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Effects of (Anti) Androgenic Endocrine Disruptors (DEHP and Butachlor) on Immunoglobulin M (IgM) and Leukocytes Counts of Male Rainbow Trout (Oncorhynchus mykiss)

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Abstract

The effect of two anti-androgenic endocrine disrupting compounds, i.e. the plasticizer di (2-ethylhexyl) phthalate (DEHP) and herbicide butachlor, were evaluated for their effects on immunoglobulin M (IgM) and leukocytes in male rainbow trout. Also, plasma testosterone (T) concentration was measured to confirm their anti-androgenic effects. In the first experiment, trout were treated with 50 mg/kg (body weight) DEHP intraperitoneally, and in the second one, fish were exposed to 0.39 mg/L butachlor for 10 days. The results showed that T concentrations and white blood cells were significantly lower in fish exposed to either DEHP or butachlor compared to control fish (p < 0.05). Fish showed significantly elevated neutrophil levels and decreased lymphocyte levels in the butachlor (p < 0.05); however, no significant difference was observed in lymphocyte and neutrophils values in the DEHP treatment (p > 0.05). In addition, no significant differences were found in IgM, eosinophil and monocyte parameters in either DEHP or butachlor treatments (p > 0.05). These results confirmed that leukocytes counts can be considered as a novel marker of immunotoxicity triggered by (anti) androgenic endocrine disruptors.

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References

  • Ahmed SA (2000) The immune system as a potential target for environmental estrogens (endocrine disrupters): a new emerging field. Toxicology 150:191–206. doi:10.1016/S0300-483X(00)00259-6

    Article  CAS  Google Scholar 

  • Chang J, Gui W, Wang M, Zhu G (2013) Effects of butachlor on reproduction and hormone levels in adult zebrafish (Danio rerio). Exp Toxicol Pathol 65:205–209. doi:10.1016/j.etp.2011.08.007

    Article  CAS  Google Scholar 

  • Chapin RE, Harris MW, Davis BJ, Ward SM, Wilson RE, Mauney MA, Lockhart AC, Smialowicz RJ, Moser VC, Burka LT, Collins BJ (1997) The effects of perinatal: juvenile methoxychlor exposure on adult rat nervous, immune, and reproductive system function. Fundam Appl Toxicol 40:138–157. doi:10.1006/faat.1997.2381

    Article  CAS  Google Scholar 

  • Crago J, Klaper R (2012) A mixture of an environmentally realistic concentration of a phthalate and herbicide reduces testosterone in male fathead minnow (Pimephales promelas) through a novel mechanism of action. Aquat Toxicol 110–111:74–83. doi:10.1016/j.aquatox.2011.12.021

    Article  Google Scholar 

  • Cravedi JP, Perdu-Durand E (2002) The phthalate diesters DEHP and DBP do not induce lauric acid hydroxylase activity in rainbow trout. Mar Environ Res 54:787–791. doi:10.1016/S0141-1136(02)00196-4

    Article  CAS  Google Scholar 

  • Cuesta A, Meseguer J, Angeles Esteban M (2008) Effects of the organochlorines p, p’-DDE and lindane on gilthead seabream leucocyte immune parameters and gene expression. Fish Shellfish Immunol 25:682–6888. doi:10.1016/j.fsi.2008.02.006

    Article  CAS  Google Scholar 

  • Del Buano D, Scarponi L, Amato RD (2005) An analytical method for the simultaneous determination of butachlor and benoxacor in wheat and soil. J Agric Food Chem 53:4326–4330. doi:10.1021/jf050127d

    Article  Google Scholar 

  • European Commission (2003) Eu risk assessment report for 1,2- benzenedicarboxylic acid, di-c9-11-branched alkyl esters, c10 rich and di-“isodecyl” phthalate (DIDP), vol. 36. European Chemicals Bureau

  • Filby AL, Thorpe KL, Maack G, Tyler CR (2007) Gene expression profiles revealing the mechanisms of anti-androgen- and estrogen-induced feminization in fish. Aquat Toxicol 81:219–231. doi:10.1016/j.aquatox.2006.12.003

    Article  CAS  Google Scholar 

  • Finne EF, Cooper GA, Koop BF, Hylland K, Tollefsen KE (2007) Toxicogenomic responses in rainbow trout (Oncorhynchus mykiss) hepatocytes exposed to model chemicals and a synthetic mixture. Aquat Toxicol 81:293–303. doi:10.1016/j.aquatox.2006.12.010

