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Toxins  2014 

Immunohistochemical Approach to Study Cylindrospermopsin Distribution in Tilapia (Oreochromis niloticus) under Different Exposure Conditions

DOI: 10.3390/toxins6010283

Keywords: Cylindrospermopsin, Aphanizomenon ovalisporum, Oreochromis niloticus, immunohistochemistry, distribution, cyanobacteria, cyanotoxin

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Abstract:

Cylindrospermopsin (CYN) is a cytotoxic cyanotoxin produced by several species of freshwater cyanobacteria ( i.e., Aphanizomenon ovalisporum). CYN is a tricyclic alkaloid combined with a guanidine moiety. It is well known that CYN inhibits both protein and glutathione synthesis, and also induces genotoxicity and the alteration of different oxidative stress biomarkers. Although the liver and kidney appear to be the main target organs for this toxin based on previous studies, CYN also affects other organs. In the present study, we studied the distribution of CYN in fish ( Oreochromis niloticus) under two different exposure scenarios using immunohistochemical (IHC) techniques. In the first method, fish were exposed acutely by intraperitoneal injection or by gavage to 200 μg pure CYN/Kg body weight (bw), and euthanized after 24 h or five days of exposure. In the second method, fish were exposed by immersion to lyophilized A. ovalisporum CYN-producing cells using two concentration levels (10 or 100 μg/L) for two different exposure times (7 or 14 days). The IHC was carried out in liver, kidney, intestine, and gills of fish. Results demonstrated a similar pattern of CYN distribution in both experimental methods. The organ that presented the most immunopositive results was the liver, followed by the kidney, intestine, and gills. Moreover, the immunolabeling signal intensified with increasing time in both assays, confirming the delayed toxicity of CYN, and also with the increment of the dose, as it is shown in the sub-chronic assay. Thus, IHC is shown to be a valuable technique to study CYN distribution in these organisms.

