Do cypermethrin and fenvalerate disturb the function of the bovine cervix in vitro?

in Journal of Endocrinology
View More View Less
  • 1 Institute of Animal Reproduction and Food Research, Polish Academy of Sciences, Olsztyn, Poland

Correspondence should be addressed to M H Wrobel: m.wrobel@pan.olsztyn.pl
Restricted access

This study aimed to investigate the effect of pyrethroid insecticides on the regulation of bovine cervical function. Cervical cells or strips obtained from cows during the periovulation period were treated with cypermethrin and fenvalerate (0.1–10 ng/mL). None of the pyrethroids exerted a cytotoxic effect, whereas only fenvalerate increased the cervical contraction force and mRNA expression of receptor of oxytocin and prostaglandin (PG) synthases. Both pyrethroids inhibited PG secretion and decreased the amount of diacylglycerol, which is the second messenger involved in oxytocin signal transmission, and fenvalerate decreased the myosin light-chain kinase level. These findings indicate that fenvalerate induces greater disruption of cervical function than cypermethrin.

 

Society for Endocrinology logo

Sept 2018 onwards Past Year Past 30 Days
Abstract Views 190 190 190
Full Text Views 8 8 8
PDF Downloads 11 11 11
  • Adelsbach TL & Tjeerdema RS 2003 Chemistry and fate of fenvalerate and esfenvalerate. Reviews of Environmental Contamination and Toxicology 176 137154. (https://doi.org/10.1007/978-1-4899-7283-5_3)

    • Search Google Scholar
    • Export Citation
  • Arrowsmith S & Wray S 2014 Oxytocin: its mechanism of action and receptor signalling in the myometrium. Journal of Neuroendocrinology 26 356369. (https://doi.org/10.1111/jne.12154)

    • Search Google Scholar
    • Export Citation
  • Badia E, Nicolas JC, Haiech J & Crastes de Paulet A 1986 Effect of steroid hormones on the regulation of uterine contractility. Pflugers Archiv 407 670676. (https://doi.org/10.1007/BF00582650)

    • Search Google Scholar
    • Export Citation
  • Bedi JS, Gill JPS, Aulakh RS & Kaur P 2015 Pesticide residues in bovine milk in Punjab, India: spatial variation and risk assessment to human health. Archives of Environmental Contamination and Toxicology 69 230240. (https://doi.org/10.1007/s00244-015-0163-6)

    • Search Google Scholar
    • Export Citation
  • Bekana M, Jonsson P & Kindahl H 1997 Bacterial isolates associated with retained fetal membranes and subsequent ovarian activity in cattle. Veterinary Record 140 232234. (https://doi.org/10.1136/vr.140.9.232)

    • Search Google Scholar
    • Export Citation
  • Bouwman H, Seereda B & Meinhadt HM 2006 Simultaneous presence of DDT and pyrethroid residues in human breast milk from malaria endemic area in South Africa. Environmental Pollution 144 902917. (https://doi.org/10.1016/j.envpol.2006.02.002)

    • Search Google Scholar
    • Export Citation
  • Bradford MM 1976 A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72 248254. (https://doi.org/10.1006/abio.1976.9999)

    • Search Google Scholar
    • Export Citation
  • Brander SM, Gabler MK, Fowler NL, Connon RE & Schlenk D 2016 Pyrethroid pesticides as endocrine disruptors: molecular mechanisms in vertebrates with a focus on fishes. Environmental Science and Technology 50 89778992. (https://doi.org/10.1021/acs.est.6b02253)

    • Search Google Scholar
    • Export Citation
  • Breeveld-Dwarkasing VNA 2002 The bovine cervix explored: the cow as a model for studies on functional changes in the uterine cervix.

  • Breeveld-Dwarkasing VNA, de Boer-Brouwer M, Möstl E, Soede NM, van der Weijden GC, Taverne MAM & van Dissel-Emiliani FMF 2002 Immunohistochemical distribution of oestrogen and progesterone receptors and tissue concentrations of oestrogens in the cervix of non-pregnant cows. Reproduction, Fertility and Development 140 487494.(https://doi.org/10.1071/rd02005)

    • Search Google Scholar
    • Export Citation
  • Chen X, Panuwet P, Hunter RE, Riederer AM, Bernoudy GC, Barr DB & Ryan PB 2014 Method for the quantification of current use and persistent pesticides in cow milk, human milk and baby formula using gas chromatography tandem mass spectrometry. Journal of Chromatography: B, Analytical Technologies in the Biomedical and Life Sciences 970 121130. (https://doi.org/10.1016/j.jchromb.2014.08.018)

