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The effects of the neurotoxic agent emamectin benzoate on the expression of immune and stress-related genes and blood serum profiles in the Rainbow trout

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Abstract

Emamectin, a neurotoxic agent, is a semi-synthetic insecticide that belongs to the Avermectin family and is used against helmintic infections in the Salmonidae family. Its secondary effects are not clear; thus, the aim of this study was to investigate the only effects of emamectin benzoate on various biochemical parameters (AST, ALT, GGT, total protein, albumin and glucose) in serum and expressional changes of IL-1β, TNF-α, HSP70 and IL-8 in liver and spleen. For the purpose stated above, rainbow trout (n = 15) were administered 50 μg EB per kg fish daily for 7, 14 and 21 days. The results indicated that weight gains did not change (p  >  0.05), AST increased at day 21 (p < 0.05), while the changes of other biochemical parameters were not significant (p > 0.05). The changes in expression of IL-1β, TNF-α and HSP70 were significant (p < 0.05), while the changes of IL-8 expressions were not significant (p ˃ 0.05). In a conclusion, EB changed immun and stress-related gene expression in liver and spleen, and furthermore, AST changed in a dose- and time-dependent manner. The results imply that emamectin benzoate cause stress. This study is helpful to understand the effects of avermectin pharmaceutical family.

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References

  1. Davies IM, Rodger GK (2000) A review of the use of ivermectin as a treatment for sea lice [Lepeophtheirus salmonis (Kroyer) and Caligus elongatus Nordmann] infestation in farmed Atlantic salmon (Salmo salar L.). Aquac Res 31:869–883. https://doi.org/10.1046/j.1365-2109.2000.00510.x

    Article  Google Scholar 

  2. Yen T, Lin J (2004) Acute poisoning with emamectin benzoate. J Toxicol Clin Toxicol 42:657–661. https://doi.org/10.1081/CLT-200026968

    Article  CAS  PubMed  Google Scholar 

  3. Lopez-Castejon G, Brough D (2011) Understanding the mechanism of IL-1β secretion. Cytokine Growth Factor Rev 22:189–195. https://doi.org/10.1016/j.cytogfr.2011.10.001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Zou J, Secombes C (2016) The function of fish cytokines. Biology (Basel) 5:23. https://doi.org/10.3390/biology5020023

    Article  CAS  Google Scholar 

  5. Hong S, Li R, Xu Q et al (2013) Two types of TNF-α exist in teleost fish: phylogeny, expression, and bioactivity analysis of type-II TNF-α3 in rainbow trout oncorhynchus mykiss. J Immunol 191:5959–5972. https://doi.org/10.4049/jimmunol.1301584

    Article  CAS  PubMed  Google Scholar 

  6. Basu N, Todgham AE, Ackerman PA et al (2002) Heat shock protein genes and their functional significance in fish. Gene 295:173–183. https://doi.org/10.1016/S0378-1119(02)00687-X

    Article  CAS  PubMed  Google Scholar 

  7. Yamashita M, Yabu T, Ojima N (2010) Stress protein HSP70 in fish. Aqua-BioSci Monogr 3:111–141. https://doi.org/10.5047/absm.2010.00304.0111

    Article  Google Scholar 

  8. Kayhan FE (2010) A biological importance of heat shock proteins (Hsp) in aquatic organisms and thermotolerance. J Fish 4:246–253. https://doi.org/10.3153/jfscom.2010026

    Article  CAS  Google Scholar 

  9. Laing K, Secombes C (2004) Chemokines. Dev Comp Immunol 28:443–460. https://doi.org/10.1016/j.dci.2003.09.006

    Article  CAS  PubMed  Google Scholar 

  10. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262

    Article  CAS  PubMed  Google Scholar 

  11. Yarahmadi P, Miandare HK, Fayaz S, Caipang CMA (2016) Increased stocking density causes changes in expression of selected stress- and immune-related genes, humoral innate immune parameters and stress responses of rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol 48:43–53. https://doi.org/10.1016/j.fsi.2015.11.007