References

[1]  Moreira, C.; Azevedo, J.; Antunes, A.; Vasconcelos, V. Cylindrospermopsin: Occurrence, methods of detection and toxicology. J. Appl. Microbiol. 2012, 114, 605–620.
[2]  Shaw, G.; Sukenik, A.; Livne, A.; Chiswell, R.K.; Smith, M.J.; Seawright, A.A.; Norris, R.L.; Eaglesham, G.K.; Moore, M.R. Blooms of the cylindrospermopsin containing cyanobacterium, Aphanizomenon ovalisporum (Forti), in newly constructed lakes, Queensland, Australia. Environ. Toxicol. 1999, 14, 167–177, doi:10.1002/(SICI)1522-7278(199902)14:1<167::AID-TOX22>3.0.CO;2-O.
[3]  Ohtani, I.; Moore, R.E.; Runnegar, M. Cylindrospermopsin: A potent hepatotoxin from the blue-green alga Cylindrospermopsis raciborskii. Am. Chem. Soc. 1992, 114, 7941–7942, doi:10.1021/ja00046a067.
[4]  Sivonen, K.; Jones, G. Cyanobacterial Toxins. In Toxic Cyanobacteria in Water: A Guide to Their Public Health Consequences, Monitoring and Management; Chorus, I., Bartram, M.J., Eds.; E & FN Spon: London, UK, 1999; pp. 41–111.
[5]  Chiswell, R.K.; Shaw, G.R.; Eaglesham, G.; Smith, M.J.; Norris, R.L.; Seawright, A.A.; Moore, M.R. Stability of cylindrospermopsin, the toxin from the cyanobacterium, Cylindrospermopsis raciborskii: Effect of pH, temperature, and sunlight on decomposition. Environ. Toxicol. 1999, 14, 155–161, doi:10.1002/(SICI)1522-7278(199902)14:1<155::AID-TOX20>3.0.CO;2-Z.
[6]  Funari, E.; Testai, E. Human health risk assessment related to cyanotoxins exposure. Crit. Rev. Toxicol. 2008, 38, 97–125, doi:10.1080/10408440701749454.
[7]  Terao, K.; Ohmori, S.; Igarashi, K.; Ohtani, I.; Watanabe, M.F.; Harada, K.I.; Ito, E.; Watanabe, M. Electron microscopic studies on experimental poisoning in mice induced by cylindrospermopsin isolated from blue-green alga Umezakia natans. Toxicon 1994, 32, 833–843, doi:10.1016/0041-0101(94)90008-6.
[8]  Falconer, I.R.; Hardy, S.J.; Humpage, A.R.; Froscio, S.M.; Tozer, G.J.; Hawkins, P.R. Hepatic and renal toxicity of the blue-green alga (cyanobacterium) Cylindrospermopsis raciborskii in male Swiss albino mice. Environ. Toxicol. 1999, 14, 143–150.
[9]  Seawright, A.A.; Nolan, C.C.; Shaw, G.R.; Chiswell, R.K.; Norris, R.L.; Moore, M.R.; Smith, M.K. The oral toxicity for mice of the tropical cyanobacterium Cylindrospermopsis raciborskii (Woloszynska). Environ. Toxicol. 1999, 14, 135–142.
[10]  Runnegar, M.T.; Kong, S.M.; Zhong, Y.Z.; Lu, S.C. Inhibition of reduced glutathione synthesis by cyanobacterial alkaloid Cylindrospermopsin in cultured rat hepatocytes. Biochem. Pharmacol. 1995, 49, 219–225, doi:10.1016/S0006-2952(94)00466-8.
[11]  Humpage, A.R.; Fontaine, F.; Froscio, S.; Burcham, P.; Falconer, I.R. Cylindrospermopsin genotoxicity and cytotoxicity: Role of cytochrome P-450 and oxidative stress. J. Toxicol. Environ. Health A 2005, 68, 739–753, doi:10.1080/15287390590925465.
[12]  Puerto, M.; Jos, A.; Pichardo, S.; Gutiérrez-Praena, D.; Cameán, A.M. Acute effects of pure Cylindrospermopsin on the activity and transcription of antioxidant enzymes in tilapia (Oreochromis niloticus) exposed by gavage. Ecotoxicology 2011, 20, 1852–1860, doi:10.1007/s10646-011-0723-0.
[13]  Young, F.M.; Micklem, J.; Humpage, A.R. Effects of the blue-green algal toxin cylindrospermopsin (CYN) on human granulosa cells in vitro. Reprod. Toxicol. 2008, 25, 374–380, doi:10.1016/j.reprotox.2008.02.006.
[14]  Gutiérrez-Praena, D.; Jos., A.; Pichardo, S.; Moreno, I.M.; Cameán, A.M. Presence and bioaccumulation of Microcystin and Cylindrospermopsin in food and the effectiveness of some cooking techniques at decreasing their concentrations: A review. Food Chem. Toxicol. 2013, 53, 139–152, doi:10.1016/j.fct.2012.10.062.
[15]  White, S.H.; Duivenvoorden, L.J.; Fabbro, L.D.; Eaglesham, G.K. Influence of intracellular toxin concentrations on cylindrospermopsin bioaccumulation in a freshwater gastropod (Melanoides tuberculata). Toxicon 2006, 47, 497–509, doi:10.1016/j.toxicon.2005.12.011.
[16]  Berry, J.P.; Lind, O. First evidence of “paralytic shellfish toxins” and cylindrospermopsin in a Mexican freshwater system, Lago Catemaco, and apparent bioaccumulation of the toxins in “tegogolo” snails (Pomacea patula catemacensis). Toxicon 2010, 55, 930–938, doi:10.1016/j.toxicon.2009.07.035.
