Abstract
This study aimed to establish the combined effect of aflatoxin B1 (AFB1) and fumonisin B1 (FB1) on wild Litopenaeus vannamei hepatopancreas alkaline phosphatase (AP) activity compared with that of farmed shrimp. AP activity in hepatopancreas extract was confirmed by several specific inhibitor assays. AP activity of wild shrimp was higher than that of farmed shrimp (p < 0.05). However, AP activity from both wild and farmed shrimp was inhibited when incubated with AFB1 and FB1. The greatest inhibition occurred when AP was incubated with a mixture of AFB1 and FB1. The IC50 for AFB1 on AP activity of wild and farmed shrimp hepatopancreases was 0.790 and 0.398 μg/mL, respectively. The IC50 of FB1 was 0.87 μg/mL for wild shrimp and 0.69 μg/mL for farmed shrimp. These results suggest that, at the mycotoxins concentrations used in the study, AP from farmed L. vannamei was sensitive to the presence of both mycotoxins; however, AP is more sensitive to the combination of AFB1 + FB1 suggesting a possible synergistic or potentiating inhibitory effect.
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References
Amos K (1985) Procedures for the detection and identification of fish health section of certain fish pathogens. American Fisheries Society, Oregon
Ásgeirsson B, Hartemink R, Chlebowski JF (1995) Alkaline phosphatase from Atlantic cod (Gadus morhua). Kinetic and structural properties which indicate adaptation to low temperatures. Comp Biochem Physiol B 110:315–329. doi:10.1016/0305-0491(94)00171-P
Bautista MN, Lavilla-Pitogo CR, Subosa PF, Begino ET (2006) Aflatoxin B1 contamination of shrimp feeds and its effect on growth and hepatopancreas of pre-adult Penaeus monodon. J Sci Food Agric 65:5–11. doi:10.1002/jsfa.2740650103
Bennett JM, Klich M (2003) Mycotoxins. Clin Microbiol Rev 16:497–516. doi:10.1128/CMR.16.3.497-516.2003
Bintvihok A, Ponpornpisit A, Tangtrongpiros J, Panichkriangkrai W, Rattanapanee R, Doi K, Kumagai S (2003) Aflatoxin contamination in shrimp feed and effects of aflatoxin addition to feed on shrimp production. J Food Prot 66:882–885
Boonyaratpalin M, Supamattaya K, Verakunpiriya V, Supraser D (2001) Effect of aflatoxin B1 on growth performance, blood components, immune function and histopathological changes in black tiger shrimps (Penaeus monodon). Aquac Res 32:388–398. doi:10.1046/j.1355-557x.2001.00046.x
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. doi:10.1016/0003-2697(76)90527-3
Burgos-Hernández A, Farias SI, Torres-Arreola W, Ezquerra-Brauer JM (2005) In vitro studies of the effects of aflatoxin B1 and fumonisin B1 on trypsin-like and collagenase-like activity from the hepatopancreas of white shrimp (Litopenaeus vannamei). Aquaculture 250:399–410. doi:10.1016/j.aquaculture.2005.05.024
Carlson DB, Williams DE, Spitsbergen JM, Ross PF, Bacon CW, Meredith FI, Riley RT (2001) Fumonisin B1 promotes aflatoxin B1 and N-methyl-N′-nitro-nitrosoguanidine-initiated liver tumors in rainbow trout. Toxicol Appl Pharmacol 172:29–36
Ceccaldi HJ (1997) Anatomy and physiology of the digestive system. In: D’Abramo LR, Conklin DE, Akiyama DM (eds) Crustacean nutrition: advances in world aquaculture. World Aquaculture Society, Baton Rouge, pp 261–291
