Abstract
The present study evaluated the effects of low doses of atrazine administered during gestation and breastfeeding on sperm characteristics of the wild rodent Calomys laucha. Adult females were divided into groups of 10 and administered different doses of atrazine through gavage, during gestational or breastfeeding period. At 3 months of age, the F1 adult male progeny of these females was evaluated. We observed a drastic reduction in the total and progressive motility of male sperm cells at all doses and during both the exposure periods. Moreover, the plasma membrane integrity of adult male sperm cells decreased at all doses of atrazine administered during the breastfeeding, whereas the membrane fluidity of these cells increased at all tested doses. Atrazine led to a decrease in the sperm mitochondrial functionality at all doses and during both exposure periods. The damage to the sperm DNA was higher in males exposed to the highest dose (1.0 mg/kg) during the gestation period, and in animals exposed to the lowest dose of atrazine (0.1 mg/kg) during breastfeeding period. Furthermore, the highest dose (1.0 mg/kg) of atrazine reduced the sperm concentration. Furthermore, the reduced levels of reactive oxygen species (ROS) were observed at all evaluated doses in males exposed during the gestation period. These results suggest that the administration of low doses of atrazine at critical periods of development may permanently reduce the sperm quality in C. laucha.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abarikwu SO, Adesiyan AC, Oyeloja TO, Oyeyemi MO, Farombi EO (2010) Changes in sperm characteristics and induction of oxidative stress in the testis and epididymis of experimental rats by a herbicide, atrazine. Arch Environ Contam Toxicol 58:874–882. https://doi.org/10.1007/s00244-009-9371-2
Abarikwu SO, Akiri OF, Durojaiye MA, Adenike A (2015) Combined effects of repeated administration of Bretmont Wipeout (glyphosate) and Ultrazin (atrazine) on testosterone, oxidative stress and sperm quality of Wistar rats. Toxicol Mech Methods 25(1):70–80. https://doi.org/10.3109/15376516.2014.989349
Abarikwu SO, Duru QC, Chinonso OV, Njoku RC (2016) Antioxidant enzymes activity, lipid peroxidation, oxidative damage in the testis and epididymis, and steroidogenesis in rats after co-exposure to atrazine and ethanol. Andrologia 48:548–557. https://doi.org/10.1111/and.12478
Adesiyan AC, Oyeloja TO, Abarikwu SO, Oyeyemi MO, Farombi EO (2011) Selenium provides protection to the liver but not the reproductive organs in an atrazine-model of experimental toxicity. Exp Toxicol Pathol 63:201–207. https://doi.org/10.1016/j.etp.2009.11.008
Alche LE, Coto CE (1993) In vitro selection of Junin vírus antigenic variants. Arch Virol 128:389–394. https://doi.org/10.1007/bf01309449
ANVISA Agência Nacional de Vigilância Sanitária (2003) Resolução Nº 899, de 29 de maio de 2003. Provides for a guide for validation of analytical and bioanalytical methods. Brasília, DF, Brazil
Balao da Silva CM, Ortega Ferrusola C, Morillo Rodriguez A, Gallardo Bolaños JM, Plaza Dávila M, Morrell JM, Rodriguez Martínez H, Tapia JA, Aparicio IM, Peña FJ (2013) Sex sorting increases the permeability of the membrane of stallion spermatozoa. Anim Reprod Sci 138:241–251. https://doi.org/10.1016/j.anireprosci.2013.02.021