[17]  Anderson, L.; Fabbro, L.D.; Cowden, K. Assessment of Blue-Green Algal Toxins in Barramundi, Red Clay and Mussels from Awoonga Dam; Central Queensland University: Gladstone, Australia, 2003.
[18]  Saker, M.L.; Metcalf, J.S.; Codd, G.A.; Vasconcelos, V.M. Accumulation and depuration of the cyanobacterial toxin cylindrospermopsin in the freshwater mussel Anodonta cygnea. Toxicon 2004, 43, 185–194, doi:10.1016/j.toxicon.2003.11.022.
[19]  Saker, M.L.; Eaglesham, G.K. The accumulation of cylindrospermopsin from the cyanobacterium Cylindrospermopsis raciborskii in tissues of the Redclaw crayfish Cherax quadricarinatus. Toxicon 1999, 37, 1065–1077, doi:10.1016/S0041-0101(98)00240-2.
[20]  White, S.H.; Duivenvoorden, L.J.; Fabbro, L.D.; Eaglesham, G.K. Mortality and toxin bioaccumulation in Bufo marinus following exposure to Cylindrospermopsis raciborskii cell extracts and live cultures. Environ. Pollut. 2007, 147, 158–167, doi:10.1016/j.envpol.2006.08.010.
[21]  Messineo, V.; Melchiorre, S.; Di Corcia, A.; Gallo, P.; Bruno, M. Seasonal succession of Cylindrospermopsis raciborskii and Aphanizomenon Ovalisporum blooms with cylindrospermopsin occurrence in the volcanic Lake Albano, Central Italy. Environ. Toxicol. 2010, 25, 18–27.
[22]  Berry, J.P.; Jaja-Chimedza, A.; Dávalos-Lind, L.; Lind, O. Apparent bioaccumulation of cylindrospermopsin and paralytic shellfish toxins by finfish in Lake Catemaco (Veracruz, Mexico). Food Addit. Contam. 2012, 2, 314–321.
[23]  Kinnear, S. Cylindrospermopsin: A decade of progress on bioaccumulation research. Mar. Drugs 2010, 8, 542–564, doi:10.3390/md8030542.
[24]  Norris, R.L.G.; Eaglesham, G.K.; Pierens, G.; Shaw, G.R.; Smith, M.J.; Chiswell, R.K.; Seawright, A.A.; Moore, M.R. Deoxycylindrospermopsin, an analog of cylindrospermopsin from Cylindrospermopsis raciborskii. Environ. Toxicol. 1999, 14, 163–165, doi:10.1002/(SICI)1522-7278(199902)14:1<163::AID-TOX21>3.0.CO;2-V.
[25]  Seifert, M.; Mcgregor, G.; Eaglesham, G.; Wickramasinghe, W.; Shaw, G. First evidence for the production of cylindrospermopsin and deoxy-cylindrospermopsin by the freshwater benthic cyanobacterium, Lyngbya wollei (Farlow ex Gomont) Speziale and Dyck. Harmful Algae 2007, 6, 73–80.
[26]  Hawkins, P.R.; Runnegar, M.T.C.; Jackson, A.R.B.; Falconer, I.R. Severe hepatotoxicity caused by the tropical cyanobacterium (blue-green alga) Cylindrospermopsis raciborskii (Woloszynska) Seenaya and Subba Raju isolated form a domestic supply reservoir. Appl. Environ. Microbiol. 1985, 50, 1292–1295.
[27]  Berry, J.P.; Gibbs, P.D.L.; Schmale, M.C.; Saker, M.L. Toxicity of cylindrospermopsin, and other apparent metabolites from Cylindrospermopsis raciborskii and Aphanizomenon ovalisporum, to the zebrafish (Danio rerio) embryo. Toxicon 2009, 53, 289–299, doi:10.1016/j.toxicon.2008.11.016.
[28]  Puerto, M.; Jos, A.; Pichardo, S.; Moyano, R.; Blanco, A.; Cameán, A.M. Acute exposure to pure Cylindrospermopsin results in oxidative stress and pathological alterations in tilapia (Oreochromis niloticus). Environ. Toxicol. 2012, doi:10.1002/tox.21764.
[29]  Gutiérrez-Praena, D.; Jos, A.; Pichardo, S.; Cameán, A.M. Oxidative stress responses in tilapia (Oreochromis niloticus) exposed to a single dose of pure Cylindrospermopsin under laboratory conditions: Influence of exposure route and time of sacrifice. Aquat. Toxicol. 2011, 105, 100–106, doi:10.1016/j.aquatox.2011.05.015.
[30]  Gutiérrez-Praena, D.; Jos, A.; Pichardo, S.; Moyano, R.; Blanco, A.; Monterde, J.G.; Cameán, A.M. Time-dependent histopathological changes induced in tilapia (Oreochromis niloticus) after acute exposure to pure Cylindrospermopsin by oral and intraperitoneal route. Ecotoxicol. Environ. Saf. 2012, 76, 102–113, doi:10.1016/j.ecoenv.2011.10.008.
[31]  Gutiérrez-Praena, D.; Puerto, M.; Prieto, A.I.; Jos, A.; Pichardo, S.; Vasconcelos, V.; Cameán, A.M. Protective role of dietary N-Acetylcysteine on the oxidative stress induced by Cylindrospermopsin in tilapia (Oreochromis niloticus). Environ. Toxicol. Chem. 2012, 31, 1548–1555, doi:10.1002/etc.1838.