    Article  CAS  Google Scholar 

  • Fromme H, Küchler T, Otto T, Pilz K, Müller J, Wenzel A (2002) Occurrence of phthalates and bisphenol A and F in the environment. Water Res 36:1429–1438. doi:10.1016/S0043-1354(01)00367-0

    Article  CAS  Google Scholar 

  • Gilliver SC (2010) Sex steroids as inflammatory regulators. J Steroid Biochem Mol Biol 120:105–115. doi:10.1016/j.jsbmb.2009.12.015

    Article  CAS  Google Scholar 

  • Guo HR, Yin LC, Zhang SC, Feng WR (2010) The toxic mechanism of high lethality of herbicide butachlor in marine flatfish flounder, Paralichthys olivaceus. J Ocean Univ China 9:257–264. doi:10.1007/s11802-010-1693-1

    Article  CAS  Google Scholar 

  • Hernández-Díaz S, Mitchell AA, Kelley KE, Calafat AM, Hauser R (2009) Medications as a potential source of exposure to phthalates in the US population. Environ Health Perspect 117:185–189. doi:10.1289/ehp.11766

    Article  Google Scholar 

  • Heudorf J, Mersch-Sundermann V, Angerer J (2007) Phthalates: toxicology and exposure. Int J Hyg Environ Health 210:623–634. doi:10.1016/j.ijheh.2007.07.011

    Article  CAS  Google Scholar 

  • Hou Y, Suzuki Y, Aida K (1999) Effects of steroid hormones on immunoglobulin M (IgM) in rainbow trout (Oncorhynchus mykiss). Fish Physiol Biochem 20:155–162. doi:10.1023/A:1007799617597

    Article  CAS  Google Scholar 

  • 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. doi:10.1016/j.fsi.2010.02.009

    Article  CAS  Google Scholar 

  • Jobling S, Reynolds T, White R, Parker MG, Sumpter JP (1995) A variety of environmentally persistent chemicals including some phthalate plasticizers are weakly estrogenic. Environ Health Perspect 103:582–587

    Article  CAS  Google Scholar 

  • Junghans M, Backhaus T, Faust M, Scholze M, Grimme LH (2003) Predictability of combined effects of eight chloroacetanilide herbicides on algal reproduction. Pest Manag Sci 59:1101–1110. doi:10.1002/ps.735

    Article  CAS  Google Scholar 

  • Klontz GW (1994) Fish hematology. In: Stolen JS, Fletcher TC, Rowley AF, Kelikoff TC, Kaattari SL, Smith SA (eds) Techniques in fish immunology, vol 3., SOS PublicationsFair Haven, NJ, pp 121–132

    Google Scholar 

  • Kurtz J, Kalbe M, Langefors A, Mayer I, Milinski M, Hasselquist D (2007) An experimental test of the immunocompetence handicap hypothesis in a teleost fish: 11-ketotestosterone suppresses innate immunity in three-spined sticklebacks. Am Nat 170:509–519. doi:10.1086/521316

    Article  Google Scholar 

  • Lasheidani M, Balouchi SN, Keyvan A, Jamili S, Falakru K (2008) Effect of butachlor on density, volume and number of abnormal sperms in caspian kutum (Rutilus Frisii Kutum). Res J Environ Sci 2:474–482. doi:10.3923/rjes.2008.474.482

    Article  CAS  Google Scholar 

  • Law WY, Chen WH, Song YL, Dufour S, Chang CF (2001) Differential in vitro suppressive effects of steroids on leukocyte phagocytosis in two teleosts tilapia and common carp. Gen Comp Endocrinol 121:163–172. doi:10.1006/gcen.2000.7593

    Article  CAS  Google Scholar 

  • Lutton B, Callard I (2006) Evolution of reproductive immune interactions. Integr Comp Biol 46:1060–1071. doi:10.1093/icb/icl050

    Article  CAS  Google Scholar 

  • Lynn SG, Birge WJ, Shepherd BS (2008) Molecular characterization and sex-specific tissue expression of estrogen receptor alpha (esr1) estrogen receptor beta a (esr2a) and ovarian aromatase (cyp19a1a) in yellow perch (Perca flavescens). Comp Biochem Physiol B Biochem Mol Biol 149:126–147. doi:10.1016/j.cbpb.2007.09.001