Breckenridge CB, Coder PS, Tisdel MO, Simpkins JW, Yi KD, Foradori CD, Handa RJ (2015) Effect of age, duration of exposure, and dose of atrazine on sexual maturation and the luteinizing hormone surge in the female Sprague–Dawley rat. Birth Defects Res B 104:204–217. https://doi.org/10.1002/bdrb.21154
Breitzka RL, Sandritter TL, Hatzopoulos FK (1997) Principles of drug transfer into breast milk and drug disposition in the nursing infant. J Hum Lact 13:155–158. https://doi.org/10.1177/089033449701300219
Breslin WJ, Liberacki AB, Dittenber DA, Quast JF (1996) Evaluation of the developmental and reproductive toxicity of chlorpyrifos in the rat. Fundam Appl Toxicol 29:119–130. https://doi.org/10.1006/faat.1996.0013
Bridges DC (2008) Benefits of triazine herbicides in corn and sorghum production. In: LeBaron HM, McFarland JE, Burnside C (eds) The triazine herbicides: 50 years revolutionizing agriculture, Edn1 edn. Elsevier, San Diego, pp 163–174
CONAMA Conselho Nacional do Meio Ambiente (2005) Resolução Nº 357, de 17 de março de 2005. Provides for the classification of water bodies and environmental guidelines for their classification, as well as establishes the conditions and standards for the discharge of effluents, and other measures. Brasília, DF, Brazil
Copeland WC (2002) Mitochondrial DNA: methods and protocols. In: Methods in molecular biology, edn 197 edn, 420p. Humana Press, Totowa
DeSesso JM, Scialli AR, White TEK, Breckenridge CB (2014) Multigeneration reproduction and male development toxicity studies on atrazine in rats. Birth Defects Res B Dev Reprod Toxicol 101:237–253. https://doi.org/10.1002/bdrb.21106
Domínguez-Rebolledo AE, Martínez-Pastor F, Bisbal AF, Ros-Santaella JL, GarcíaÁlvarez O, Maroto-Morales A, Soler AJ, Garde JJ, Fernández-Santos MR (2011) Response of thawed epididymal red deer spermatozoa to increasing concentrations of hydrogenperoxide, and importance of individual male variability. Reprod Domest Anim 46:393–403. https://doi.org/10.1111/j.1439-0531.2010.01677.x
Fernández-Gago R, Domínguez JC, Martínez-Pastor F (2013) Seminal plasma applied post-thawing affects boar sperm physiology: flow cytometry study. Theriogenology 80:400–410. https://doi.org/10.1016/j.theriogenology.2013.05.003
Feyzi-Dehkhargani S, Shahrooz R, Malekineja H, Sadrkhanloo RA (2012) Atrazine in sub-acute exposure results in sperm DNA disintegrity and nuclear immaturity in rats. Vet Res Forum 3:19–26 PMCID:PMC4312814
Forest CL (1983) Specific contact between mating structure membranes observed in conditional fusion-defective Chlamydomonas mutants. Exp Cell Res 148:143–154. https://doi.org/10.1016/0014-4827(83)90194-5
Fraites MJ, Narotsky MG, Best DS, Stoker TE, Davis LK, Goldman JM, Hotchkiss MG, Klinefelter GR, Kamel A, Qian Y et al (2011) Gestational atrazine exposure: effects on male reproductive development and metabolite distribution in the dam, fetus, and neonate. Reprod Toxicol 32:52–63. https://doi.org/10.1016/j.reprotox.2011.04.003
Friedmann AS (2002) Atrazine inhibition of testosterone production in rat males following peripubertal exposure. Reprod Toxicol 16:275–279. https://doi.org/10.1016/S0890-6238(02)00019-9
García MA, Santaeufemia M, Melgar MJ (2012) Triazine residues in raw milk and infant formulas from Spanish northwest, by a diphasic dialysis extraction. Food Chem Toxicol 50:503–510. https://doi.org/10.1016/j.fct.2011.11.019
