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Effect of pure microcystin-LR on activity and transcript level of immune-related enzymes in the white shrimp (Litopenaeus vannamei)

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Abstract

Microcystins (MCs) in freshwater and marine waters released by toxin-producing cyanobacteria have negative impacts to the aquatic environment. This study aimed to investigate the effect of pure microcystin-LR on activity and transcript level of immune-related enzymes in the white shrimp Litopenaeus vannamei. After exposed to varying concentrations of pure microcystin-LR (MC-LR) for 30 days, the activity of superoxide dismutase (SOD), lysozyme (LZM), glutathione peroxidase (GPx), peroxidase (POD), acid phosphatase (ACP), alkaline phosphatase (AKP) and transcript level of cMn-sod, lzm, gpx were investigated in the hepatopancreas of white shrimp (L. vannamei). Immune-related enzyme activities responded differently to MC-LR exposure. SOD, GPx, and POD activity in the hepatopancreas were activated in a concentration-dependent manner while LZM activity was significantly inhibited in the treatment groups. ACP and AKP activity showed an increase, followed by a decrease. The transcript levels of cMn-sod, lzm, and gpx were consistent with changes in their encoding enzyme activity. These results demonstrated that sub-chronical exposure to MC-LR induced the alteration of immune-related enzymes and corresponding genes in the hepatopancreas, which may help explain the presence of detoxification mechanisms in crustaceans and how they were protected from MC-LR stress for a long period of time.

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References

  • Amado LL, Monserrat JM (2010) Oxidative stress generation by microcystins in aquatic animals: why and how. Environ Int 36:226–235

    Article  CAS  Google Scholar 

  • Alverca E, Andrade M, Dias E, Bento FS, Batoréu MC, Jordan P, Silva MJ, Pereira P (2009) Morphological and ultrastructural effects of microcystin-LR from Microcystis aeruginosa, extract on a kidney cell line. Toxicon 54:283–294

    Article  CAS  Google Scholar 

  • Atencio L, Moreno I, Jos A, Pichardo S, Moyano R, Blanco A, Cameán AM (2008) Dose-dependent antioxidant responses and pathological changes in tenca (Tinca tinca) after acute oral exposure to microcystis, under laboratory conditions. Toxicon 52:1–12

    Article  CAS  Google Scholar 

  • Best JH, Eddy FB, Codd GA (2001) Effects of purified microcystin-LR and cell extracts of Microcystis strains PCC 7813 and CYA 43 on cardiac function in brown trout (Salmo trutta) alevins. Fish Physiol Biochem 24:171–178

    Article  CAS  Google Scholar 

  • Bieczynski F, De Anna JS, Pirez M, Brena BM, Villanueva SS, Luquet CM (2014) Cellular transport of microcystin-LR in rainbow trout (Oncorhynchus mykiss) across the intestinal wall: possible involvement of multidrug resistance-associated proteins. Aquat Toxicol 154:97–106

    Article  CAS  Google Scholar 

  • Botha N, Gehringer MM, Downing TG, van de Venter M, Shephard EG (2004) The role of microcystin-LR in the induction of apoptosis and oxidative stress in CaCo2 cells. Toxicon 43:85–92

    Article  CAS  Google Scholar 

  • Bouaicha N, Maatouk I (2004) Microcystin-LR and nodularin induce intracellularglutathione alteration, reactive oxygen species production and lipid peroxidationin primary cultured rat hepatocytes. Toxicol Lett 148:53–63

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  Google Scholar 

  • Cao P, Huang XH, Li CL, Jin YL, Liu JF (2011) Effects of Oscillatoria sp. on growth and immune activities of Litopenaeus vannamei (in Chinese). Fishery Modernization 38:25–30

    Google Scholar 

  • Carmichael WW (1997) The cyanotoxins. Advances in Botanical. Research 27:211–256