    Article  CAS  PubMed  Google Scholar 

  12. Douxfils J, Fierro-Castro C, Mandiki SNM et al (2017) Dietary β-glucans differentially modulate immune and stress-related gene expression in lymphoid organs from healthy and Aeromonas hydrophila -infected rainbow trout (Oncorhynchus mykiss ). Fish Shellfish Immunol 63:285–296. https://doi.org/10.1016/j.fsi.2017.02.027

    Article  CAS  PubMed  Google Scholar 

  13. Benedetto A, Brizio P, Squadrone S et al (2016) Oxidative stress related to chlorpyrifos exposure in rainbow trout: acute and medium term effects on genetic biomarkers. Pest Biochem Physiol 129:63–69. https://doi.org/10.1016/j.pestbp.2015.10.019

    Article  CAS  Google Scholar 

  14. El-Sayed YS, Saad TT, El-Bahr SM (2007) Acute intoxication of deltamethrin in monosex Nile tilapia, Oreochromis niloticus with special reference to the clinical, biochemical and haematological effects. Environ Toxicol Pharmacol 24:212–217. https://doi.org/10.1016/j.etap.2007.05.006

    Article  CAS  PubMed  Google Scholar 

  15. Sandnes K, Lie O, Waagbo R (1988) Normal ranges of some blood chemistry parameters in adult farmed Atlantic salmon, Salmo salar. J Fish Biol 32:129–136. https://doi.org/10.1111/j.1095-8649.1988.tb05341.x

    Article  CAS  Google Scholar 

  16. Kusatan Z (2004) Clarias lazera (valenciennes, 1840)’nın çeşitli dokularındaki kadmiyum birikiminin bazı biyokimyasal parametreler üzerine kantitatif etkileri. Mersin University

  17. Velisek J, Wlasow T, Gomulka P et al (2012) Effects of cypermethrin on rainbow trout (Oncorhynchus mykiss)&nbsp. Vet Med (Praha) 51:469–476. https://doi.org/10.17221/5580-VETMED

    Article  Google Scholar 

  18. Noyan T (2009) Serum gama glutamil transferaz: son elde edilen bulgular ve çeşitli hastalıkların fizyopatolojisindeki önemi. Van Med J 16:48–55

    Google Scholar 

  19. Velisek J, Svobodova Z, Piackova V (2009) Effects of acute exposure to bifenthrin on some haematological, biochemical and histopathological parameters of rainbow trout (Oncorhynchus mykiss). Vet Med (Praha) 54:131–137. https://doi.org/10.17221/15/2009-VETMED

    Article  CAS  Google Scholar 

  20. Parker LM, Laurén DJ, Hammock BD et al (1993) Biochemical and histochemical properties of hepatic tumors of Rainbow trout, Oncorhynchus mykiss. Carcinogenesis 14:211–217. https://doi.org/10.1093/carcin/14.2.211

    Article  CAS  PubMed  Google Scholar 

  21. Kaya H (2012) Tilapia’da (Oreochromis mossambicus) kurşun toksisitesi: oksidatif stres ve bazı fizyolojik etkiler. Canakkale 18 Mart University

  22. Ural MS, Parlak AE, Alayunt NÖ (2013) Farklı ortamlarda yetişen gökkuşağı alabalığı’nın (Oncorhynchus mykiss Walbaum, 1792) bazı kan parametrelerinin karşılaştırılması. Fırat Unv J Sci 25:19–26

    Google Scholar 

  23. Vazirzadeh A, Roosta H, Masoumi H et al (2020) Long-term effects of three probiotics, singular or combined, on serum innate immune parameters and expressions of cytokine genes in rainbow trout during grow-out. Fish Shellfish Immunol 98:748–757. https://doi.org/10.1016/j.fsi.2019.11.023

    Article  CAS  PubMed  Google Scholar 

  24. Wedemeyer G, Chatterton K (1970) Some blood chemistry values for the rainbow trout (Salmo gairdneri ). J Fish Res Board Can 27:1162–1164. https://doi.org/10.1139/f70-135

    Article  CAS  Google Scholar 

  25. Al-Kahtani MA (2011) Effect of an insecticide abamectin on some biochemical characteristics of tilapia fish (Oreochromis Niloticus). Am J Agric Biol Sci 6:62–68. https://doi.org/10.3844/ajabssp.2011.62.68