Gely-Pernot A, Hao C, Becker E, Stuparevic I, Kervarrec C, Chalmel F, Primig M, Jégou B, Smagulova F (2015) The epigenetic processes of meiosis in male mice are broadly affected by the widely used herbicide atrazine. BMC Genomics 16:885. https://doi.org/10.1186/s12864-015-2095-y
Hao C, Gely-Pernot A, Kervarrec C, Boudjema M, Becker E, Khil P, Tevosian S, Jégou B, Smagulova F (2016) Exposure to the widely used herbicide atrazine results in deregulation of global tissue-specific RNA transcription in the third generation and is associated with a global decrease of histone trimethylation in mice. Nucleic Acids Res 44(20):9784–9802. https://doi.org/10.1093/nar/gkw840
Jablonowski ND, Schäffer A, Burauel P (2011) Still present after all these years: Persistence plus potential toxicity raise questions about the use of atrazine. Environ Sci Pollut Res 18:328–331. https://doi.org/10.1007/s11356-010-0431-y
Jasperses VL, Covaci A, Voorspoels S, Dauwe T, Eens M, Schepens P (2005) Brominated flame retardants and organochlorine pollutants in a quatic and terrestrial predatory birds of Belgium: levels, patterns, tissue distribution and condition factors. Environ Pollut 139:340–352. https://doi.org/10.1016/j.envpol.2005.05.008
Jestadi DB, Phaniendra A, Babji U, Shanmuganathan B, Periyasamy L (2014) Effects of atrazine on reproductive health of nondiabetic and diabetic male rats. Int Scholarly Res Notices 676013:1–7. https://doi.org/10.1155/2014/676013
Jin Y, Zhang X, Shu L, Chen L, Sun L, Qian H, Liu W, Fu Z (2010) Oxidative stress response and gene expression with atrazine exposure in adult female zebrafish (Danio rerio). Chemosphere 78:846–852. https://doi.org/10.1016/j.chemosphere.2009.11.044
Jin Y, Wang L, Fu Z (2013) Oral exposure to atrazine modulates hormone synthesis and the transcription of steroidogeneic genes in male peripubertal mice. Gen Comp Endocrinol 184:120–127. https://doi.org/10.1016/j.ygcen.2013.01.010
Kniewald J, Jakominic M, Tomljenovic A, Simic B, Romac P, Vranesic D, Kniewald Z (2000) Disorders of male rat reproductive tract under the influence of atrazine. J Appl Toxicol 20:61–68. https://doi.org/10.1002/(SICI)1099-1263(200001/02)20:1<61::AID-JAT628>3.0.CO;2-3
LeBaron HM, MacFarland JE, Burnside C (2008) The triazine herbicides: a milestone in the development of weed control technology. In: LeBaron HM, McFarland JE, Burnside C (eds) The triazine herbicides: 50 years revolutionizing agriculture, Edn1 edn. Elsevier, San Diego, pp 1–12
Lim S, Ahn SY, Song IC, Chung MH, Jang HC, Park KS, Lee KU, Pak YK, Lee HK (2009) Chronic exposure to the herbicide, atrazine, causes mitochondrial dysfunction and insulin resistance. PLoS One 4(4):e5186. https://doi.org/10.1371/journal.pone.0005186
Lin J, Zhao H, Qin L, Li XN, Zhang C, Xia J, Li JL (2018) Atrazine triggers mitochondrial dysfunction and oxidative stress in quail (Coturnix C. coturnix) cerebrum via activating xenobiotic-sensing nuclear receptors and modulating cytochrome P450 systems. J Agric Food Chem 66(25):6402–6413. https://doi.org/10.1021/acs.jafc.8b01413
Mansour SA, Mohamed DA, Sutra JF (2014) Which exposure stage (gestation or lactation) is more vulnerable to atrazine toxicity? Studies on mouse dams and their pups. Toxicol Rep 1:53–68. https://doi.org/10.1016/j.toxrep.2014.04.001
McBirney M, King SE, Pappalardo M, Houser E, Unkefer M, Nilsson E, Sadler-Riggleman I, Beck D, Winchester P, Skinner MK (2017) Atrazine induced epigenetic transgenerational inheritance of disease, lean phenotype and sperm epimutation pathology biomarkers. PLoS One 12(9):e0184306. https://doi.org/10.1371/journal.pone.0184306