    CAS  Google Scholar 

  • Cazenave J, de los Angeles Bistoni M, Pesce SF, Wunderlin DA (2006) Differential detoxification and antioxidant response in diverse organs of Corydoras paleatus experimentally exposed to microcystin-RR. Aquat Toxicol 76:1–12

    Article  CAS  Google Scholar 

  • Chen J, Xie P (2005) Seasonal dynamics of the hepatotoxic microcystins in various organs of four freshwater bivalves from the large eutrophic lake Taihu of subtropical China and the risk to human consumption. Environ Toxicol 20:572–584

    Article  CAS  Google Scholar 

  • Chen T, Zhao X, Liu Y, Shi Q, Hua Z, Shen P (2004) Analysis of immunomodulating nitric oxide, inos and cytokines mrna in mouse macrophages induced by microcystin-LR. Toxicology 197:67–77

    Article  CAS  Google Scholar 

  • Di Giulio RT (1991) Indices of oxidative stress as biomarkers for environmental contamination. In Aquatic Toxicology and Risk Assessment: Fourteenth Volume. ASTM International.

  • Ding WX, Shen HM, Zhu HG, Ong CN (1998) Studies on oxidative damage induced by cyanobacteria extract in primary cultured rat hepatocytes. Environ Res 78:12–18

    Article  CAS  Google Scholar 

  • Ferrão-Filho ADS, Kozlowsky-Suzuki B (2011) Cyanotoxins: bioaccumulation and effects on aquatic animals. Mar Drugs 9:2729–2772

    Article  Google Scholar 

  • Ferreira MFN, Oliveira VM, Oliveira R, da Cunha PV, Grisolia CK, Júnior ORP (2010) Histopathological effects of [D-Leu 1] Microcystin-LR variants on liver, skeletal muscle and intestinal tract of Hypophthalmichthys molitrix (Valenciennes, 1844). Toxicon 55:1255–1262

    Article  CAS  Google Scholar 

  • Fischer WJ, Dietrich DR (2000) Pathological and biochemical characterization of microcystin-induced hepatopancreas and kidney damage in carp (Cyprinus carpio). Toxicol Appl Pharmacol 164:73–81

    Article  CAS  Google Scholar 

  • Fischer WJ, Altheimer S, Cattori V, Meier PJ, Dietrich DR, Hagenbuch B (2005) Organic anion transporting polypeptides expressed in liver and brain mediate uptake of microcystin. Toxicol Appl Pharmacol 203:257–263

    Article  CAS  Google Scholar 

  • Franco AA, Odom RS, Rando TA (1999) Regulation of antioxidant enzyme gene expression in response to oxidative stress and during differentiation of mouse skeletal muscle. Free Radical Bio Med 27:1122–1132

    Article  CAS  Google Scholar 

  • Galanti LN, Amé MV, Wunderlin DA (2013) Accumulation and detoxification dynamic of cyanotoxins in the freshwater shrimp Palaemonetes argentinus. Harmful Algae 27:88–97

    Article  CAS  Google Scholar 

  • Gonçalves-Soares D, Zanette J, Yunes JS, Yepiz-Plascencia GM, Bainy AC (2012) Expression and activity of glutathione S-transferases and catalase in the shrimp Litopenaeus vannamei inoculated with a toxic Microcystis aeruginosa strain. Mar Environ Res 75:54–61

    Article  Google Scholar 

  • Guicciardi ME, Leist M, Gores GJ (2004) Lysosomes in cell death. Oncogene 23:2881–2890

    Article  CAS  Google Scholar 

  • Halliwell B, Gutteridge JMJ (ed) (2015) Free radicals in biology and medicine. Oxford University Press, New York, NY, pp 3–45

  • Han ZG, Wu BG, Zheng JS, Xie LC (2001) Advances research on cyanobacterial toxins in freshwater bodies(A review). J Jinan Univ 22:129–135

