.6641.
Horion, S., Thomé, J.P., Gismondi, E., Changes in antitoxic defense systems of the freshwater amphipod Gammarus pulex exposed to BDE-47 and BDE-99. Ecotoxicology 24:4 (2015), 959–966, 10.1007/s10646-015-1438-4.
Huang, D.J., Chen, H.C., Wu, J.P., Wang, S.Y., Reproduction obstacles for the female green neon shrimp (Neocaridina denticulata) after exposure to chlordane and lindane. Chemosphere 64 (2006), 11–16, 10.1016/j.chemosphere.2005.12.017.
Huang, D.-J., Chen, H.-C., Effects of chlordane and lindane on testosterone and vitellogenin levels in green neon shrimp (Neocaridina denticulata). Int. J. Toxicol. 23 (2004), 91–95, 10.1080/10915810490435604.
Hyne, R.V., Review of the reproductive biology of amphipods and their endocrine regulation: identification of mechanistic pathways for reproductive toxicants. Environ. Toxicol. Chem. 30 (2011), 2647–2657, 10.1002/etc.673.
InVS-Inserm, 2009. Impact sanitaire de l'utilisation du chlordécone aux Antilles françaises – Recommandations pour les recherches et les actions de santé publique – Octobre 2009. Saint-Maurice (Fra) : Institut de veille sanitaire, mars 2010, p. 96. (Available on)〈 www.invs.sa〉.
James, M.O., Boyle, S.M., Cytochromes P450 in crustacea. Comp. Biochem. Physiol. Part C. Pharmacol. Toxicol. Endocrinol. 121 (1998), 157–172, 10.1016/S0742-8413(98)10036-1.
Jasmani, S., Ohira, T., Jayasankar, V., Tsutsui, N., Aida, K., Wilder, M.N., Localization of vitellogenin mRNA expression and vitellogenin uptake during ovarian maturation in the giant freshwater prawn Macrobrachium rosenbergii. J. Exp. Zool. A. Comp. Exp. Biol. 301 (2004), 334–343, 10.1002/jez.a.20044.
Jubeaux, G., Simon, R., Salvador, A., Quéau, H., Chaumot, A., Geffard, O., 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 (2012), 72–82, 10.1016/j.aquatox.2012.01.011.
Kloas, W., Urbatzka, R., Opitz, R., Würtz, S., Behrends, T., Hermelink, B., Hofmann, F., Jagnytsch, O., Kroupova, H., Lorenz, C., Neumann, N., Pietsch, C., Trubiroha, A., Van Ballegooy, C., Wiedemann, C., Lutz, I., Endocrine Disruption in Aquatic Vertebrates. Ann. N. Y. Acad. Sci. 1163 (2009), 187–200, 10.1111/j.1749-6632.2009.04453.x.
Koenig, S., Fernández, P., Solé, M., Differences in cytochrome P450 enzyme activities between fish and crustacea: relationship with the bioaccumulation patterns of polychlorobiphenyls (PCBs). Aquat. Toxicol. 108 (2012), 11–17, 10.1016/j.aquatox.2011.10.016.
Kusk, K.O., Wollenberger, L., Towards an internationally harmonized test method for reproductive and developmental effects of endocrine disrupters in marine copepods. Ecotoxicology 16 (2007), 183–195, 10.1007/s10646-006-0112-2.
Lafontaine, A., Gismondi, E., Boulangé-Lecomte, C., Geraudie, P., Dodet, N., Caupos, F., Lemoine, S., Lagadic, L., Thomé, J.-P., Forget-Leray, J., Effects of chlordecone on 20-hydroxyecdysone concentration and chitobiase activity in a decapod crustacean, Macrobrachium rosenbergii. Aquat. Toxicol. 176 (2016), 53–63, 10.1016/j.aquatox.2016.04.006.
Lafontaine, A., Hanikenne, M., Boulangé-Lecomte, C., Forget-Leray, J., Thomé, J.-P., Gismondi, E., Vitellogenin and vitellogenin receptor gene expression and 20-hydroxyecdysone concentration in Macrobrachium rosenbergii exposed to chlordecone. Environ. Sci. Pollut. Res., 2016, 1–11, 10.1007/s11356-016-7273-1.
Legrand, E., Forget-Leray, J., Duflot, A., Olivier, S., Thomé, J.-P., Danger, J.-M., Boulangé-Lecomte, C., Transcriptome analysis of the copepod Eurytemora affinis upon exposure to endocrine disruptor pesticides: focus on reproduction and development. Aquat. Toxicol. 176 (2016), 64–75, 10.1016/j.aquatox.2016.04.010.