Mills JN, Ellis BA, Childs JE, Maiztegui JL, Castro-Vasquez A (1992) Seasonal changes in mass and reproductive condition of the corn mouse (Calomys musculinus) on the Argentine pampa. J Mammal 73:876–884. https://doi.org/10.2307/1382210
Moreira JC, Peres F, Simões AC, Pignati WA, Dores EC, Vieira SN, Strüssmann C, Mott T (2012) Contaminação de águas superficiais e de chuva por agrotóxicos em uma região do estado do Mato Grosso. Ciência e Saúde Coletiva 17:1557–1568. https://doi.org/10.1590/S1413-81232012000600019
Nwani CD, Lakra WS, Nagpure NS, Kumar R, Kushwaha B, Srivastava SK (2010) Toxicity of the herbicide atrazine: effects on lipid peroxidation and activities of antioxidant enzymes in the freshwater fish Channa punctatus (Bloch). Int J Environ Res Public Health 7:3298–3312. https://doi.org/10.3390/ijerph7083298
Oliveira-Brett AM, Silva LA (2002) A DNA-electrochemical biosensor for screening environmental damage caused by s-triazinederivatives. Anal Bioanal Chem 373:717–723. https://doi.org/10.1007/s00216-002-1259-1
Peighambarzadeh SZ, Safi S, Shahtaheri SJ, Javanbakht M, Forushani AR (2011) Presence of atrazine in the biological samples of cattle and its consequence adversity in human health. Iran J Publ Health 40:112–121 PMCID:PMC3481744
Piehler E, Petrunkina AM, Ekhlasi-Hundrieser M, Töpfer-Petersen E (2005) Dynamic quantification of the tyrosine phosphorylation of the sperm surface proteins during capacitation in vitro. Cytomet 69:1062–1070. https://doi.org/10.1002/cyto.a.20338
Pogrmic K, Fa S, Dakic V, Kaisarevic S, Kovacevic R (2009) Atrazine oral exposure of peripubertal male rats downregulates steroidogenesis gene expression in Leydig cells. Toxicol Sci 111:189–197. https://doi.org/10.1093/toxsci/kfp135
Pogrmic-Majkic K, Fa S, Dakic V, Kaisarevic S, Kovacevic R (2010) Upregulation of peripubertal rat Leydig cell steroidogenesis following 24 h in vitro and in vivo exposure to atrazine. Toxicol Sci 118:52–60. https://doi.org/10.1093/toxsci/kfq227
Rosenberg BG, Chen H, Folmer J, Liu J, Papadopoulos V, Zirkin BR (2008) Gestational exposure to atrazine: effects on the postnatal development of male offspring. J Androl 29:304–311. https://doi.org/10.2164/jandrol.107.003020
Ross MK, Jones TL, Filipov NM (2009) Disposition of the herbicide 2-chloro–4-(ethylamino)–6-(isopropylamino)-S-triazine (atrazine) and its major metabolites in mice: A liquid chromatography/mass spectrometry analysis of urine, plasma, and tissue levels. Drug Metab Dispos 37:776–786. https://doi.org/10.1124/dmd.108.024927
Saalfeld GQ, Varela Junior AS, Castro T et al (2018) Low atrazine dosages reduce sperm quality of Calomys laucha mice. Environ Sci Pollut Res 25:2924. https://doi.org/10.1007/s11356-017-0657-z
Sanderson JT, Seinen W, Giesy JP, Van den Berg M (2000) 2-Chloro-s-triazine herbicides induce aromatase (CYP19) activity in H295R human adrenocortical carcinoma cells: a novel mechanism for estrogenicity? Toxicol Sci 54:121–127. https://doi.org/10.1093/toxsci/54.1.121
Silva EF, Varela-Junior AS, Cardoso TF, Stefanello FM, Kalb AC, Martínez PE, Corcini CD (2016) Reproductive toxicology of 2,4 dinitrophenol in boar sperm. Toxicol in Vitro 35:31–35. https://doi.org/10.1016/j.tiv.2016.05.002
Singh M, Sandhir R, Kiran R (2008) Atrazine-induced alterations in rat erythrocyte membranes: ameliorating effect of vitamin E. J Biochem Mol Toxicol 22:363–369. https://doi.org/10.1002/jbt.20249