    • Search Google Scholar
    • Export Citation
  • Conrad JT & Hoover P 1982 Variations in the mechanical behavior of the rabbit cervix with endocrine state and anatomic site. American Journal of Obstetrics and Gynecology 143 661666. (https://doi.org/10.1016/0002-9378(8290111-9)

    • Search Google Scholar
    • Export Citation
  • Du G, Shen O, Sun H, Fei J, Lu C, Song L, Xia Y, Wang S & Wang X 2010 Assessing hormone receptor activities of pyrethroid insecticides and their metabolites in reporter gene assays. Toxicological Sciences 116 5866. (https://doi.org/10.1093/toxsci/kfq120)

    • Search Google Scholar
    • Export Citation
  • Duchens M, Fredriksson G, Kindahl H & Aiumlamai S 1993 Effect of intracervical administration of a prostaglandin E2 gel in pregnant and non-pregnant heifers. Veterinary Record 133 546549. (https://doi.org/10.1136/vr.133.22.546)

    • Search Google Scholar
    • Export Citation
  • Fields MJ & Fields PA 1996 Morphological characteristics of the bovine corpus luteum during the oestrous cycle and pregnancy. Theriogenology 45 12951325. (https://doi.org/10.1016/0093-691x(9600099-4)

    • Search Google Scholar
    • Export Citation
  • Firestone GL & Kapadia BJ 2012 Minireview: regulation of gap junction dynamics by nuclear hormone receptors and their ligands. Molecular Endocrinology 26 17981807. (https://doi.org/10.1210/me.2012-1065)

    • Search Google Scholar
    • Export Citation
  • Forgue MF, Pipy B, Beraud M, Souqual MC & Combis JM 1990 1-Naphthyl N-methyl carbamate effect on intra- and extracellular concentrations of arachidonic acid metabolites, and on the chemiluminescence generation by mouse peritoneal macrophages. International Journal of Immunopharmacology 12 155163. (https://doi.org/10.1016/0192-0561(9090049-s)

    • Search Google Scholar
    • Export Citation
  • Fuchs AR, Ivell R, Fields PA, Chang SM & Fields MJ 1996 Oxytocin receptors in bovine cervix: distribution and gene expression during the estrous cycle. Biology of Reproduction 54 700708. (https://doi.org/10.1095/biolreprod54.3.700)

    • Search Google Scholar
    • Export Citation
  • Gao X, Yu L, Castro L, Moore AB, Hermon T, Bortner C, Sifre M & Dixon D 2010 An endocrine-disrupting chemical, fenvalerate, induces cell cycle progression and collagen type I expression in human uterine leiomyoma and myometrial cells. Toxicology Letters 196 133141. (https://doi.org/10.1016/j.toxlet.2010.03.004)

    • Search Google Scholar
    • Export Citation
  • Gimpl G & Fahrenholz F 2001 The oxytocin receptor system: structure, function, and regulation. Physiological Reviews 81 629683. (https://doi.org/10.1152/physrev.2001.81.2.629)

    • Search Google Scholar
    • Export Citation
  • Goff AK 2004 Steroid hormone modulation of prostaglandin secretion in the ruminant endometrium during the estrous cycle. Biology of Reproduction 71 1116. (https://doi.org/10.1095/biolreprod.103.025890)

    • Search Google Scholar
    • Export Citation
  • Hirsbrunner G, Reist M, Keller C & Steiner A 2003 An in vitro study on spontaneous cervical contractility in the cow during oestrus and diestrus. Journal of Veterinary Medicine Series A 50 442446. (https://doi.org/10.1046/j.1439-0442.2003.00583.x)

    • Search Google Scholar
    • Export Citation
  • Hollingsworth M 1974 The innervation of the rat cervix and its pharmacology in vitro and in vivo. British Journal of Pharmacology 52 539547. (https://doi.org/10.1111/j.1476-5381.1974.tb09722.x)

    • Search Google Scholar
    • Export Citation
  • Kim IY, Shin JH, Kim HS, Lee SJ, Kang IH, Kim TS, Moon HJ, Choi KS, Moon A & Han SY 2004 Assessing estrogenic activity of pyrethroid insecticides using in vitro combination assays. Journal of Reproduction and Development 50 245255. (https://doi.org/10.1262/jrd.50.245)

    • Search Google Scholar
    • Export Citation
  • Kim CW, Go RE & Choi KC 2015 Treatment of BG-1 ovarian cancer cells expressing estrogen receptors with Lambda-cyhalothrin and cypermethrin caused a partial estrogenicity via an estrogen receptor-dependent pathway. Toxicological Research 31 331337. (https://doi.org/10.5487/TR.2015.31.4.331)

