Online ISSN: 3007-0244,
Print ISSN:  2410-4280
MORPHOLOGICAL CHARACTERISTICS of granuloSA cells of mice ovarian under lindane exposure
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Introduction. Analysis of materials that characterize the human environment in the Aral Sea, has shown a sharp increase of the chemical (pesticides, fertilizers, salt components, heavy metals) pollution of drinking water, air, soil, pesticide contamination of food products of plant and animal origin, fishery products.

Aim. Еvaluate the ultrastructural changes in granulosa cells of mice under the exposure of lindane pesticide in vitro.

Methods. The experimental work carried out in the Laboratory Centre of Microscopy Department of Life, Health and Environmental Sciences University L’Aquila, Italy; 80 female mice control (10), control with solution of dimethyl sulfoxide (10), lindane 1 μM (20), lindane 10 μM (20), lindane 100 μM (20). The material of the study were ovarian granulosa cells. After preparing the samples for transmission electron microscopy, ultra-thin sections (60-80 nm) were obtained on an ultramicrotome and contrasted with salts of heavy metals with uranyl acetate and lead citrate (Sic Rome, Italy).

Results. Comparative analysis of the group showed the dependence of ultrastructural changes in the applied lindane concentration.The presence of irregularly shaped cells were observed early signs of fragmentation of the cytoplasm, which was filled with a plurality of mitochondria and fatty droplets. In the group with the highest concentration of toxicant cells appeared marginalization of chromatin remnants of apoptotic bodies and single organelles.

Conclusion. The exposure of lindane in vitro have shown a dose-dependent toxicity effect on the granulosa cells; ultrastructural changes caused granulosa cells strictly correlated on the applied dose.

Aru D. Balmagambetova ¹, http://org/0000-0003-1151-5651

Gulmira A. Zhurabekova ¹, http://orcid.org/0000-0002-2166-3095

Guido Macchiarelli ², http://orcid.org/0000-0003-1040-5338

Maria Grazia Palmerini ², http://orcid.org/0000-0003-3171-5888

Stefania Anarita Nottola ³, http://orcid.org/0000-0003-1829-5989

 

¹ West Kazakhstan State Medical University n.a. M. Ospanov, Department of Normal and Topographical anatomy, Department of Life, Health and Environmental Sciences and Center of Electron Microscopies, Aktobe, Kazakhstan;

² University of L’Aquila, Department of Anatomy, Histology, Forensic Medicine and Orthopaedics, Laboratory of Electron Microscopy n.a. Pietro M. Motta, L’Aquila, Italy;

³ University La Sapienza, Rome, Italy

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6.         Ackert C. L., Gittens J. E., O’Brien M. J., Eppig J. J., Kidder G. M. Intercellular communication via connexin 43 gap junctions is required for ovarian folliculogenesis in the mouse // Dev Biol. 2001. 233. P. 258-270.

7.         Akhilesh K. C. et all. Engineering bacteria for bioremediation of persistent organochlorine pesticide lindane (gamma-hexachlorocyclohexane) // Bioresource Technology. 2013. 149. P. 439–445.

8.         Alm H., Tiemann U., Torner H. Influence of organochlorine pesticides on development of mouse embryos in vitro // Reproductive Toxicology. 1996. 10. P. 321-326.

9.         Alm H., Torner H., Tiemann U., Kanitz W. Influence of organochlorine pesticides on maturation and postfertilization development of bovine oocytes in vitro // Reproductive Toxicology. 1998. 12. P. 559-563.

10.     Cecconi S., Rossi G., Coticchio G., Macchiarelli G., Borini A., Canipari R. Influence of thyroid hormone on mouse preantral follicle development in vitro // Fertil Steril. 2004. 81. P. 919–24.

11.     Cecconi S., Rossi G. Mouse antral oocytes regulate preantral granulosa cell ability to stimulate oocyte growth in vitro // Developmental Biology. 2001. 233. P. 186 –191.

12.     Cecconi S. et al. Akt expression in mouse oocytes matured in vivo and in vitro // Reproductive BioMedicine Online. 2010. 20. P. 35–41.