Lemos, M.F.L., Cristina Esteves, A., Samyn, B., Timperman, I., van Beeumen, J., Correia, A., van Gestel, C.A.M., Soares, A.M.V.M., Protein differential expression induced by endocrine disrupting compounds in a terrestrial isopod. Chemosphere 79 (2010), 570–576, 10.1016/j.chemosphere.2010.01.055.
Leung, P.T.Y., Wang, Y., Mak, S.S.T., Ng, W.C., Leung, K.M.Y., Differential proteomic responses in hepatopancreas and adductor muscles of the green-lipped mussel Perna viridis to stresses induced by cadmium and hydrogen peroxide. Aquat. Toxicol. 105 (2011), 49–61, 10.1016/j.aquatox.2011.05.010.
Li, Y., Ma, W.M., Dai, J.Q., Feng, C.Z., Yang, F., Ohira, T., Nagasawa, H., Yang, W.J., Inhibition of a novel sperm gelatinase in prawn sperm by the male reproduction-related kazal-type peptidase inhibitor. Mol. Reprod. Dev. 75 (2008), 1327–1337, 10.1002/mrd.20872.
Li, Y., Qian, Y.Q., Ma, W.M., Yang, W.J., Inhibition mechanism and the effects of structure on activity of Male Reproduction-Related Peptidase Inhibitor Kazal-Type (MRPINK) of Macrobrachium rosenbergii. Mar. Biotechnol. 11 (2009), 252–259, 10.1007/s10126-008-9140-7.
Li, Z., Xu, X., Wang, J., Wang, C., Possible Roles of Farnesoic Acid O -Methyltransferase in Regulation of Molting in the Shrimp, Penaeus Chinensis. J. World Aquac. Soc. 44 (2013), 826–834, 10.1111/jwas.12083.
Mahaffey, W.R., Pritchard, P.H., Bourquin, a.W., Effects of Kepone on growth and respiration of several estuarine bacteria. Appl. Environ. Microbiol. 43 (1982), 1419–1424, 10.1016/0198-0254(82)90405-8.
Mak, A.S.C., Choi, C.L., Tiu, S.H.K., Hui, J.H.L., He, J.G., Tobe, S.S., Chan, S.M., Vitellogenesis in the red crab Charybdis feriatus: hepatopancreas-specific expression and farnesoic acid stimulation of vitellogenin gene expression. Mol. Reprod. Dev. 70 (2005), 288–300, 10.1002/mrd.20213.
Makkapan, W., Maikaeo, L., Miyazaki, T., Chotigeat, W., Molecular mechanism of serotonin via methyl farnesoate in ovarian development of white shrimp: Fenneropenaeus merguiensis de Man. Aquaculture 321 (2011), 101–107, 10.1016/j.aquaculture.2011.08.016.
Matozzo, V., Gagné, F., Marin, M.G., Ricciardi, F., Blaise, C., Vitellogenin as a biomarker of exposure to estrogenic compounds in aquatic invertebrates: a review. Environ. Int. 34 (2008), 531–545, 10.1016/j.envint.2007.09.008.
Matsumoto, T., Osada, M., Osawa, Y., Mori, K., Gonadal Estrogen Profile and Immunohistochemical Localization of Steroidogenic Enzymes in the Oyster and Scallop during Sexual Maturation. Comp. Biochem. Physiol. Part B Biochem. Mol. Biol. 118 (1997), 811–817, 10.1016/S0305-0491(97)00233-2.
Meyer-Reil, L.-A., Köster, M., Eutrophication of marine waters: effects on Benthic microbial communities. Mar. Pollut. Bull. 41 (2000), 255–263, 10.1016/S0025-326X(00)00114-4.
Mishra, S.K., Koury, M., Desaiah, D., Inhibition of calcium ATPase activity in rat brain and muscle by chlordecone. Bull. Environ. Contam. Toxicol. 25 (1980), 262–268, 10.1007/BF01985522.
Nagaraju, G.P.C., Is methyl farnesoate a crustacean hormone?. Aquaculture 272 (2007), 39–54, 10.1016/j.aquaculture.2007.05.014.
New, M.B., Farming Freshwater Prawns: a Manual for the Culture of the Giant River Prawn (Macrobrachium rosenbergii). 2002, Food and Agriculture - Organization of the United Nations.
Newhouse, K., Berner, T., Mukerjee, D., Rooney, A., IRIS Toxicological Review of Chlordecone (Kepone), U.S. Environmental Protection Agency. 2009, U.S. Environmental Protection Agency, Washington DC.
Oberdörster, E., Cheek, A.O., Gender benders at the beach: endocrine disruption in marine and estuarine organisms. Environ. Toxicol. Chem. 20 (2001), 23–36, 10.1002/etc.5620200103.
Oberdörster, E., Rice, C.D., Irwin, L.K., 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 (2000), 199–207, 10.1016/S0742-8413(00)00146-8.
