Movento influences development of granulosa cells and ovarian follicles and FoxO1 and Vnn1 gene expression in BALB/c mice

Document Type : Original Article

Authors

1 Department of Biology, Science and Research Branch, Islamic Azad University, Tehran, Iran

2 Department of Biology, Research Center for Applied Biology, Mashhad Branch, Islamic Azad University, Mashhad, Iran

3 Medical Genetics Research Center, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran

4 Department of Medical Genetics, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran

Abstract

Objective(s): Pesticides has wide range of infertility in female reproductive. This study was done to evaluate the effect of movento pesticide on development of granulosa cells and ovarian follicles and FoxO1 and Vnn1 gene expression in BALB/c mice.
Materials and Methods: In this study 40 healthy BALB/c mice 5-6 weeks age were used. Animals were randomly allocated into four groups. Control (without any intervention), three experimental groups received 25, 50 and 100 mg/kg movento dissolved in PBS by gavage for 21 days. Animals scarified after three weeks. For determining the effects of movento on granulosa cells in culture, treatments were conducted to movento (125, 250, 500 μg/ml) for 24 hr. We surveyed the expression of the FoxO1 and Vnn1 in granulosa cells in vitro, and its relation to cell death by flowcytometer and DAPI. Levels of FoxO1 and Vnn1 were analyzed by real-time PCR.
Results: Exposure to movento significantly decreased ovarian weight and the number of primary, secondary and antral follicles. Further, treatment with different concentration of movento induced apoptosis on granulosa cells. Gene expression analysis showed the transcriptional expression of FoxO1 and vnn1 in granulosa cells. Level of Vnn1 mRNA in granulosa cells was decreased in granulosa cells and expression of FoxO1 significantly increased in treated groups in compare to controls (P-value <0.05).
Conclusion: Exposure to movento significantly reduced the number of follicles and increased apoptosis of granulosa cells leading disruption of the reproductive system. Also movento reduced expression of Vnn1 and increased FoxO1 genes in a dose dependent manner.