    CAS  Google Scholar 

  • Hauser-Davis RA, Lavradas RT, Lavandier RC, Rojas EGA, Guarino AWS, Ziolli RL (2015) Accumulation and toxic effects of microcystin in tilapia (Oreochromis niloticus) from an eutrophic Brazilian lagoon. Ecotoxicol Environ Saf 112:132–136

    Article  CAS  Google Scholar 

  • Hou J, Li L, Xue T, Long M, Su Y, Wu N (2015) Hepatic positive and negative antioxidant responses in zebrafish after intraperitoneal administration of toxic microcystin-LR. Chemosphere 120:729–736

    Article  CAS  Google Scholar 

  • Jiang J, Gu X, Song R, Zhang Q, Geng J, Wang X, Yang L (2011) Time-dependent oxidative stress and histopathological changes in Cyprinus carpio L. exposed to microcystin-LR. Ecotoxicology 20:1000–1009

    Article  CAS  Google Scholar 

  • Jos Á, Pichardo S, Prieto AI, Repetto G, Vázquez CM, Moreno I, Cameán AM (2005) Toxic cyanobacterial cells containing microcystins induce oxidative stress in exposed tilapia fish (Oreochromis sp.) under laboratory conditions. Aquat Toxicol 72:261–271

    Article  CAS  Google Scholar 

  • Lankoff A, Kolataj A (2001) Influence of microcystin-YR and nodularin on the activity of some proteolytic enzymes in mouse liver. Toxicon 39:419–423

    Article  CAS  Google Scholar 

  • Lankoff A, Banasik A, Obe G, Deperas M, Kuzminski K, Tarczynska M, Jurczak T, Wojcik A (2003) Effect of microcystin-lr and cyanobacterial extract from polish reservoir of drinking water on cell cycle progression, mitotic spindle, and apoptosis in cho-k1 cells. Toxicol Appl Pharmacol 189:204–213

    Article  CAS  Google Scholar 

  • Lankoff A, Krzowski L, Glab J, Banasik A, Lisowska H, Kuszewski T, Góźdź S, Wójcik A (2004) DNA damage and repair in human peripheral blood lymphocytes following treatment with microcystin-LR. Mutat Res Fund Mol M 559:131–142

    Article  CAS  Google Scholar 

  • Leist M, Jäättelä M (2001) Triggering of apoptosis by cathepsins. Cell Death Differ 8:324–326

    Article  CAS  Google Scholar 

  • Lenartova V, Holovska K, Rafael Pedrajas J, Martinez Lara E, Peinado J, Lopez Barea J, Kosuth P (1997) Antioxidant and detoxifying fish enzymes as biomarkers of river pollution. Biomarkers 2:247–252

    Article  CAS  Google Scholar 

  • Li L, Xie P, Guo L, Ke Z, Zhou Q, Liu Y, Qiu T (2008) Field and laboratory studies on pathological and biochemical characterization of microcystin-induced liver and kidney damage in the phytoplanktivorous bighead carp. Sci World J 8:121–137

    Article  CAS  Google Scholar 

  • Li X, Liu Y, Song L, Liu J (2003) Responses of antioxidant systems in the hepatocytes of common carp (Cyprinus carpio L.) to the toxicity of microcystin-LR. Toxicon 42:85–89

    Article  CAS  Google Scholar 

  • Li X, Liu L, Zhang Y, Fang Q, Li Y, Li Y (2013) Toxic effects of chlorpyrifos on lysozyme activities, the contents of complement C3 and lgM, and lgM and complement C3 expressions in common carp (Cyprinus carpio, L.). Chemosphere 93:428–433

    Article  CAS  Google Scholar 

  • Li XY, Chung IK, Kim JI, Lee JA (2004) Subchronic oral toxicity of microcystin in common carp (Cyprinus carpio L.) exposed to Microcystis under laboratory conditions. Toxicon 44:821–827