    • Search Google Scholar
    • Export Citation
  • Kugathas S, Audouze K, Ermler S, Orton F, Rosivatz E, Scholze M & Kortenkamp A 2016 Effects of common pesticides on prostaglandin D2 (PGD2) inhibition in SC5 mouse sertoli cells, evidence of binding at the COX-2 active site, and implications for endocrine disruption. Environmental Health Perspectives 124 452459. (https://doi.org/10.1289/ehp.1409544)

    • Search Google Scholar
    • Export Citation
  • Laskowski DA 2002 Physical and chemical properties of pyrethroids. Reviews of Environmental Contamination and Toxicology 174 49170. (https://doi.org/10.1007/978-1-4757-4260-2_3)

    • Search Google Scholar
    • Export Citation
  • Leemans M, Couderq S, Demeneix B & Fini JB 2019 Pesticides with potential thyroid hormone-disrupting effects: a review of recent data. Frontiers in Endocrinology 10 743. (https://doi.org/10.3389/fendo.2019.00743)

    • Search Google Scholar
    • Export Citation
  • Marettova E, Maretta M & Legáth J 2017 Effect of pyrethroids on female genital system. Review. Animal Reproduction Science 184 132138. (https://doi.org/10.1016/j.anireprosci.2017.07.007)

    • Search Google Scholar
    • Export Citation
  • Martyn F, McAuliffe FM & Wingfield M 2014 The role of the cervix in fertility: is it time for a reappraisal? Human Reproduction 29 20922098. (https://doi.org/10.1093/humrep/deu195)

    • Search Google Scholar
    • Export Citation
  • Minamoto T, Arai K, Hirakawa S & Nagai Y 1987 Immunohistochemical studies on collagen types in the uterine cervix in pregnant and nonpregnant states. American Journal of Obstetrics and Gynecology 156 138144. (https://doi.org/10.1016/0002-9378(8790225-0)

    • Search Google Scholar
    • Export Citation
  • Najak Z, Hillier K & Karim SM 1970 The action of prostaglandins of the human isolated non-pregnant cervix. Journal of Obstetric and Gynecology of the British Commonwealth 77 701709. (https://doi.org/10.1111/j.1471-0528.1970.tb03595.x)

    • Search Google Scholar
    • Export Citation
  • Pajntar M & Verdenik I 1995 Electromyographic activity in cervices with very low bishop score during labor. International Journal of Gynaecology and Obstetrics 49 277281. (https://doi.org/10.1016/0020-7292(9502374-l)

    • Search Google Scholar
    • Export Citation
  • Petr J, Chmelíková E, Zalmanová T, Tůmová L, Kheilová K, Kučerová-Chrpová V & Jílek F 2013 Pyrethroids cypermethrin, deltamethrin and fenvalerate have different effects on in vitro maturation of pig oocytes at different stages of growth. Animal 7 134142. (https://doi.org/10.1017/S1751731112001140)

    • Search Google Scholar
    • Export Citation
  • Rekawiecki R, Nowocin A & Kotwica J 2010 Relationship between concentrations of progesterone, oxytocin, noradrenaline, gene expression and protein level for their receptors in corpus luteum during estrous cycle in the cow. Prostaglandins and Other Lipid Mediators 92 1318. (https://doi.org/10.1016/j.prostaglandins.2010.01.002)

    • Search Google Scholar
    • Export Citation
  • Rekawiecki R, Kowalik MK & Kotwica J 2013 Validation of housekeeping genes for studying differential gene expression in the bovine myometrium. Acta Veterinaria Hungarica 61 505516. (https://doi.org/10.1556/AVet.2013.037)

    • Search Google Scholar
    • Export Citation
  • Sagsoz H, Akbalik ME, Saruhan BG & Ketani MA 2011 Localization of estrogen receptor α and progesterone receptor B in bovine cervix and vagina during the follicular and luteal phases of the sexual cycle. Biotechnic and Histochemistry 86 262271. (https://doi.org/10.3109/10520291003795861)

    • Search Google Scholar
    • Export Citation
  • Sassine A, Moura S, Léo VM & Bustillos OV 2004 Cypermethrin residuesdetermination in the milk of lactating dairycows by gas chromatography-ion trapmass spectrometry. Journal of Analytical Toxicology 28 238241. (https://doi.org/10.1093/jat/28.4.238)

    • Search Google Scholar
    • Export Citation
  • Shan G, Wengatz I, Stoutamire DW, Gee SJ & Hammock BD 1999 An enzyme-linked immunosorbent assay for the detection of esfenvalerate metabolites in human urine. Chemical Research in Toxicology 12 10331041. (https://doi.org/10.1021/tx990091h)

    • Search Google Scholar
    • Export Citation
  • Simaremare SRS, Hung CC, Hsieh CJ & Yiin LM 2019 Relationship between organophosphate and pyrethroid insecticides in blood and their metabolites in urine: a pilot study. International Journal of Environmental Research and Public Health 17 34. (https://doi.org/10.3390/ijerph17010034)