13.     Campagna C., Sirard M. A., Ayotte P., Bailey J. L. Impaired maturation, fertilization, and embryonic development of porcine oocytes following exposure to an environmentally relevant organo- chlorine mixture // Biol Reprod. 2001. 65. P. 554–560.

14.     Devendra K. B., Mehajbeen B. Modulation of tricarboxylic acid cycle dehydrogenases during hepatocarcinogenesis induced by hexachlorocyclohexane in mice // Experimental and Toxicologic Pathology. 2009. 61. P. 325–332.

15.     Foster W., Chan S., Platt L., Hughes C. Detection of endocrine disrupting chemicals in samples of second trimester human amniotic fluid // The Journal of Clinical Endocrinology & Metabolism. 2000. 85. P. 2954-2955.

16.     Ke F-C., Fang S-H., Lee M-T., Sheu S-Y., Lai S-Y., Chen Y. J., Huang F-L., Wang P. S., Stocco D. M., Hwang J-J. Lindane, a gap junction blocker, suppresses FSH and transforming growth factor β1-induced connexin43 gap junction formation and steroidogenesis in rat granulosa cells // J. Endocrinol. 2005. 184. P. 555–566.

17.     Kuni O., Hashizume M., Chiba M., Sasaki S., Shimoda T., Caypil W., Dauletbaev D. Respiratory Symptoms and Pulmonary Function among School-Age Children in the Aral Sea Region // Archives of Environmental Health. November 2003. 11. Vol. 58.

18.     Jensen S., Mazhitova Z., Zetterstrom R. Environmental pollution and child health in the Aral Sea region in Kazakhstan // Sci Total Environ. 1997. 206. P. 187-93.

19.     Li R., Mather J. P. Lindane, an inhibitor of gap junction formation, abolishes oocyte directed follicle organizing activity in vitro // Endocrinology. 1997. 138. P. 4477-4480.

20.     Lindenau A., Fisher B., Seiler P., Beier H. M. Effects of persistent chlorinated hydrocarbons on reproductive tissues in female rabbits // Hum.Reprod. 1994. 9. P. 772-80.

21.     Maranghi F., Rescia M., Macri C., Di Consiglio E., De Angelis G., Testai E. et al. Lindane may modulate the female reproductive development through the interactionwith ER-beta:aninvivo–invitroapproach // Chem Biol Interact. 2007. 169. P. 1–14.

22.     Milagrosa O. et all. Lindane toxicity on early life stages of gilthead seabream (Sparus aurata) with a note on its histopathological manifestations // Environmental Toxicology and Pharmacology. 2008. 25. P. 94–102.

23.     Rasier G. et all. Female sexual maturation and reproduction after prepubertal exposure to estrogens and endocrine disrupting chemicals: A review of rodent and human data // Molecular and Cellular Endocrinology. 2006. 254–255. P. 187–201.

24.     Rossi G., Buccione R., Baldassarre M., Macchiarelli G., Palmerini M. G., Cecconi S. Mancozeb exposure in vivo impairs mouse oocyte fertiliz- ability // Reprod Toxicol. 2005.

25.     Padma V. V. et all. Protective effect of gallic acid against lindane induced toxicity in experimental rats // Food and Chemical Toxicology. 2011. 49. P. 991–998.

26.     Report on Carcinogens, Thirteenth Edition National Toxicology Program, Department of Health and Human Services For Table of Contents, see home page: http://ntp.niehs.nih.gov/go/roc13.

27.     Scascitelli M., Pacchierotti F. Effects of lindane on oocyte maturation and preimplantation embryonic development in the mouse // Reproductive Toxicology. 2003. 17. P. 299–303.

28.     Stephen A. S. Noise Effects on Health in the Context of Air Pollution Exposure // Int. J. Environ. Res. Public Health. 2015. 12. P. 12735-12760.

29.     Tiemann U., Pohland R. Inhibitory effects of organochlorine pesticides on intercellular transfer of Lucifer Yellow in cultured bovine oviductal cells // Reprod Toxicol. 1999. 13. P. 123–130.

