In vitro Interference of a Glyphosate Commercial Formulation with the Stimulation of Ovarian Maturation by Progesterone, in the Estuarine Crab Neohelice granulata

Abstract

This study was aimed at evaluating the possible interference of formulated glyphosate to the endocrine control of ovarian growth exerted by progesterone, in the estuarine crab Neohelice granulata. The addition of Roundup Ultramax® (0.2 mg/L of glyphosate in the incubation medium) was able to potentiate the stimulating effect of progesterone on total vitellogenic protein (Vg) content of ovarian pieces from crabs. Moreover, the sole addition of mifepristone (antagonist of progesterone receptors) was able to produce a decrement of the Vg content, which was not reverted by the addition of Roundup. A similar result was confirmed by means of histological analysis, which showed that mifepristone, both alone and in combination with Roundup, inhibited ovarian maturation, while Roundup alone increased it, in terms of a higher proportion of vitellogenic oocytes. We conclude that Roundup could stimulate the progesterone secretion exerted by the ovary and/or could act as a partial agonist of this hormone in the same tissue.

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References

  1. Aparicio VC, De Gerónimo E, Marino D, Primost J, Carriquiriborde P, Costa JL (2013) Environmental fate of glyphosate and aminomethylphosphonic acid in surface waters and soil of agricultural basins. Chemosphere 93:1866–1873

    CAS  Article  Google Scholar 

  2. Armiliato N, Ammar D, Nezzi L, Straliotto M, Muller YMR, Nazari EM (2014) Changes in ultrastructure and expression of steroidogenic factor-1 in ovaries of zebrafish Danio rerio exposed to glyphosate. J Toxicol Environ Health 77A:405–414

    Article  Google Scholar 

  3. Avigliano L, Álvarez NB, Mac Loughlin C, Rodríguez EM (2014) Effects of glyphosate on egg incubation, larvae hatching and ovarian re-maturation, in the estuarine crab Neohelice granulata. Environ Toxicol Chem 33:1879–1884

    CAS  Article  Google Scholar 

  4. Canosa IS (2019) Interferencia del herbicida glifosato sobre el control endocrino de la reproducción, en el cangrejo de estuario Neohelice granulata (Decapoda, Brachyura). PhD Thesis, University of Buenos Aires, p 232

  5. Canosa IS, Silveyra GR, Avigliano L, Medesani DA, Rodríguez EM (2018) Ovarian growth impairment after chronic exposure to Roundup Ultramax®, in the estuarine crab Neohelice granulata. Environ Sci Pollut Res 25:1568–1575

    CAS  Article  Google Scholar 

  6. Cooke IM, Haylett BA, Weatherby TM (1977) Electrically elicited neurosecretory and electrical responses of the isolated crab sinus gland in normal and reduced calcium salines. J Exp Biol 101:125–149

  7. Ferré LE, Medesani DA, Grodzielski M, García CF, Rodríguez EM (2012) Vitellogenin levels in hemolymph, ovary and hepatopancreas of the freshwater crayfish Cherax quadricarinatus, during the reproductive cycle. Int J Trop Biol 60:253–261

  8. Gasnier C, Dumont C, Benachour N, Clair E, Chagnon MC, Séralini GE (2009) Glyphosate-based herbicides are toxic and endocrine disruptors in human cell lines. Toxicology 262:184–191

    CAS  Article  Google Scholar 

  9. Giesy JP, Dobson S, Solomon KR (2000) Ecotoxicological risk assessment for roundup herbicide. Rev Environ Contam Toxicol 167:35–120

    CAS  Google Scholar 

  10. Lee RF, Walker A (1995) Lipovitelin and and lipid droplet accumulation in oocytes during ovarian maturation in the blue crab, Callinectes sapidus. J Exp Zool 271:401–412

    CAS  Article  Google Scholar 

  11. Leguizamón A (2014) Modifying Argentina: GM soy and socioenvironmental change. Geoforum 53:149–160

  12. Matozzo V, Fabrello J, Marin MG (2020) The effects of glyphosate and its commercial formulations to marine invertebrates: a review. J Mar Sci Eng 8:399

    Article  Google Scholar 

  13. Medesani DA, Ferré LE, Canosa IS, Silveyra GR, Rodríguez EM (2015) Induction of vitellogenesis by 17-hydroxyprogesterone and methyl farnesoate during post-reproductive period, in the estuarine crab Neohelice granulata. Invertebr Reprod Dev 59:104–110

  14. Merlin J, Mohanlal DL, Balasubramanian CP, Sherly T, Subramoniam T, Syamadayal J, Ravichandran P, Ponniah AG, Gopal C, Vijayan KK (2015) Induction of vitellogenesis and reproductive maturation in tiger shrimp, Penaeus monodon by 17ß-estradiol and 17α-hydroxyprogesterone: in vivo and in vitro studies. Invertebr Reprod Dev 59:166–175