    Article  CAS  Google Scholar 

  • Li XY, Chung IK, Kim JI, Lee JA (2005) Oral exposure to Microcystis increases activity-augmented antioxidant enzymes in the liver of loach (Misgurnus mizolepis) and has no effect on lipid peroxidation. Comp Biochem Physiol C Toxicol Pharmacol 141:292–296

    Article  Google Scholar 

  • Li XY (ed) (2007) Study on the toxicology of microcystins (in Chinese). Science Press, Beijing, pp 5–26

  • Li Z, Fu YM, Li X, Liu FS, Liu LP (2014) Expression profiles of three antimicrobial peptide genes in Litopenaeus vannamei induced by microcystin (MC-LR) (in Chinese). J Shanghai Ocean Univ 23:842–847

    Article  CAS  Google Scholar 

  • Livingstone DR (2001) Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms. Mar Pollut Bull 42:656–666

    Article  CAS  Google Scholar 

  • Magalhães VF, Marinho MM, Domingo P, Oliveira AC, Costa SM, Azevedo LO, Azevedo SMFO (2003) Microcystins (cyanobacteria hepatotoxins) bioaccumulation in fish and crustaceans from Sepetiba Bay (Brasil, RJ). Toxicon 42:289–295

    Article  Google Scholar 

  • Malbrouck C, Kestemont P (2006) Effects of microcystins on fish. Environ Toxicol Chem 25:72–86

    Article  CAS  Google Scholar 

  • Mazorra MT, Rubio JA, Blasco J (2002) Acid and alkaline phosphatase activities in the clam Scrobicularia plana: kinetic characteristics and effects of heavy metals. Comp Biochem Phys B Biochem Mol Biol 131:241–249

    Article  CAS  Google Scholar 

  • Möck A, Peters G (1990) Lysozyme activity in rainbow trout, Oncorhynchus mykiss (Walbaum), stressed by handling, transport and water pollution. J Fish Biol 37:873–885

    Article  Google Scholar 

  • Molina R, Moreno I, Pichardo S, Jos A, Moyano R, Monterde JG, Cameán A (2005) Acid and alkaline phosphatase activities and pathological changes induced in Tilapia fish (Oreochromis sp.) exposed subchronically to microcystins from toxic cyanobacterial blooms under laboratory conditions. Toxicon 46:725–735

    Article  CAS  Google Scholar 

  • Mukherjee S, Ray M, Ray S (2016) Shift in aggregation, ROSROS generation, antioxidative defense, lysozyme and acetylcholinesterase activities in the cells of an Indian freshwater sponge exposed to washing soda (sodium carbonate). Comp Biochem Phys C Toxicol Pharmacol 187:19–31

    Article  CAS  Google Scholar 

  • Murray CK, Fletcher TC (1976) The immunohistochemical localization of lysozyme in plaice (Pleuronectes platessa L.) tissues. J Fish Biol 9:329–334

    Article  CAS  Google Scholar 

  • Pandey S, Parvez S, Sayeed I, Haque R, Bin-Hafeez B, Raisuddin S (2003) Biomarkers of oxidative stress: a comparative study of river Yamuna fish Wallago attu (Bl. and Schn.). Sci Total Environ 309:105–115

    Article  CAS  Google Scholar 

  • Pavagadhi S, Gong Z, Hande MP, Dionysiou DD, Armah A, Balasubramanian R (2012) Biochemical response of diverse organs in adult Danio rerio (zebrafish) exposed to sub-lethal concentrations of microcystin-LR and microcystin-RR: a balneation study. Aquat Toxicol 109:1–10

    Article  CAS  Google Scholar 

  • Peng CC, Li ZJ, Cao YC, Liu XZ, Hu XJ (2011) Structure characteristics of planktonic microalgae community in Litopenaeus vannamei shoal water culture ponds in western Guangdong (in Chinese). Progress in Fishery. Sciences 32:117–125