30.     Tiemann U., Pohland R., Kuchenmeister U., Viergutz T. Influence of organochlorine pesticides on transmembrane potential, oxidative activity, and ATP-induced calcium release in cultured bovine oviductal cells // Reprod Toxicol. 1998.12. P. 551–557.

31.     Usman M. et all. Chemical oxidation of hexachlorocyclohexanes (HCHs) in contaminated soils // Science of the Total Environment. 2014. 476–477. 434–439.

32.     Zucchini N., de Sousa G., Bailly-Maitre B., Gugenheim J., Bars R., Lemaire G., Rah-mani R., Regulation of Bcl-2 and Bcl-xL anti-apoptotic protein expression by nuclear receptor PXR in primary cultures of human and rat hepatocytes // Biochim. Biophys. 2005. 1745. P.48 -58.

 

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6.         Ackert C. L., Gittens J. E., O’Brien M. J., Eppig J. J. and Kidder G. M. (2001) Intercellular communication via connexin43 gap junctions is required for ovarian folliculogenesis in the mouse. Dev Biol. 2001, 233, pp. 258-270.

7.         Akhilesh K. C. et all. Engineering bacteria for bioremediation of persistent organochlorine pesticide lindane (gamma-hexachlorocyclohexane). Bioresource Technology. 2013, 149, pp. 439–445.

8.         Alm H., Tiemann U., Torner H. Influence of organochlorine pesticides on development of mouse embryos in vitro. Reproductive Toxicology. 1996, 10, pp. 321-326.

9.         Alm H., Torner H., Tiemann U., Kanitz W. Influence of organochlorine pesticides on maturation and postfertilization development of bovine oocytes in vitro. Reproductive Toxicology. 1998, 12, pp. 559-563.

10.     Cecconi S., Rossi G., Coticchio G., Macchiarelli G., Borini A., Canipari R. Influence of thyroid hormone on mouse preantral follicle development in vitro. Fertil Steril. 2004, 81, pp. 919–24.

11.     Cecconi S., Rossi G. Mouse antral oocytes regulate preantral granulosa cell ability to stimulate oocyte growth in vitro. Developmental Biology. 2001, 233, pp. 186 –191.

12.     Cecconi S. et al. Akt expression in mouse oocytes matured in vivo and in vitro. Reproductive BioMedicine Online. 2010, 20, pp. 35–41.

13.     Campagna C., Sirard M. A., Ayotte P., Bailey J. L. Impaired maturation, fertilization, and embryonic development of porcine oocytes following exposure to an environmentally relevant organo- chlorine mixture. Biol Reprod. 2001, 65, pp. 554–560.

14.     Devendra K. B, Mehajbeen B. Modulation of tricarboxylic acid cycle dehydrogenases during hepatocarcinogenesis induced by hexachlorocyclohexane in mice. Experimental and Toxicologic Pathology. 2009, 61, pp. 325–332.

15.     Foster W., Chan S., Platt L., Hughes C. Detection of endocrine disrupting chemicals in samples of second trimester human amniotic fluid. The Journal of Clinical Endocrinology & Metabolism. 2000, 85, pp. 2954-2955.

16.     Ke F-C., Fang S-H., Lee M-T., Sheu S-Y., Lai S-Y., Chen Y. J., Huang F-L., Wang P. S., Stocco D. M., Hwang J-J. Lindane, a gap junction blocker, suppresses FSH and transforming growth factor β1-induced connexin43 gap junction formation and steroidogenesis in rat granulosa cells. J. Endocrinol. 2005, 184, pp. 555–566.

17.     Kuni O., Hashizume M., Chiba M., Sasaki S., Shimoda T., Caypil W., Dauletbaev D. Respiratory Symptoms and Pulmonary Function among School-Age Children in the Aral Sea Region. Archives of Environmental Health. November, 2003, 11, Vol. 58.

18.     Jensen S., Mazhitova Z., Zetterstrom R. Environmental pollution and child health in the Aral Sea region in Kazakhstan. Sci Total Environ. 1997, 206, pp. 187-93.