    Article  Google Scholar 

  • Miles DB, Sinervo B, Hazard C, Svensson EI, Costa D (2007) Relating endocrinology physiology and behaviour using species with alternative mating strategies. Funct Ecol 21:653–665. doi:10.1111/j.1365-2435.2007.01304.x

    Article  Google Scholar 

  • Milla S, Depiereux S, Kestemont P (2011) The effects of estrogenic and androgenic endocrine disruptors on the immune system of fish: a review. Ecotoxicology 20:305–319. doi:10.1007/s10646-010-0588-7

    Article  CAS  Google Scholar 

  • Misumi I, Yada T, Leong JA, Schreck CB (2009) The effect of in vitro exposure to tributyltin on the immune competence of chinook Salmon (Oncorhynchus tshawytscha) leukocytes. Arch Environ Contam Toxicol 56:229–237. doi:10.1007/s00244-008-9187-5

    Article  CAS  Google Scholar 

  • Onorato TM, Brown PW, Morris PL (2008) Mono-(2-ethylhexyl) phthalate increases spermatocyte mitochondrial peroxiredoxin 3 and cyclooxygenase 2. J Androl 29:293–303. doi:10.2164/jandrol.107.003335

    Article  CAS  Google Scholar 

  • Petrovic M, Eljarrat E, López de Alda MJ, Barceló D (2001) Analysis and environmental levels of endocrine-disrupting compounds in freshwater sediments. TrAC Trends Anal Chem 20:637–648. doi:10.1016/S0165-9936(01)00118-2

    Article  CAS  Google Scholar 

  • Roberts ML, Buchanan KL, Evans MR (2004) Testing the immunocompetence handicap hypothesis: a review of the evidence. Anim Behav 68:227–239. doi:10.1016/j.anbehav.2004.05.001

    Article  Google Scholar 

  • Robertson OH (1961) Prolongation of the life span of Kokanee salmon (Oncorhynchus nerka kennerlyi) by castration before beginning of gonad development. Proc Natl Acad Sci USA 47:609–621. doi:10.1073/pnas.47.4.609

    Article  CAS  Google Scholar 

  • Ros AF, Ferreira C, Santos RS, Oliveira RF (2006) Regulation of immunocompetence by different androgen metabolites in a blenny with alternative reproductive tactics. J Exp Zool A Comp Exp Biol 305:986–994. doi:10.1002/jez.a.349

    Article  Google Scholar 

  • Saha NR, Usami T, Suzuki Y (2004) In vitro effects of steroid hormones on IgM-secreting cells and IgM secretion in common carp (Cyprinus carpio). Fish Shellfish Immunol 17:149–158. doi:10.1016/j.fsi.2004.01.001

    Article  CAS  Google Scholar 

  • Shved N, Berishvili G, Hausermann E, D’Cotta H, Baroiller JF, Eppler E (2009) Challenge with 17alpha-ethinylestradiol (EE2) during early development persistently impairs growth differentiation and local expression of IGF-I and IGFII in immune organs of tilapia. Fish Shellfish Immunol 26:524–530. doi:10.1016/j.fsi.2009.02.003

    Article  CAS  Google Scholar 

  • Slater CH, Schreck CB (1997) Physiological levels of testosterone kill salmonid leukocytes in vitro. Gen Comp Endocrinol 106:113–119. doi:10.1006/gcen.1996.6858

    Article  CAS  Google Scholar 

  • Slater CH, Fitzpatrick MS, Schreck CB (1995) Characterization of an androgen receptor in salmonid lymphocytes: possible link to androgen-induced immunosuppression. Gen Comp Endocrinol 100:218–225. doi:10.1006/gcen.1995.1151

    Article  CAS  Google Scholar 

  • Suzuki Y, Otaka T, Sato S, Hou YY, Aida K (1997) Reproduction related immunoglobulin changes in rainbow trout. Fish Physiol Biochem 17:415–421. doi:10.1023/A:1007795827112

    Article  CAS  Google Scholar 

  • Tait AS, Butts CL, Sternberg EM (2008) The role of glucocorticoids and progestins in inflammatory, autoimmune, and infectious disease. J Leukoc Biol 84:924–931. doi:10.1189/jlb.0208104