    Google Scholar 

  • Sabatini SE, Brena BM, Luquet CM, San Julián M, Pirez M, Ríos de Molina MC (2011) Microcystin accumulation and antioxidant responses in the freshwater clam Diplodon chilensis patagonicus upon subchronic exposure to toxic Microcystis aeruginosa. Ecotoxicol Environ Saf 74:1188–1194

    Article  CAS  Google Scholar 

  • Sabatini SE, Brena BM, Pirez M, de Molina MDCR, Luquet CM (2015) Oxidative effects and toxin bioaccumulation after dietary microcystin intoxication in the hepatopancreas of the crab Neohelice (Chasmagnathus) granulata. Ecotoxicol Environ Saf 120:136–141

    Article  CAS  Google Scholar 

  • Saqrane S, Ghazali IE, Ouahid Y, Hassni ME, Hadrami IE, Bouarab L, del Campo FF, Oudra B, Vasconcelos V (2007) Phytotoxic effects of cyanobacteria extract on the aquatic plant Lemna gibba: microcystin accumulation, detoxication and oxidative stress induction. Aquat Toxicol 83:284–294

    Article  CAS  Google Scholar 

  • Sieroslawska A, Rymuszka A, Velisek J, Pawlik-Skowrońska B, Svobodova Z, Skowroński T (2012) Effects of microcystin-containing cyanobacterial extract on hematological and biochemical parameters of common carp (Cyprinus carpio L.). F Physiol Biochem 38:1159–1167

    Article  CAS  Google Scholar 

  • Söderhall K, Cerenius L (1998) Role of prophenoloxidase-activating system in invertebrate immunity. Curr Opin Immunol 10:23–28

    Article  Google Scholar 

  • Song LR, Chen W (2009) Production of microcystins in bloom-forming cyanobacteria and their environmental fates: a review. Journal of Lake Sciences 21:749–757

    Article  CAS  Google Scholar 

  • Vogt G (1994) Life-cycle and functional cytology of the hepatopancreas cells of Astacus astacus (Crustacea, Decapoda). Zoomorphology 114:83–101

    Article  Google Scholar 

  • Wang JP, Wu XF (2000) Status of study on the haemocyte and humoral immunity of shrimps (in Chinese). J Zhejiang Ocean Univ 19:354–360

    Google Scholar 

  • Wang WB, Wang JG, Li AH, Cai TZ (2004) Changes of cortisol and lysozyme levels in Carassius auratus blood after crowding stress and the fish sensitivity to pathogen (in Chinese). J Fishery Sci China 11:408–412

    CAS  Google Scholar 

  • Xie L, Xie P, Ozawa K, Honma T, Yokoyama A, Park HD (2004) Dynamics of microcystins-LR and-RR in the phytoplanktivorous silver carp in a sub-chronic toxicity experiment. Environ Pollut 127:431–439

    Article  CAS  Google Scholar 

  • Xie L, Xie P, Guo L, Li L, Miyabara Y, Park HD (2005) Organ distribution and bioaccumulation of microcystins in freshwater fish at different trophic levels from the eutrophic Lake Chaohu, China. Environ Toxicol 20:293–300

    Article  CAS  Google Scholar 

  • Xiong Q, Xie P, Li H, Hao L, Li G, Qiu T, Liu Y (2010) Acute effects of microcystins exposure on the transcription of antioxidant enzyme genes in three organs (liver, kidney, and testis) of male Wistar rats. J Biochem Mol Toxicol 24:361–367

    Article  CAS  Google Scholar 

  • Xu YP, Wang TT, Sun YX, Liu WJ, You JS, Jin LJ (2011) Current research on function and application of aquatic animal lysozyme (in Chinese). Fisheries Sci 30:307–310

    CAS  Google Scholar 

  • Yuan J, Gu Z, Zheng Y, Zhang Y, Gao J, Chen S, Wang ZZ (2016) Accumulation and detoxification dynamics of microcystin-LR and antioxidant responses in male red swamp crayfish Procambarus clarkii. Aquat Toxicol 177:8–18