Keywords


1. Gupta RK, Miller KP, BabusJK, Flaws JA. Methoxychlor inhibits growth and induces atresia of antral follicles through an oxidative stress pathway. Toxicol Sci 2006; 93:382–389.
2. Mokhtar HI, Abdel HA, Elmazoudy RH, Abdelwahab WM, Saad MI. Effect of methomyl on fertility, embryotoxicity and physiological parameters in female rats. J App Pharm Sci 2013; 3:109-119.
3. Saleh  AMT, Hijji AM, Elel SJ, Al Yacoub AN.  Effect of carbamate insecticide, Lannate, on the gonads of mice.  J Adv. Lab. Res. Biol 2014; 5:140-145.
4. Sargazi Z, Nikravesh MR, Jalali M, Sadeghnia HR, RahimiAnbarkeh F, Mohammadzadeh L. Gender-related differences in sensitivity to diazinonin gonads of adult rats and the protective effect of vitamin E. IJWHR Sci 2015; 3:40–47.
5. Sharma D, Sangha GK, Khera KS. Triazophos-induced oxidative stress and histomorphological changes in ovary of female wistar rats. pestic Biochem physiol 2015; 117:9-18.
6. Sverdrup LE, Bjorge C,  Eklo OM, Grung M, Kallqvist T, Klingen I, et al. Risk assessment of the insecticide Movento 100 SC with the active substance spirotetramat. Bayer Crop Sci 2012; 13: 1-25.
7. Etchechury FM, Gramont S, Sanchez R, Romero C, Enriquez R, Cervantes L, et al. Spirotetramat induces histological and biochemical changes in wistar rats. Rev Toxicol 2015; 30:215-217.
8. Roffeni S, Arangeli G, Boebel A, Gollo M, Gualco A, Venturini V, et al. Spirotetramat (MOVENTO®): A novel systemic insecticide to control main harmful sucking pests of cultivated crops. ATTI Giornate Fitopatolo 2010; 1:3-10.
9. Marcic D, Mutavdzic S, Medjo I, Prijovic M, Peric P. Spirotetramat toxicity to immatures and sublethal effects on fecundity of female adults of Tetranychus urticae Koch. J Zoosymposia 2011; 6:99–103.
10. Bruck E, Elbert A, Fischer R, Krueger S, Kuhnhold J, KluekenAM, et al. Movento®, an innovative ambimobile insecticide for sucking insect pest control in agriculture: Biological profile and field performance. Crop prot 2009; 10:838-844.
11. Martin F, Malergue F, Pitari G, Philippe JM, Philips S, Chabret C, et al. Vanin genes are clustered (human 6q22–24 and mouse 10A2B1) and encode isoforms of pantetheinase ectoenzymes. Immunogenetics 2001; 53: 296–306.
12. Barthel A, Schmoll D, Unterman TG. FoxO proteins in insulin action and metabolism. Trends Endocrinol Metab 2005;16:183–189.
13. Accili D, Arden KC. FoxOs at the crossroads of cellular metabolism, differentiation, and transformation. Cell 2004; 117:421–426.
14. Greer EL, Brunet A. FOXO transcription factors at the interface between longevity and tumor suppression. Oncogene 2005; 24:7410–7425.
15. Huang H, Tindall DJ. Dynamic FoxO transcription factors. J Cell Sci 2007; 120: 2479–2487.
16. Kaur P, Guraya SS. Follicular growth and kinetics during the estrous cycle, pregnancy and postpartum in the Indian mole rat (Bandicota bengalensis). Am J Anat 1983; 166:469–482.
17. Armenti AME, Mahakali ZA, Passantino L, Uzumcu M. Developmental methoxychlor exposure affects multiple reproductive parameters and ovarian: folliculogenesis and gene expression in adult rats. Toxicol Appl Pharmacol 2008; 233: 286–296.
18. Saleh AMT, Hijji AM, Elel SJ, Al Yacoub AN.  Effect of carbamate insecticide, lannate, on the gonads of mice. J Adv. Lab. Res. Biol 2014; 140-145.
19. El-Sayyad HI. Histological effects of thiosicarb on the reproductive system of the adult female mouse. J Egypt Germ. Soc. Zool 1994; 13: 47-65.
20. Matter FE, Farid NM, Rageb AF. A histochemical study on the ovaries of rat treated with an insecticide. "Carbaryl". Egypt J Histol 2000; 4:87-92.
21. Bhardwaj JK, Saraf P. Malathion-induced granulosa cell apoptosis in caprine nntral follicles: an ultrastructural and flow cytometric analysis. Microsc Microanal 2014; 20: 1861-1868.
22. Wojtowicz  AK, Gregoraszczuk EL, Ptak A, Falandysz J. Effect of single and repeated in vitro exposure of ovarian follicles to o,p'-DDT and p,p'-DDT and their metabolites. Pol J Pharmacol 2004; 56:465-472.
23. Rocket JC, Narotsky  MG, Thomson KE, Thilladarajah I, Blystone CB, Goetza A, et al. Effect of conozole fungicides on reproductive development in female rats. J Reprod Toxicol 2006; 22: 647-648.
24. Carbone  MC, Tatone C, Delle MS, Marci R, Caserta D, Colonna R, et al. Antioxidant enzymatic defenses in human follicular fluid: Characterization and agedependent changes. Mol Hum Reprod 2003; 9: 639-643.
25. Li HJ, Liu DJ, Cang M, Wang LM, Jin MZ, Ma YZ, Shorgan B. Early apoptosis is associated with improved developmental potential in bovine oocytes. Anim Reprod Sci 2009; 114:89–98.
26. Bunel A, Nivet A, Blondin P, Vigneault C, Richard F, Sirard M. Cumulus cell gene expression associated with pre-ovulatory acquisition of developmental competence in bovine oocytes. Reprod Fertil Dev 2014; 26:855–865.
27. Nivet AL, Vigneault C, Blondin P, Sirard MA. Changes in granulosa cells' gene expression associated with increased oocyte competence in bovine. Reproduction 2013; 145:555–565.
28. Grimmond S, Van Hateren N, Siggers P, Arkell R, Larder R, Soares MB, et al. Sexually dimorphic expression of protease nexin-1 and vanin-1 in the developing mouse gonad prior to overt differentiation suggests a role in mammalian sexual development. Hum Mol Genet 2000; 12:1553-1560.
29. Berruyer C, Martin FM, Castellano R, Macone A, MalergueF,Garrido-Urbani S, et al. Vanin-1K/K mice exhibit a glutathione-mediated tissue resistanceto oxidative stress. Mol Cell Biol 2004; 24: 7214–7224.
30. Girard A, Dufort I, Douville G, Sirard MA. Global gene expression in granulosa cells of growing, plateau and atretic dominant follicles in cattle. J Reprod Biol Endocrinol 2015; 13:1-15.
31. Megan JW, Jeyasuria P, Keith LP, KoopmanP. The transcription factors steroidogenic factor-1 and SOX9 regulate expression of Vanin-1 during mouse testis development. J Biol chem 2005; 18: 5917–5923.
32. Matsuda F, Inoue N, Maeda A, Cheng Y, Sai T, Gonda H, et al. Expression and function of apoptosis initiator FOXO3 in granulosa cells during follicular atresia in pig ovaries. J Reprod Dev 2011; 57:151-158.
33. Shen M, Lin F, Zhang J, Tang Y, Chen WK, Liu H. Involvement of the up-regulated FoxO1 expression in follicular granulosa cell apoptosis induced by oxidative stress. J Biol chem 2012; 31: 25727–25740.
34. Burgering BM, Medema RH. Decisions on life and death: FOXO forkhead transcription factors are in command when PKB/Akt is off duty. J Leukoc Biol 2003; 73:689–701.