Stanko JP, Enoch RR, Rayner JL, Davis CC, Wolf DC, Malarkey DE, Fenton SE (2010) Effects of gestation exposure to a low dose atrazine metabolite mixture on pubertal timing and prostate development of male Long-Evans rats. Reprod Toxicol 30:540–549. https://doi.org/10.1016/j.reprotox.2010.07.006
Stoker TE, Cooper RL (2007) Distribution of 14C-atrazine following an acute lactational exposure in the Wistar rat. Reprod Toxicol 23:607–610. https://doi.org/10.1016/j.reprotox.2007.02.004
Stoker TE, Robinette CL, Cooper RL (1999) Maternal exposure to atrazine during lactation suppresses suckling-induced prolactin release and results in prostatitis in the adult offspring. Toxicol Sci 52:68–79. https://doi.org/10.1093/toxsci/52.1.68
Stoker TE, Laws SC, Guidici DL, Cooper RL (2000) The effect of atrazine on puberty in male Wistar rats: an evaluation in the protocol for the assessment of pubertal development and thyroid function. Toxicol Sci 58:50–59. https://doi.org/10.1093/toxsci/58.1.50
Trentacoste SV, Friedmann AS, Youker RT, Breckenridge CB, Zirkein BR (2001) Atrazine effects on testosterone levels and androgen-dependent reproductive orangs in peripubertal male rats. J Androl 22:142–148. https://doi.org/10.1002/j.1939-4640.2001.tb02164.x
Victor-Costa AB, Bandeira SMC, Oliveira AG, Mahecha GAB, Oliveira CA (2010) Changes in testicular morphology and steroidogenesis in adult rats exposed to Atrazine. Reprod Toxicol 29:323–331. https://doi.org/10.1016/j.reprotox.2009.12.006
Whyatt RM, Barr DB, Camann DE, Kinney PL, Barr JR, Andrews HF, Hoepne LA, Garfinkel R, Hazi Y, Reyes A, Ramirez J, Cosme Y, Perera FP (2003) Contemporary-use pesticides in personal air samples during pregnancy and blood samples at delivery among urban minority mothers and newborns. Environ Health Perspect 111:749–756. https://doi.org/10.1289/ehp.5768
Yanagimachi R (1994) Mammalian. In: Knobil E, Niell JD (eds) The physiology of reproduction, edn 2 edn. Raven Press, New York, pp 189–317
Zeljezic D, Garaj-Vrhovac V, Perkovic P (2006) Evaluation of DNA damage induced by atrazine and atrazine-based herbicide in human lymphocytes in vitro using a comet and DNA diffusion assay. Toxicol in Vitro 20:923–935. https://doi.org/10.1016/j.tiv.2006.01.017
Acknowledgements
We thank the ReproPel team from the University of Pelotas for help with the semen analyses.
Funding
The study was financially supported by CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, Brasília, DF, Brazil).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
The capture and maintenance of the animals were approved by the Brazilian Institute for Environmental Protection (IBAMA) through Biodiversity Information and Authorization System (SISBIO: permission no. 14174). The experimental protocols were approved by the Ethics Committee of FURG (CEUA: report no. P031/2013).
Conflict of interest
The authors declare that there are no conflicts of interest.
Additional information
Responsible editor: Philippe Garrigues
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Saalfeld, G.Q., Varela Junior, A.S., Castro, T. et al. Atrazine exposure in gestation and breastfeeding affects Calomys laucha sperm cells. Environ Sci Pollut Res 26, 34953–34963 (2019). https://doi.org/10.1007/s11356-019-06577-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-019-06577-x