[32]  Yoshida, T.; Makita, Y.; Tsutsumi, T.; Nagata, S.; Tashiro, F.; Yoshida, F.; Sekijima, M.; Tamura, S.I.; Harada, T.; Maita, K.; et al. Immunohistochemical localization of Microcystin-LR in the liver of mice: A study on the pathogenesis of Microcystin-LR-induced hepatotoxicity. Toxicol. Pathol. 1998, 26, 411–418.
[33]  Guzmán, R.E.; Solter, P.F. Characterization of sublethal microcystin-LR exposure in mice. Vet. Pathol. 2002, 39, 17–26, doi:10.1354/vp.39-1-17.
[34]  Fischer, W.J.; Hitzfeld, B.C.; Tencalla, F.; Eriksson, J.E.; Mikhailov, A.; Dietrich, D.R. Microcystin-LR toxicodynamics, induced pathology, and immunohistochemical localization in livers of blue-green algae exposed Rainbow trout (Oncorhynchus mykiss). Toxicol. Sci. 2000, 54, 365–373, doi:10.1093/toxsci/54.2.365.
[35]  Lance, E.; Josso, C.; Dietrich, D.; Ernst, B.; Paty, C.; Senger, F.; Bormans, M.; Gérard, C. Histopathology and Microcystin distribution in Lymnaea stagnalis (Gastropoda) following toxic cyanobacterial or dissolved microcystin-LR exposure. Aquat. Toxicol. 2010, 98, 211–220, doi:10.1016/j.aquatox.2010.02.014.
[36]  Niedobitek, G.; Kremmer, E.; Herbst, H.; Whitehead, L.; Dawson, C.W.; Niedobitek, E.; von Ostau, C.; Rooney, N.; Gr?sser, F.A.; Young, L.S. Immunohistochemical detection of the Epstein-Barr Virus-encoded latent membrane protein 2A in Hodkin’s disease and infectious mononucleosis. Blood 1997, 90, 1664–1672.
[37]  Risalde, M.A.; Molina, V.; Sánchez-Cordón, P.J.; Pedrera, M.; Romero-Palomo, F.; Bautista, M.J.; Moreno, A.; Gómez-Villamandos, J.C. Comparison of pathologic changes and viral antigen distribution in tissues of calves with and without pre-existing bovine viral diarrhea virus infection following challenge with bovine Herpesvirus-1. Am. J. Vet. Res. 2013, 74, 598–610, doi:10.2460/ajvr.74.4.598.
[38]  Oosterwijk, E.; Ruiter, M.D.; Wakka, J.C.; Huiskens-van der Meij, J.W.; Jonas, U.; Fleuren, G.J.; Zwartendijk, J.; Hoedemaeker, P.; Warnaar, S.O. Immunohistochemical analysis of monoclonal antibodies to renal antigens. Application in the diagnosis of renal cell carcinoma. J. Am. Pathol. 1986, 123, 301–309.
[39]  Guzmán-Guillén, R.; Prieto, A.I.; Moreno, I.; Vasconcelos, V.M.; Moyano, R.; Blanco, A.; Cameán, A.M. Cyanobacterium producing Cylindrospermopsin cause histopathological changes at environmentally relevant concentrations in sub-chronically exposed tilapia (Oreochromis niloticus). Environ. Toxicol. 2013, doi:10.1002/tox.21904.
[40]  Ito, E.; Kondo, F.; Harada, K.H. First report of the distribution of orally administered Microcystin-LR in mouse tissue using an immunostaining method. Toxicon 2000, 38, 37–48, doi:10.1016/S0041-0101(99)00084-7.
[41]  Humpage, A.R.; Falconer, I.R. Oral toxicity of the cyanobacterial toxin cylindrospermopsin in male Swiss albino mice: Determination of no observed adverse effect level for deriving a drinking water guideline value. Environ. Toxicol. 2003, 18, 94–103, doi:10.1002/tox.10104.
[42]  Norris, R.L.G.; Seawright, A.A.; Shaw, G.R.; Smith, M.J.; Chiswell, R.K.; Moore, M.R. Distribution of 14C Cylindrospermopsin in vivo in the Mouse. Environ. Toxicol. 2001, 16, 498–505, doi:10.1002/tox.10008.
[43]  Guzmán-Guillén, R.; Prieto, A.I.; Moreno, I.M.; González, G.; Soria-Díaz, M.E.; Vasconcelos, V.; Cameán, A.M. Development and optimization of a method for the determination of Cylindrospermopsin from strains of Aphanizomenon cultures: Intra-laboratory assessment of its accuracy by using validation standards. Talanta 2012, 100, 356–363.
[44]  Hancock, D.C.; O’Reilly, N.J. Production of Polyclonal Antibodies in Rabbits. Methods Mol. Biol. 2005, 295, 27–40.
[45]  Elliot, C.T.; Redshaw, C.H.; George, S.E.; Campbell, K. First development and characterization of polyclonal and monoclonal antibodies to the emerging fresh water toxin Cylindrospermopsin. Harmful Algae 2013, 24, 10–19, doi:10.1016/j.hal.2012.12.005.
[46]  Straus, W. Cleavage of heme from horseradish peroxidase by methanol with inhibition of enzyme activity. J. Histochem. Cytochem. 1974, 22, 908–911, doi:10.1177/22.9.908.

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