    Article  CAS  Google Scholar 

  26. Sakin F, Yonar SM, Enis Yonar M, Saglam N (2012) Changes in selected immunological parameters and oxidative stress responses in different organs of Oncorhynchus mykiss exposed to ivermectin. Rev Chim 63:989–995

    CAS  Google Scholar 

  27. Remia KM, Logaswamy S, Logankumar K, Rajmohan D (2008) Effect of an insecticide (Monocrotophos) on some biochemical constituents of the fish Tilapia mossambica. Pollut Res 27:523–526

    CAS  Google Scholar 

  28. Celik EŞ, Aslan A, Alparslan M (2008) Balıklarda kan glukozunu etkileyen başlıca faktörler. Erciyes Üniversitesi Fen Bilim Enstitüsü Fen Bilim Derg 24:364–379

    Google Scholar 

  29. Aslan A (2009) Çanakkale Boğazı’ndaki izmarit balığının, Spicara maena (Linnaeus,1758), bazı hematolojik vebiyokimyasalkan parametrelerinin belirlenmesi. Canakkale 18 Mart University

  30. Katharios P, Iliopoulou-Georgudaki J, Kapata-Zoumbos K, Spiropoulos S (2002) Toxicity of intraperitoneally injected ivermectin in sea bream, Sparus aurata. Fish Physiol Biochem 25:99–108. https://doi.org/10.1023/A:1020574810332

    Article  Google Scholar 

  31. Eder C (2009) Mechanisms of interleukin-1β release. Immunobiology 214:543–553. https://doi.org/10.1016/j.imbio.2008.11.007

    Article  CAS  PubMed  Google Scholar 

  32. Rebl A, Goldammer T, Seyfert H-M (2010) Toll-like receptor signaling in bony fish. Vet Immunol Immunopathol 134:139–150. https://doi.org/10.1016/j.vetimm.2009.09.021

    Article  CAS  PubMed  Google Scholar 

  33. Franklin CE, Davison W, McKenzie JC (1993) The role of the spleen during exercise in the Antarctic Teleost, Pagothenia Borchgrevinki. J Exp Biol 174:381–386

    Google Scholar 

  34. Gao B, Jeong W-I, Tian Z (2007) Liver: an organ with predominant innate immunity. Hepatology 47:729–736. https://doi.org/10.1002/hep.22034

    Article  CAS  Google Scholar 

  35. Rymuszka A, Adaszek Ł (2012) Pro- and anti-inflammatory cytokine expression in carp blood and head kidney leukocytes exposed to cyanotoxin stress – An in vitro study. Fish Shellfish Immunol 33:382–388. https://doi.org/10.1016/j.fsi.2012.05.021

    Article  CAS  PubMed  Google Scholar 

  36. Poley J, Purcell SL, Igboeli OO et al (2013) Combinatorial effects of administration of immunostimulatory compounds in feed and follow-up administration of triple-dose SLICE ® (emamectin benzoate) on Atlantic salmon, Salmo salar L., infection with Lepeophtheirus salmonis. J Fish Dis 36:299–309. https://doi.org/10.1111/jfd.12062

    Article  CAS  PubMed  Google Scholar 

  37. Cárcamo JG, Aguilar MN, Barrientos CA et al (2011) Effect of emamectin benzoate on transcriptional expression of cytochromes P450 and the multidrug transporters (Pgp and MRP1) in rainbow trout (Oncorhynchus mykiss) and the sea lice Caligus rogercresseyi. Aquaculture 321:207–215. https://doi.org/10.1016/j.aquaculture.2011.09.012

    Article  CAS  Google Scholar 

  38. Roca FJ, Mulero I, López-Muñoz A et al (2008) Evolution of the inflammatory response in vertebrates: fish TNF-α is a powerful activator of endothelial cells but hardly activates phagocytes. J Immunol 181:5071–5081. https://doi.org/10.4049/jimmunol.181.7.5071

    Article  CAS  PubMed  Google Scholar 

  39. Patibandla S, Jiang J-Q, Shu X (2018) Toxicity assessment of four pharmaceuticals in aquatic environment before and after ferrate(VI) treatment. J Environ Chem Eng 6:3787–3797. https://doi.org/10.1016/j.jece.2018.05.024

