152
Views
11
CrossRef citations to date
0
Altmetric
Basic Research

Transmission electron microscopic analysis of malathion-induced cytotoxicity in granulosa cells of caprine antral follicles

, PhD & , MSc
Pages 43-50 | Received 21 May 2015, Accepted 26 Aug 2015, Published online: 29 Oct 2015

References

  • Erickson G, Shimasaki S. The role of the oocyte in folliculogenesis. Trends Endocr Met 2000;11(5): 193–8.
  • Paulini F, Silva RC, Paula-Rôlo JLJ, et al. Ultrastructural changes in oocytes during folliculogenesis in domestic mammals. J Ovarian Res 2014;7:102–14.
  • Luborsky JL, Meyer P, Sowers MF, et al. Premature menopause in a multi-ethnic population study of the menopause transition. Hum Reprod 2003;18:199–206.
  • Zhou KL, Xu JJ, Ni YH, et al. SIRT1 activator (SRT1720) improves the follicle reserve and prolongs the ovarian lifespan of diet-induced obesity in female mice via activating SIRT1 and suppressing mTOR signalling. J Ovarian Res 2014;7:97–109.
  • Manabe N, Goto Y, Matsuda-Minehata F, et al. Regulation mechanism of selective atresia in porcine follicles: Regulation of granulosa cell apoptosis during atresia. J Reprod Dev 2004;50:493–514.
  • Li R, Albertini DF. The road to maturation: Somatic cell interaction and self-organization of the mammalian oocyte. Nat Rev Mol Cell Biol 2013;14:141–52.
  • Elmore S. Apoptosis: A review of programmed cell death. Toxicol Pathol 2007;35(4): 495–516.
  • Taaties DJ, Sobel BE, Budd RC. Morphological and cytochemical determination of cell death by apoptosis. Histochem Cell Biol 2008;129(1): 33–43.
  • Walker PR, Weaver VM, Lach B, et al. Endonuclease activities associated with high molecular weight and internucleosomal DNA fragmentation in apoptosis. Exp Cell Res 1994;213(1): 100–6.
  • Valdez KE, Cuneo SP, Turzillo AM. Regulation of apoptosis in the atresia of dominant bovine follicles of the first follicular wave following ovulation. Reproduction 2005;130:71–81.
  • Matsui T, Manabe N, Goto Y, et al. Expression and activity of Apaf1 and caspase-9 in granulosa cells during follicular atresia in pig ovaries. Reproduction 2003;126:113–20.
  • Sharma RK, Bhardwaj JK. Granulosa cell apoptosis in situ in caprine ovary. J Cell Tissue Res 2007;7:1111–4.
  • Sharma RK, Bhardwaj JK. Ultrastructural characterization of apoptotic granulosa cells in caprine cells. J Microsc 2009;236:236–42.
  • Wu J, Jing L, Yuan H, et al. T-2 toxin induces apoptosis in ovarian granulosa cells of rats through reactive oxygen species-mediated mitochondrial pathway. Toxicol Lett 2011;202(3): 168–77.
  • Yu YS, Sui HS, Han ZB, et al. Apoptosis in granulosa cells during follicular atresia: Relationship with steroids and insulin-like growth factors. Cell Res 2004;14:341–6.
  • Devine PJ, Perreault SD, Luderer U. Roles of reactive oxygen species and antioxidants in ovarian toxicity. Biol Reprod 2012;86(2): 27–37.
  • Shem M, Lin F, Zhang J, et al. Involvement of the up-regulated FoxO1 expression in follicular granulosa cell apoptosis induced by oxidative stress. J Biol Chem 2012;287(31): 25727–40.
  • Choudhary A, Ali AS, Ali SA. Adverse health effects of organophosphate pesticides among occupationally exposed farm sprayers: A case study of Bhopal Madhya Pradesh, India. Asian J Biomed Pharm Sci 2014;4(35): 29–34.
  • Prashanthi N, Narayana K, Nayanatara A, et al. The reproductive toxicity of the organophosphate pesticide 0,0-dimethyl 0- 4-nitrophenyl phosphorothioate (methyl parathion) in the male rat. Folia Morphol (Warsz) 2006;65(4): 309–21.
  • Joshi SC, Mathur R, Gulati N. Testicular toxicity of chlorpyrifos (an organophosphate pesticide) in albino rat. Toxicol Ind Health 2007;23(7): 439–44.
  • Bustos-Obregón E, Sobarzo C. Acute effect of parathion on the seminiferous epithelium of immature mice. Rev Chil Anat 2002;18:61–8.
  • Azarnia M, Koochesfahani HM, Rajabi M, et al. Histological examination of endosulfan effects on follicular development of BALB/C mice. Bul J Vet Med 2008;12(1): 33−41.