Chuang NN, Shih SL (1990) Purification and some properties of alkaline phosphatase from the hepatopancreas of the shrimp Penaeus japonicus (Crustacea: Decapoda). J Exp Zool A 256:1–7. doi:10.1002/jez.1402560102
Córdova-Murueta JH, García-Carreño FL, Navarrete del Toro MA (2004) Effects of stressors on shrimp digestive enzymes from assays of feces: an alternate method of evaluation. Aquaculture 233:439–449. doi:10.1016/j.aquaculture
Cuccioloni M, Mozzicafreddo M, Barocci S, Ciuti F, Re L, Eleuteri AM, Angeletti M (2009) Aflatoxin B1 misregulates the activity of serine proteases: possible implications in the toxicity of some mycotoxins. Toxicol in Vitro 23:393–399. doi:10.1016/j.tiv.2009.01.002
Filippov AA, Golovanova IL, Aminov AI (2013) Effect of organic pollutants on fish digestive enzymes: a review. Aquat Toxicol 6:155–160. doi:10.1134/S199508291302003X
Fukuda H, Shima H, Vesonder RF, Tokuda H, Nishino H, Katoh S, Tamura S, Takashi S, Nagao M (1996) Inhibition of protein serine/threonine phosphatases by fumonisin B1, a mycotoxin. Biochem Biophys Res Commun 220:160–165
García-Morales MH, Pérez-Velázquez M, González-Féliz ML, Burgos-Hernández A, Cortez-Rocha MO, Bringas-Alvarado L, Ezquerra-Brauer JM (2015) Effects of fumonisin B1-containing feed on the muscle proteins and ice-storage life of white shrimp (Litopenaeus vannamei). J Aquat Food Prod Technol 24:340–353. doi:10.1080/10498850.2013.775621
Han D, Xie S, Zhu X, Yang Y, Guo Z (2009) Growth and hepatopancreas performance of gibel carp diets containing low levels of afaltoxin B1. Aquac Nutr 16:335–342. doi:10.1111/j.1365-2095.2009.00669.x
Harvey RB, Edrington TS, Kubena LF, Elissalde MH, Rottinghaus GE (1995) Influence of aflatoxin and fumonisin B1-containing culture material on growing barrows. Am J Vet Res 56:1668–1672
Hose JE, Lightner DV, Redman RM, Danald DA (1984) Observations on the pathogenesis of the imperfect fungus, Fusarium solani, in the California brown shrimp, Penaeus californiensis. J Invertebr Pathol 44:292–303. doi:10.1016/0022-2011(84)90027-2
Jobling M (1998) A review of the physiological and nutritional energetics of cod, Gadus morhua L., with particular reference to growth under farmed conditions. Aquaculture 70:1–19. doi:10.1016/0044-8486(88)90002-6
Kautsky N, Rönnbäck P, Tedengren M, Troell M (2000) Ecosystem perspectives on management of disease in shrimp pond farming. Aquaculture 191:145–161. doi:10.1016/S0044-8486(00)00424-5
Kitani H (1994) Identification of wild postlarvae of penaids shrimp, genus Penaeus, in the Pacific coast of Central America. Fish Sci 60:243–247. doi:10.2331/fishsci.60.243
Kubena LF, Edrington TS, Kamps-Holtzapple C, Harvey RB, Elissalde MH, Rottinghaus E (1995) Effects of feeding fumonisin B1 present in Fusarium monoliforme culture material and aflatoxin singly and combination to turkey poults. Poult Sci 74:1295–1303. doi:10.3382/ps.0741295
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685. doi:10.1038/227680a0
Lee AC, Chuang NN (1991) Characterization of different molecular forms of alkaline phosphatase in the hepatopancreas from the shrimp Penaues monodon (Crustacea: Decapoda). Comp Biochem Physiol B 99B:845–850. doi:10.1016/0305-0491(91)90152-4
Lee NA, Wang S, Allan RD, Kennedy IR (2004) A rapid aflatoxin B1 ELISA: development and validation with reduced matrix effect for peanuts, corn, pistachio, and soybeans. J Agric Food Chem 52:2746–2755. doi:10.1021/jf0354038