    CAS  Article  Google Scholar 

  15. Mesnage R, Defarge N, Spiroux de Vendômois J, Seralini GE (2015) Potential toxic effects of glyphosate and its commercial formulations below regulatory limits. Food Chem Toxicol 84:133–153

    CAS  Article  Google Scholar 

  16. Meunpol O, Iam-Pai S, Suthikrai W, Piyatiratitivorakul S (2007) Identification of progesterone and 17α-hydroxyprogesterone in polychaetes (Perinereis sp.) and the effects of hormone extracts on penaeid oocyte development in vitro. Aquaculture 270:485–492

    CAS  Article  Google Scholar 

  17. Paolucci M, Di Cristo C, Di Cosmo A (2002) Immunological evidence for progesterone and estradiol receptors in the freshwater crayfish Austropotamobius pallipes. Mol Reprod Dev 63:55–62

    CAS  Article  Google Scholar 

  18. Peruzzo PJ, Porta AA, Ronco AE (2008) Levels of glyphosate in surface waters, sediments and soil associated with direct sowing soybean cultivation in north pampasic region of Argentina. Environ Pollut 156:61–66

    CAS  Article  Google Scholar 

  19. Preechaphol R, Klinbunga S, Ponza P, Menasveta P (2010) Isolation and characterization of progesterone receptor-related protein p23 (Pm-p23) differentially expressed during ovarian development of the giant tiger shrimp Penaeus monodon. Aquaculture 308:75–82

    Article  Google Scholar 

  20. Quackenbush LS (1994) Lobster reproduction: a review. Crustaceana 67:82–94

    Article  Google Scholar 

  21. Reddy Buchi S, Vaadala S, Hosamani N, Reddy Pamuru R, Reddy PS (2016) Regulation of vitellogenesis by selected endocrine modulators in crab Oziothelphusa senex senex, with special reference to methyl farnesoate. Aquacult Rep 3:24–30

    Article  Google Scholar 

  22. Rodriguez EM, Medesani DA, Lopez Greco LS, Fingerman M (2002) Effects of some steroids and other compounds on ovarian growth of the red swamp crayfish, Procambarus clarkii, during early vitellogenesis. J Exp Zool 292:82–87

    CAS  Article  Google Scholar 

  23. Shih JT, Liao CF (1998) Conversion of cholesterol to sex steroid-like substances by tissues of Mictyris brevidactylus in vitro. Zool Stud 37:102–110

    CAS  Google Scholar 

  24. Silveyra GR, Canosa IS, Rodríguez EM, Medesani DA (2017) Effects of atrazine on ovarian growth, in the estuarine crab Neohelice granulata. Comp Biochem Physiol 192C:1–6

  25. Subramoniam T (2017) Steroidal control of vitellogenesis in Crustacea: a new understanding for improving shrimp hatchery production. Proc Indian Natl Sci Acad 83:595–610

    Google Scholar 

  26. Thongbuakaew Y, Siangcham T, Suwansa-ard S, Elizur A, Cummins SF, Sobhon P, Sretarugsa P (2016) Steroids and genes related to steroid biosynthesis in the female giant freshwater prawn, Macrobrachium rosenbergii. Steroids 107:149–160

    CAS  Article  Google Scholar 

  27. Wrobel MH (2018) Glyphosate affects the secretion of regulators of uterine contractions in cows while it does not directly impair the motoric function of myometrium in vitro. Toxicol Appl Pharmacol 349:55–61

    CAS  Article  Google Scholar 

  28. Ye H, Huang H, Song P (2010) The identification and distribution of progesterone receptors in the brain and thoracic ganglion in the mud crab Scylla paramamosain (Crustacea: Decapoda: Brachyura). Invert Neurosci 10:1–16

    Article  Google Scholar 

  29. Zapata V, López Greco LS, Medesani DA, Rodríguez EM (2003) Ovarian growth in the crab Chasmagnathus granulata, induced by hormones and neuroregulators throughout the year. In vivo and in vitro studies. Aquaculture 224:339–352

    CAS  Article  Google Scholar 

  30. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York

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Acknowledgements

This work was supported by Grants from ANPCYT (PICT 2016-0040), UBACYT 2020 (code 20020190100014BA), and CONICET (PIP 2015, code 11220150100100CO)

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Correspondence to Enrique M. Rodríguez.

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Canosa, I.S., Silveyra, G.R., Lonné, M.N. et al. In vitro Interference of a Glyphosate Commercial Formulation with the Stimulation of Ovarian Maturation by Progesterone, in the Estuarine Crab Neohelice granulata. Bull Environ Contam Toxicol (2021). https://doi.org/10.1007/s00128-021-03107-9

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Keywords

  • Glyphosate
  • Estuarine crabs
  • Ovarian growth
  • Vitellogenic proteins
  • Progesterone