Oetken, M., Bachmann, J., Schulte-Oehlmann, U., Oehlmann, J., Evidence for Endocrine Disruption in Invertebrates, in: International Review of Cytology. 2004, Academic Press, 1–44.
Olmstead, A.W., Leblanc, G.A., Juvenoid hormone methyl farnesoate is a sex determinant in the crustacean Daphnia magna. J. Exp. Zool. 293 (2002), 736–739, 10.1002/jez.10162.
Qian, Y.Q., Li, Y., Yang, F., Yu, Y.Q., Yang, J.S., Yang, W.J., Two Kazal-type protease inhibitors from Macrobrachium nipponense and Eriocheir sinensis: comparative analysis of structure and activities. Fish. Shellfish Immunol. 32 (2012), 446–458, 10.1016/j.fsi.2011.12.006.
Qian, Z., He, S., Liu, T., Liu, Y., Hou, F., Liu, Q., Wang, X., Mi, X., Wang, P., Liu, X., Identification of ecdysteroid signaling late-response genes from different tissues of the Pacific white shrimp, Litopenaeus vannamei. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 172 (2014), 10–30, 10.1016/j.cbpa.2014.02.011.
Rider, C.V., Gorr, T.A., Olmstead, A.W., Wasilak, B.A., LeBlanc, G.A., Stress signaling: coregulation of hemoglobin and male sex determination through a terpenoid signaling pathway in a crustacean. J. Exp. Biol. 208 (2005), 15–23, 10.1242/jeb.01343.
Ringwood, H.A., Hameedi, M.J., Lee, R.F., Brouwer, M., Peters, E.C., Scott, G.I., Luoma, S.N., Digiulio, R.T., 2008. Bivalve Biomarker Workshop: overview and discussion group summaries. Biomarkers.
Rodriguez, E.M., Medesani, D.A., Fingerman, M., Endocrine disruption in crustaceans due to pollutants: a review. Comp. Biochem. Physiol. - A Mol. Integr. Physiol. 146 (2007), 661–671, 10.1016/j.cbpa.2006.04.030.
Rodríguez-Ortega, M.J., Alhama, J., Funes, V., Romero-Ruíz, A., Rodríguez-Ariza, A., López-Barea, J., Biochemical biomarkers of pollution in the clam Chamaelea gallina from South-Spanish littoral. Environ. Toxicol. Chem. 21 (2002), 542–549, 10.1002/etc.5620210311.
Rodríguez-Ortega, M.J., Grøsvik, B.E., Rodríguez-Ariza, A., Goksøyr, A., López-Barea, J., Changes in protein expression profiles in bivalve molluscs (Chamaelea gallina) exposed to four model environmental pollutants. Proteomics 3 (2003), 1535–1543, 10.1002/pmic.200300491.
Sanchez, B.C., Ralston-Hooper, K., Sepúlveda, M.S., Review of recent proteomic applications in aquatic toxicology. Environ. Toxicol. Chem. 30 (2011), 274–282, 10.1002/etc.402.
Sanders, M.B., Billinghurst, Z., Depledge, M.H., Clare, A.S., Larval development and vitellin-like protein expression in Palaemon elegans larvae following Xeno-oestrogen exposure. Integr. Comp. Biol. 45 (2005), 51–60, 10.1093/icb/45.1.51.
Sankhon, N., Lockey, T., Rosell, R.C., Rothschild, M., Coons, L., Effect of methoprene and 20-hydroxyecdysone on vitellogenin production in cultured fat bodies and backless explants from unfed female Dermacentor variabilis. J. Insect Physiol. 45 (1999), 755–761, 10.1016/S0022-1910(99)00054-2.
Schimmel, S.C., Patrick, J.M., Faas, L.F., Oglesby, J.L., Wilson, A.J., Kepone: toxicity and bioaccumulation in blue crabs. Estuaries Coasts 2 (1979), 9–15, 10.1007/BF02823701.
Silva Gunawardene, Y.I.N., Tobe, S.S., Bendena, W.G., Chow, B.K.C., Yagi, K.J., Chan, S.M., Function and cellular localization of farnesoic acid O-methyltransferase (FAMeT) in the shrimp, Metapenaeus ensis. Eur. J. Biochem. 269 (2002), 3587–3595, 10.1046/j.1432-1033.2002.03048.x.
Silvestre, F., Tu, H.T., Bernard, A., Dorts, J., Dieu, M., Raes, M., Phuong, N.T., Kestemont, P., A differential proteomic approach to assess the effects of chemotherapeutics and production management strategy on giant tiger shrimp Penaeus monodon. Comp. Biochem. Physiol. Part D. Genom. Proteom. 5 (2010), 227–233, 10.1016/j.cbd.2010.06.003.
Snegaroff, J., Les résidus d′insecticides organochlorés dans les sols et les rivières de la région bananière de Guadeloupe. Phytiatr. Phytopharm. 26 (1977), 251–268.