    Article  CAS  Google Scholar 

  40. Wang Y, Wu S, Chen J et al (2018) Single and joint toxicity assessment of four currently used pesticides to zebrafish (Danio rerio) using traditional and molecular endpoints. Chemosphere 192:14–23. https://doi.org/10.1016/j.chemosphere.2017.10.129

    Article  CAS  PubMed  Google Scholar 

  41. Goetz F (2004) Tumor necrosis factors. Dev Comp Immunol 28:487–497. https://doi.org/10.1016/j.dci.2003.09.008

    Article  CAS  PubMed  Google Scholar 

  42. Fierro-Castro C, Barrioluengo L, López-Fierro P et al (2013) Fish cell cultures as in vitro models of inflammatory responses elicited by immunostimulants. Expression of regulatory genes of the innate immune response. Fish Shellfish Immunol 35:979–987. https://doi.org/10.1016/j.fsi.2013.07.015

    Article  CAS  PubMed  Google Scholar 

  43. Kontas-Askar T, Ergun N, Turunc V (2007) Isı şok proteinler ve fizyolojik rolleri. Kafkas Üniversitesi Vet Fakültesi Derg 13:109–114

    Google Scholar 

  44. Baykal Y, Gok F, Kocabalkan F (2000) Isı şok proteinleri ve hastalıklardaki rolü. T Klin J Med Sci 20:187–195

    Google Scholar 

  45. Olsvik PA, Lie KK, Mykkeltvedt E et al (2008) Pharmacokinetics and transcriptional effects of the anti-salmon lice drug emamectin benzoate in Atlantic salmon (Salmo salar L.). BMC Pharmacol 8:16. https://doi.org/10.1186/1471-2210-8-16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Alak G, Yeltekin AÇ, Tas IH et al (2017) Investigation of 8-OHdG, CYP1A, HSP70 and transcriptional analyses of antioxidant defence system in liver tissues of rainbow trout exposed to eprinomectin. Fish Shellfish Immunol 65:136–144. https://doi.org/10.1016/j.fsi.2017.04.004

    Article  CAS  PubMed  Google Scholar 

  47. Fast MD, Johnson SC, Jones SRM (2007) Differential expression of the pro-inflammatory cytokines IL-1β-1, TNFα-1 and IL-8 in vaccinated pink (Oncorhynchus gorbuscha) and chum (Oncorhynchus keta) salmon juveniles. Fish Shellfish Immunol 22:403–407. https://doi.org/10.1016/j.fsi.2006.06.012

    Article  CAS  PubMed  Google Scholar 

  48. Omaima Harun N, Zou J, Zhang Y-A et al (2008) The biological effects of rainbow trout (Oncorhynchus mykiss) recombinant interleukin-8. Dev Comp Immunol 32:673–681. https://doi.org/10.1016/j.dci.2007.10.005

    Article  CAS  Google Scholar 

  49. Jin Y, Chen R, Liu W, Fu Z (2010) Effect of endocrine disrupting chemicals on the transcription of genes related to the innate immune system in the early developmental stage of zebrafish (Danio rerio). Fish Shellfish Immunol 28:854–861. https://doi.org/10.1016/j.fsi.2010.02.009

    Article  CAS  PubMed  Google Scholar 

  50. Cantalamessa F (1993) Acute toxicity of two pyrethroids, permethrin, and cypermethrin in neonatal and adult rats. Arch Toxicol 67:510–513. https://doi.org/10.1007/BF01969923

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by Mersin University Scientific Research Unit [Grant Number 2016-2-TP3-1874].

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KS and AO—Authors worked in field. KS, YBM and OH—Authors worked in laboratory.

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Correspondence to Serdar Kilercioglu.

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The protocol of the research study was approved by the Animal Experiments Ethics Committee of Mersin University, Mersin, Turkey. Paper no: 52602694-050/E.98219. It was loaded to system.

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Kilercioglu, S., Ay, O., Oksuz, H. et al. The effects of the neurotoxic agent emamectin benzoate on the expression of immune and stress-related genes and blood serum profiles in the Rainbow trout. Mol Biol Rep 47, 5243–5251 (2020). https://doi.org/10.1007/s11033-020-05599-w

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