19.     Li R., Mather J. P. Lindane, an inhibitor of gap junction formation, abolishes oocyte directed follicle organizing activity in vitro. Endocrinology. 1997, 138, pp. 4477-4480.

20.     Lindenau A., Fisher B., Seiler P., Beier H. M. Effects of persistent chlorinated hydrocarbons on reproductive tissues in female rabbits. Hum.Reprod. 1994, 9, pp. 772-80.

21.     Maranghi F., Rescia M., Macri C., Di Consiglio E., De Angelis G., Testai E., et al. Lindane may modulate the female reproductive development through the interactionwith ER-beta:aninvivo–invitroapproach. Chem. Biol. Interact. 2007, 169. pp. 1–14.

22.     Milagrosa O. et all. Lindane toxicity on early life stages of gilthead seabream (Sparus aurata) with a note on its histopathological manifestations. Environmental Toxicology and Pharmacology. 2008, 25, pp. 94–102.

23.     Rasier G. et all. Female sexual maturation and reproduction after prepubertal exposure to estrogens and endocrine disrupting chemicals: A review of rodent and human data. Molecular and Cellular Endocrinology. 2006, 254–255, pp. 187–201.

24.     Rossi G., Buccione R., Baldassarre M., Macchiarelli G., Palmerini M. G., Cecconi S. Mancozeb exposure in vivo impairs mouse oocyte fertiliz- ability. Reprod Toxicol. 2005.

25.     Padma V. V. et all. Protective effect of gallic acid against lindane induced toxicity in experimental rats. Food and Chemical Toxicology. 2011, 49, pp. 991–998.

26.     Report on Carcinogens, Thirteenth Edition National Toxicology Program, Department of Health and Human Services For Table of Contents, see home page: http://ntp.niehs.nih.gov/go/roc13.

27.     Scascitelli M., Pacchierotti F. Effects of lindane on oocyte maturation and preimplantation embryonic development in the mouse. Reproductive Toxicology. 2003, 17, pp. 299–303.

28.     Stephen A. S. Noise Effects on Health in the Context of Air Pollution Exposure. Int. J. Environ. Res. Public Health. 2015, 12, pp. 12735-12760.

29.     Tiemann U., Pohland R. Inhibitory effects of organochlorine pesticides on intercellular transfer of Lucifer Yellow in cultured bovine oviductal cells. Reprod Toxicol. 1999, 13, pp. 123–130.

30.     Tiemann U., Pohland R., Kuchenmeister U., Viergutz T. Influence of organochlorine pesticides on transmembrane potential, oxidative activity, and ATP-induced calcium release in cultured bovine oviductal cells. Reprod Toxicol. 1998, 12, pp. 551–557.

31.     Usman M. et all. Chemical oxidation of hexachlorocyclohexanes (HCHs) in contaminated soils. Science of the Total Environment. 2014, 476–477, pp. 434–439.

32.     Zucchini N., de Sousa G., Bailly-Maitre B., Gugenheim J., Bars R., Lemaire G., Rah-mani R. Regulation of Bcl-2 and Bcl-xL anti-apoptotic protein expression by nuclear receptor PXR in primary cultures of human and rat hepatocytes. Biochim. Biophys. 2005, 1745, pp. 48 -58.

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Bibliography link

Балмагамбетова А. Д., Журабекова Г.А., Маккиарелли Г., Пальмерини М.Г., Ноттола С.А. Морфологическая характеристика гранулезных клеток яичников мышей при воздействии линдана / / Наука и Здравоохранение. 2016. №2. С. 106-117.

Balmagambetova A.D., Zhurabekova G.A., Macchiarelli G., Palmerini M.G., Nottola S.A. Morphological characteristics of granulosa cells of mice ovarian under lindane exposure. Nauka i Zdravookhranenie [Science & Healthcare]. 2016, 2, pp. 106-117.

Балмағамбетова А.Д., Жорабекова Г.А., Маккиарелли Г., Пальмерини М.Г., Ноттола С.А. Линданның әсерімен тышқандардың аналық бездерінің түйіршікті жасушаларының морфологиялық сипаттамасы / / Ғылым және Денсаулық сақтау. 2016. №2. Б. 106-117.


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