    Article  CAS  Google Scholar 

  • Tellez-Bañuelos MC, Santerre A, Casas-Solis J, Zaitseva G (2010) Endosulfan increases seric interleukin-2 like (IL-2L) factor and immunoglobulin M (IgM) of Nile tilapia (Oreochromis niloticus) challenged with Aeromona hydrophila. Fish Shellfish Immunol 28:401–405. doi:10.1016/j.fsi.2009.11.017

    Article  Google Scholar 

  • Thibaut R, Porte C (2004) Effects of endocrine disrupters on sex steroid synthesis and metabolism pathways in fish. J Steroid Biochem Mol Biol 92:485–494. doi:10.1016/j.jsbmb.2004.10.008

    Article  CAS  Google Scholar 

  • Todo T, Ikeuchi T, Kobayashi T, Nagahama Y (1999) Fish androgen receptor: cDNA cloning steroid activation of transcription in transfected mammalian cells and tissue mRNA levels. Biochem Biophys Res Commun 254:378–383. doi:10.1006/bbrc.1998.9919

    Article  CAS  Google Scholar 

  • Tollefsen KE (2002) Interaction of estrogen mimics, singly and in combination, with plasma sex steroid-binding proteins in rainbow trout (Oncorhynchus mykiss). Aquat Toxicol 56:215–225. doi:10.1016/S0166-445X(01)00154-0

    Article  CAS  Google Scholar 

  • Tomlin C (1994) The pesticide manual, 10th edn. Crop Protection Publications, British Crop Protection Council, Farnham

    Google Scholar 

  • Tu W, Niu L, Liu W, Xu C (2013) Embryonic exposure to butachlor in zebrafish (Danio rerio): endocrine disruption, developmental toxicity and immunotoxicity. Ecotoxicol Environ Saf 89:189–195. doi:10.1016/j.ecoenv.2012.11.031

    Article  CAS  Google Scholar 

  • Uren-Webster TM, Lewis C, Filby AL, Paull GC, Santos EM (2010) Mechanisms of toxicity of di(2-ethylhexyl) phthalate on the reproductive health of male zebrafish. Aquat Toxicol 99:360–369. doi:10.1016/j.aquatox.2010.05.015

    Article  CAS  Google Scholar 

  • Viney ME, Riley EM, Buchanan KL (2005) Optimal immune responses: immunocompetence revisited. Trends Ecol Evol 20:665–669. doi:10.1016/j.tree.2005.10.003

    Article  Google Scholar 

  • Weeks BA, Anderson DP, DuFour AP, Fairbrother A, Goven AJ, Lahvis GP, Peters G (1992) Immunological biomarkers to assess environmental stress. In: Huggett RJ, Kimerle RA, Mehrle PM, Bergmann HL (eds) Biomarkers: biochemical physiological and histological markers of anthropogenic stress. Lewis Publishers, Boca Raton, pp 211–234

    Google Scholar 

  • Wester PW, Vethaak AD, van Muiswinkel WB (1994) Fish as biomarkers in immunotoxicology. Toxicology 86:213–232. doi:10.1016/0300-483X(94)90005-1

    Article  CAS  Google Scholar 

  • Yu YL, Chen YX, Luo YM, Pan XD, He YF, Wong MH (2003) Rapid degradation of butachlor in wheat rhizosphere soil. Chemosphere 50:771–774. doi:10.1016/S0045-6535(02)00218-7

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Aquatic Animal Health, Faculty of Veterinary Medicine, University of Tehran, P.O. Box: 14155-6453, Tehran, Iran

    Sohrab Ahmadivand & Ashkan Zargar

  2. Department of Fisheries, Faculty of Natural Resources, University of Tehran, P.O. Box 4314, Karaj, Iran

    Hamid Farahmand, Alireza Mirvaghefi & Soheil Eagderi

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  1. Sohrab Ahmadivand
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  2. Hamid Farahmand
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  3. Alireza Mirvaghefi
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  4. Soheil Eagderi
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  5. Ashkan Zargar
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Correspondence to Hamid Farahmand.

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Ahmadivand, S., Farahmand, H., Mirvaghefi, A. et al. Effects of (Anti) Androgenic Endocrine Disruptors (DEHP and Butachlor) on Immunoglobulin M (IgM) and Leukocytes Counts of Male Rainbow Trout (Oncorhynchus mykiss). Bull Environ Contam Toxicol 94, 695–700 (2015). https://doi.org/10.1007/s00128-015-1503-y

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