Snyder, M.J., Identification of a new cytochrome P450 family, CYP45, from the lobster, Homarus americanus, and expression following hormone and xenobiotic exposures. Arch. Biochem. Biophys. 358 (1998), 271–276, 10.1006/abbi.1998.0878.
Snyder, M.J., Mulder, E.P., Environmental endocrine disruption in decapod crustacean larvae: hormone titers, cytochrome P450, and stress protein responses to heptachlor exposure. Aquat. Toxicol. 55 (2001), 177–190, 10.1016/s0166-445x(01)00173-4.
Sumpter, J.P., Jobling, S., Vitellogenesis as a biomarker for estrogenic contamination of the aquatic environment. Environ. Health Perspect. 103 (1995), 173–178, 10.1289/ehp.95103s7173.
Tatarazako, N., Oda, S., Watanabe, H., Morita, M., Iguchi, T., Juvenile hormone agonists affect the occurrence of male Daphnia. Chemosphere 53 (2003), 827–833, 10.1016/s0045-6535(03)00761-6.
Thomson, S.A., Baldwin, W.S., Wang, Y.H., Kwon, G., LeBlanc, G.A., Annotation, phylogenetics, and expression of the nuclear receptors in Daphnia pulex. BMC Genom., 10, 2009, 500, 10.1186/1471-2164-10-500.
Thornton, J., Need, E., Crews, D., Resurrecting the ancestral steroid receptor: ancient origin of estrogen signaling. Science 301 (2003), 1714–1717, 10.1126/science.1086185.
Toyota, K., Miyakawa, H., Hiruta, C., Furuta, K., Ogino, Y., Shinoda, T., Tatarazako, N., Miyagawa, S., Shaw, J.R., Iguchi, T., Methyl farnesoate synthesis is necessary for the environmental sex determination in the water flea Daphnia pulex. J. Insect Physiol. 80 (2015), 22–30, 10.1016/j.jinsphys.2015.02.002.
Trapp, J., Armengaud, J., Pible, O., Gaillard, J.-C., Abbaci, K., Habtoul, Y., Chaumot, A., Geffard, O., Proteomic investigation of male Gammarus fossarum, a freshwater Crustacean, in response to endocrine disruptors. J. Proteome Res. 14 (2014), 292–303, 10.1021/pr500984z.
Tseng, D.-Y., Chen, Y.-N., Kou, G.-H., Lo, C.-F., Kuo, C.-M., Hepatopancreas is the extraovarian site of vitellogenin synthesis in black tiger shrimp. Penaeus monodon. Comp. Biochem. Physiol. Part A Mol. & Integr. Physiol. 129 (2001), 909–917, 10.1016/s1095-6433(01)00355-5.
Williams, K.L., Genomes and proteomes: towards a multidimensional view of biology. Electrophoresis 20 (1999), 678–688, 10.1002/(SICI)1522-2683(19990101)20:4/5<678::AID-ELPS678>3.0.CO;2-R.
Wright, P.C., Noirel, J., Ow, S.Y., Fazeli, a., A review of current proteomics technologies with a survey on their widespread use in reproductive biology investigations. Theriogenology 77 (2012), 738–765, 10.1016/j.theriogenology.2011.11.012.
Yamamoto, H., Okino, T., Yoshimura, E., Tachibana, A., Shimizu, K., Fusetani, N., Methyl farnesoate induces larval metamorphosis of the barnacle, Balanus amphitrite via protein kinase C activation. J. Exp. Zool. 278 (1997), 349–355.
Yang, F., Qian, Y.Q., Ma, W.M., Li, Y., Yang, J.S., Yang, W.J., MSG is involved in sperm gelatinolytic activity in the prawn, Macrobrachium rosenbergii. Chin. Sci. Bull. 58 (2013), 2113–2118, 10.1007/s11434-012-5597-x.
Zhao, W., Chen, L., Zhang, F., Wu, P., Li, E., Qin, J., Molecular characterization of cathepsin L cDNA and its expression during oogenesis and embryogenesis in the oriental river prawn Macrobrachium nipponense (Palaemonidae). Genet. Mol. Res. 12 (2013), 5215–5225, 10.4238/2013.October.30.6.
Zhou, X., Ding, Y., Wang, Y., Proteomics: present and future in fish, shellfish and seafood. Rev. Aquac. 4 (2012), 11–20, 10.1111/j.1753-5131.2012.01058.x.
Zou, E., Bonvillain, R., Chitinase activity in the epidermis of the fiddler crab, Uca pugilator, as an in vivo screen for molt-interfering xenobiotics. Comp. Biochem. Physiol. - C. Toxicol. Pharmacol. 139 (2004), 225–230, 10.1016/j.cca.2004.11.003.