    Article  CAS  Google Scholar 

  • Zastepa A, Pick FR, Blais JM, Saleem A (2015) Analysis of intracellular and extracellular microcystin variants in sediments and pore waters by accelerated solvent extraction and high performance liquid chromatography-tandem mass spectrometry. Anal Chim Acta 872:26–34

    Article  CAS  Google Scholar 

  • Zegura B, Gajski G, Straser A, Garaj-Vrhovac V, Filipic M (2011) Microcystin-LR induced DNA damage in human peripheral blood lymphocytes. Mutat Res 726:116–122

    Article  CAS  Google Scholar 

  • Zha GC, Zhou CQ, Niu XG (2007) Harm of Microcystis aeruginosa to Litopenaeus vannamei low salinity stocking (in Chinese). Acta Scientiarum Naturalium Universitatis Sunyatseni 46:64–67

    Google Scholar 

  • Zhang D, Xie P, Chen J, Dai M, Qiu T, Liu Y, Liang G (2009a) Determination of microcystin-LR and its metabolites in snail (Bellamya aeruginosa), shrimp (Macrobrachium nipponensis) and silver carp (Hypophthalmichthys molitrix) from Lake Taihu, China. Chemosphere 76:974–981

    Article  CAS  Google Scholar 

  • Zhang SL, Lu KH, Zheng ZM, Pan JH, Zhu JY (2009b) Accumulation and degradation of microcystins and their effects on activities of three kinds of enzymes in liver of Bellamya Aeruginosa (in Chinese). J Agro Environ Sci 28:54–59

    Google Scholar 

  • Zhou J, Wang WN, Wang AL, He WI, Zhou QT, Liu Y, Xu J (2009) Glutathione S-transferase in the white shrimp Litopenaeus vannamei: characterization and regulation under pH stress. Comp Biochem Phys C 150:224–230

    Google Scholar 

  • Zimba PV, Khoo L, Gaunt PS, Brittain S, Carmichael WW (2001) Confirmation of catfish, Ictalurus punctatus (Ralfinesque), mortality from Microcystis toxins. J Fish Dis 24:41–47

    Article  CAS  Google Scholar 

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Acknowledgements

This study was supported by Guangdong Special Marine fishery Science and Technology Promotion Project (A201308B10) and Guangdong Special Marine Fishery Science and Technology and Industrial Development Project (A201508B08). The authors thank Natalie Defraene for English editing, and an anonymous reviewer for critical comments.

Author contributions

X.H. and C.L. designed the experiment. Y.C. performed the experiment. Y.C. and J.W. prepared and revised the manuscript. X.H. and C.L. reviewed the initial and final version of the manuscript.

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Authors and Affiliations

  1. Department of Aquaculture, Fishery College, Guangdong Ocean University, East Huguangyan, Mazhang District, Zhanjiang, Guangdong, 524088, China

    Yanyan Chen, Xianghu Huang & Changling Li

  2. Engineering Technology Research Center for Algae Breeding and Application, Zhanjiang, Guangdong, 524088, China

    Yanyan Chen, Xianghu Huang & Changling Li

  3. Shenzhen Research Institute of Guangdong Ocean University, Shenzhen, 518108, China

    Yanyan Chen, Xianghu Huang & Changling Li

  4. Collaborative Innovation Center for Geo-hazards and Eco-environment in Three Gorges Area, Hubei Province, The Three Gorges University, Yichang, 443002, China

    Jianzhu Wang

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  1. Yanyan Chen
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Correspondence to Xianghu Huang.

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Chen, Y., Huang, X., Wang, J. et al. Effect of pure microcystin-LR on activity and transcript level of immune-related enzymes in the white shrimp (Litopenaeus vannamei). Ecotoxicology 26, 702–710 (2017). https://doi.org/10.1007/s10646-017-1802-7

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