    • Search Google Scholar
    • Export Citation
  • Skarzynski DJ, Bogacki M & Kotwica J 1999 Involvement of ovarian steroids in basal and oxytocin-stimulated prostaglandin (PG) F2α secretion by the bovine endometrium in vitro. Theriogenology 52 385397. (https://doi.org/10.1016/S0093-691X(9900137-5)

    • Search Google Scholar
    • Export Citation
  • Slonina D, Kowalik MK, Subocz M & Kotwica J 2009 The effect of ovarian steroids on oxytocin-stimulated secretion and synthesis of prostaglandins in bovine myometrial cells. Prostaglandins and Other Lipid Mediators 90 6975. (https://doi.org/10.1016/j.prostaglandins.2009.08.006)

    • Search Google Scholar
    • Export Citation
  • Taylor SC, Berkelman T, Yadav G & Hammond MA 2013 A defined methodology for reliable quantification of western blot data. Molecular Biotechnology 55 217226. (https://doi.org/10.1007/s12033-013-9672-6)

    • Search Google Scholar
    • Export Citation
  • van Engelen E, Taverne MA, Everts ME, Van der Weijden GC, Doornenbal A & Breeveld-Dwarkasing VN 2007 EMB activity of the muscular and stromal layer of the cervix in relation to EMG activity of the myometrium and cervical dilatation in PGF2α induced parturition in the cow. Theriogenology 67 11581167. (https://doi.org/10.1016/j.theriogenology.2007.01.005)

    • Search Google Scholar
    • Export Citation
  • Vesanen M 1993 Bovine uterine, cervical and ovarian cytosol estrogen and progesterone receptor concentrations in cystic ovarian disease. Acta Veterinaria Scandinavica 34 3543. (https://doi.org/10.1186/BF03548221)

    • Search Google Scholar
    • Export Citation
  • Vink J & Feltovich H 2016 Cervical etiology of spontaneous preterm birth. Seminars in Fetal and Neonatal Medicine 21 106112. (https://doi.org/10.1016/j.siny.2015.12.009)

    • Search Google Scholar
    • Export Citation
  • Wrobel MH 2018 Do chlorinated insecticides (aldrin and DDT) or products of their transformations (dieldrin and DDE) impair signal transfer from regulators (oxytocin and relaxin) of bovine myometrium motility in vitro? Environmental Research 167 234239. (https://doi.org/10.1016/j.envres.2018.07.027)

    • Search Google Scholar
    • Export Citation
  • Wrobel MH & Mlynarczuk J 2017 Secretory function of ovarian cells and myometrial contractions in cow are affected by chlorinated insecticides (chlordane, heptachlor, mirex) in vitro. Toxicology and Applied Pharmacology 314 6371. (https://doi.org/10.1016/j.taap.2016.11.011)

    • Search Google Scholar
    • Export Citation
  • Wrobel MH, Rekawiecki R & Kotwica J 2009 Involvement of prostaglandin F2α in the adverse effect of PCB 77 on the force of contractions of bovine myometrium. Toxicology 262 224229. (https://doi.org/10.1016/j.tox.2009.06.012)

    • Search Google Scholar
    • Export Citation
  • Wrobel MH, Mlynarczuk J & Kotwica J 2012 The effect of DDT and its metabolite (DDE) on prostaglandin secretion from epithelial cells and on contractions of the smooth muscle of the bovine oviduct in vitro. Toxicology and Applied Pharmacology 259 152159. (https://doi.org/10.1016/j.taap.2011.12.019)

    • Search Google Scholar
    • Export Citation
  • Wrobel MH, Bedziechowski P, Mlynarczuk J & Kotwica J 2014 Impairment of uterine smooth muscle contractions and prostaglandin secretion from cattle myometrium and corpus luteum in vitro is influenced by DDT, DDE and HCH. Environmental Research 132 5461. (https://doi.org/10.1016/j.envres.2014.02.018)

    • Search Google Scholar
    • Export Citation
  • Zhao S & Fernald RD 2005 Comprehensive algorithm for quantitative real-time polymerase chain reaction. Journal of Computational Biology 12 10471064. (https://doi.org/10.1089/cmb.2005.12.1047)

    • Search Google Scholar
    • Export Citation
  • Zhong M, Murtazina DA, Phillips J, Ku CY & Sanborn BM 2008 Multiple signals regulate phospholipase CBeta3 in human myometrial cells. Biology of Reproduction 78 10071017. (https://doi.org/10.1095/biolreprod.107.064485)

    • Search Google Scholar
    • Export Citation