Lightner DV, Redman RM, Price RL, Wiseman MO (1982) Histopathology of aflatoxicosis in the marine shrimp Penaeus stylirostris and P. vannamei. J Invertebr Pathol 40:279–291. doi:10.1016/0022-2011(82)90127-6
Lu Z, Che W, Liu R, Hu X, Ding Y (2010) A novel method for high-level production of psychrophilic TAB5 alkaline phosphatase. Protein Expr Purif 74:217–222. doi:10.1016/j.pep.2010.06.010
Mata AT, Ferreira JP, Oliveira BR, Batoréu MC, Crespo MT, Pereira VJ, Bronze MR (2015) Bottled water: analysis mycotoxins by LC-MS/MS. Food Chem 176:455–464. doi:10.1016/j.foodchem.2014.12.088
Mexia-Salazar AL, Burgos-Hernández A, Cortez-Rocha M, Hernandez-López J, Castro-Longoria R, Ezquerra-Brauer JM (2008) Role of fumonisin B1 addition on the immune system, histopathology, and muscle proteins white shrimp (Litopenaeus vannamei). Food Chem 110:471–479. doi:10.1016/j.foodchem.2008.02.028
Nielsen I, Øverbø K, Olsen R (2001) Thermolabile alkaline phosphatase from Northern shrimp (Pandalus borealis): protein and cDNA sequence analyse. Comp Biochem Physiol 129B:853–861. doi:10.1016/S1096-4959(01)00391-8
Nomoto M, Ohsawa M, Wang H, Chen C, Yen K (1988) Purification and characterization of extracellular alkaline phosphatase from an alkalophilic bacterium. Agric Biol Chem 52:1643–1647. doi:10.1271/bbb1961.52.1643
Olsen RL, Øvervø K, Myrnes B (1991) Alkaline phosphatase from the hepatopancreas of shrimp (Pandalus borealis): a dimeric enzyme with catalytically active subunits. Comp Biochem Physiol 99B:755–761. doi:10.1016/0305-0491(91)90139-5
Ostrowski-Meissner HT, LeaMaster BR, Duerr E, Walsh WA (1995) Sensitivity of the Pacific white shrimp, Penaeus vannamei, to aflatoxin B1. Aquaculture 131:155–164. doi:10.1016/0044-8486(95)98125-U
Pascual C, Gaxiola G, Rosas C (2003) Blood metabolites and hemocyanin of the white shrimp, Litopenaeus vannamei: the effect of culture conditions and comparison with other crustacean species. Mar Biol 142:735–745. doi:10.1007/s00227-002-0995-2
Rader BA, Kremer N, Apicella MA, Goldman EW, McFall-Ngaia MJ (2012) Modulation of symbiont lipid a signaling by host alkaline phosphatases in the squid-vibrio symbiosis. MBio 3:96–112. doi:10.1128/mBio.00093-12
Riley RT (1998) Mechanistic interactions of mycotoxins: theoretical consideration. In: Sinha KK, Bhatanagar D (eds) Mycotoxins in agriculture and food safety. Marcel Dekker Inc, Basel, pp 227–254
Sadhu AK, Chowdhury DK, Mukhopadhyay PK (1985) Relationship between serum enzymes, histological features and enzymes in hepatopancreas after sublethal exposure to malathion and phosphamidon in the murrel Channa striatus (BL.). Int J Environ Stud 24:35–41. doi:10.1080/00207238508710174
SAGARPA (2015). Secretaria de Agricultura y Ganadería, Desarrollo Rural, Pesca y Alimentación. Comisión Nacional de Acuacultura y Pesca. http://www.conapesca.sagarpa.gob.mx/wb/cona/12de marzo mexico df. Accessed 30 November 2015
Šegviċ Klariċ M (2012) Adverse effects of combined mycotoxins. Arh Hig Rada Toksikol 63:519–530. doi:10.2478/10004-1254-63-2012-2299
Serrano AB, Font G, Mañes J, Ferrer E (2015) Dispersive liquid-liquid microextraction for the determination of emerging Fusarium mycotoxins in water. Food Anal Methods 9:856–863. doi:10.1007/s12161-015-0257-9
Speijers GJA, Speijers MHM (2004) Combined toxic effect of mycotoxins. Toxicol Lett 153:91–98. doi:10.1016/j.toxlet.2004.04.046
Supamattaya K, Sukrakanchana N, Boonyaratpalin M, Schatzmayr D, Chittiwan V (2005) Effects of ochratoxin A and deoxynivalenol on growth performance and immuno-physiological parameters in black tiger shrimp (Penaeus monodon). Songklanakarin J Sci Technol 27:91–99
Tepšič K, Gunde-Cimerman N, Frisvand JC (1997) Growth and mycotoxin production by Aspergillus fumigatus strain isolated from a saltern. FEMS Microbiol Lett 157:9–12. doi:10.1016/S0378-1097(97)0044-8
Tomková I, Ševčíková Z, Levkut M, Revajová V, Čonková E, Laciaková A, Lenhardt L’ (2001) Effect of aflatoxin B1 on CD3T cells an alkaline phosphatase in the intestine of mice. Mycopathologia 154:15–19
Torres O, Matute J, Gelineau-van Waes J, Maddox JR, Gregory SG, Ashley-Koch AE, Showker JL, Voss KA, Riley RT (2015) Human health implications from co-exposure to aflatoxins and fumonisins in maize-based food in Latin America: Guatemala as a case study. World Mycotoxin J 8:143–159. doi:10.3920/WMJ2014.1736
Trevan JW (1927) The error of determination of toxicity. Proc R Soc Lond B Biol Sci 101:483–514. doi:10.1098/rspb.1927.0030
Van Belle H (1976) Alkaline phosphatase. I. Kinetics and inhibition by levamisole of purified isoenzymes from humans. Clin Chem 22:972–976
Wang S, Quan Y, Lee N, Keenedy IR (2006) Rapid determination of fumonisin B1 in food samples by enzyme immunosorbent assay and colloidal gold immunoassay. J Agric Food Chem 54:2491–2495. doi:10.1021/jf0530401
Weibking TS, Ledoux DR, Brown TP, Rottinghaus GE (1993) Fumonisin toxicity in turkey poults. J Vet Diagn Investig 5:75–83. doi:10.1177/104063879300500116
Whitaker JR (1994) Principles of enzymology for the food sciences. Marcel Dekker, New York
Wiseman M, Price RL, Lightner DV, Williams WR (1982) Toxicity of aflatoxin B1 to penaeid shrimp. Appl Environ Microbiol 44:1479–1481
Zeng SL, Long WQ, Tian LX, Xie SW, Chen YJ, Yang HJ, Liu YJ (2015) Effects of dietary aflatoxin B1 on growth performance, body composition, haematological parameters and histopathology of juvenile Pacific white shrimp (Litopenaeus vannemei). Aquac Nutr. doi:10.1111/anu.12331
Ziaei-Nejad S, Habibi M, Azari G, Lovett D, Mirvaghefi A, Shakouri M (2006) The effect of Bacillus spp. bacteria used as probiotics on digestive enzyme activity, survival and growth in the Indian white shrimp Fenneropenaeus indicus. Aquaculture 252:516–524. doi:10.1016/j.aquaculture.2005.07.021
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This study was supported by a CONACYT 154046 grant given to author Josafat Marina Ezquerra-Brauer. The author expresses gratitude to CONACYT for the scholarship given to Jesús Alberto Pérez-Acosta.
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Pérez-Acosta, J.A., Burgos-Hernandez, A., Velázquez-Contreras, C.A. et al. An in vitro study of alkaline phosphatase sensitivity to mixture of aflatoxin B1 and fumonisin B1 in the hepatopancreas of coastal lagoon wild and farmed shrimp Litopenaeus vannamei . Mycotoxin Res 32, 117–125 (2016). https://doi.org/10.1007/s12550-016-0246-x
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DOI: https://doi.org/10.1007/s12550-016-0246-x