  • Koc ND, Kayhan FE, Sesal C, et al. Dose-dependent effects of endosulfan and malathion on adult Wistar albino rat ovaries. Pak J Biol Sci 2009;12:498–503.
  • Chitnis SS, Navlakhe RM, Shinde GC, et al. Granulosa cell apoptosis induced by a novel FSH binding inhibitory peptide from human ovarian follicular fluid. J Histochem Cytochem 2008;56(11): 961–8.
  • Centurione L, Giampietro F, Sancilio S, et al. Morphometric and ultrastructural analysis of human granulosa cells after gonadotrophin-releasing hormone agonist or antagonist. Reprod BioMed 2010;20:625–33.
  • Kročková J, Massányi P, Sirotkin AV, et al. Nickel-induced structural and functional alterations in porcine granulosa cells in vitro. Biol Trace Elem Res 2013;154:190–5.
  • Hertig A, Adams E. Studies on human oocyte and its follicle, ultrastructure and its cytochemical observation on the preovulatory follicles. J Cell Biol 1967;34:647–75.
  • Bhardwaj JK, Saraf P. Malathion-induced granulosa cell apoptosis in caprine antral follicles: An ultrastructural and flow cytometric analysis. Microsc Microanal 2014;20:1861–8.
  • Miller KP, Gupta RK, Greenfeld CR, et al. Methoxychlor directly affects ovarian antral follicle growth and atresia through Bcl-2- and bax mediated pathways. Toxicol Sci 2005;88(1): 213–21.
  • Peluso JJ, Steger RW. Surface ultrastructural changes in granulosa cells of atretic follicles. Biol Reprod 1977;16:600–4.
  • Escobar ML, Echeverría OM, Casasa AS, et al. Involvement of pro-apoptotic and pro-autophagic proteins in granulosa cell death. Cell Biol 2013;1(1): 9–17.
  • Sugimoto M, Manabe N, Kimura Y, et al. Ultrastructure changes in granulosa cells in porcine antral follicles undergoing atresia indicate apoptotic cell death. J Reprod Dev 1998;44(1): 7–14.
  • Peluso JJ, Charlesworth C, Bolender DL, et al. Ultrastructural alterations associated with the initiation of follicular atresia. Cell Tiss Res 1980;211:105–15.
  • Wójtowicz AK, Gregoraszczuk EL, Ptak A, et al. 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;56:465–72.
  • Funkhouser CM, Sknepneka R, Shimib T, et al. Mechanical model of blebbing in nuclear lamin meshworks. PNAS 2013;10(9): 1348–53.
  • Dechat T, Pfleghaar K, Sengupta K, et al. Nuclear lamins: Major factors in the structural organization and function of the nucleus and chromatin. Genes Dev 2008;22(7): 832–53.
  • Broers JL, Bronnenberg, NM, Kuijpers HJ, et al. Partial cleavage of A- type lamins concurs with their total disintegration from the nuclear lamina during apoptosis. Eur J Cell Biol 2002;81:677–91.
  • Croft DR, Coleman ML, Li S, et al. Actin-myosin–based contraction is responsible for apoptotic nuclear disintegration. J Cell Biol 2005;168(2): 245–55.
  • Ferrando-May E, Cordes V, Biller-Ckovric I, et al. Caspases mediate nucleoporin cleavage, but not early redistribution of nuclear transport factors and modulation of nuclear permeability in apoptosis. Cell Death Differ 2001;8:495–505.
  • Andrade R, Crisol L, Prado R, et al. Plasma membrane and nuclear envelope integrity during the blebbing stage of apoptosis: A time-lapse study. Biol Cell 2010;102:25–35.
  • Lu XT, Ma Y, Wang C, et al. Cytotoxicity and DNA damage of five organophosphorus pesticides mediated by oxidative stress in PC12 cells and protection by vitamin E. J Environ Sci Health B 2012;47(5): 445–54.
  • Raturi A, Simmen T. Where the endoplasmic reticulum and the mitochondrion tie the knot: The mitochondria-associated membrane (MAM). Biochem Biophys Acta 2013;1833(1): 213–24.
  • Maxfield FR, Menon AK. Intracellular sterol transport and distribution. Curr Opin Cell Biol 2006;18:379–85.
  • Weihua F, Gabriel A, Baby-Periyanayak M, et al. Genome-wide analysis of sterol-lipid storage and trafficking in saccharomyces cerevisiae. American society for microbiology. Eukaryot Cell 2008;7(2): 401–14.
  • Hyttel P, Westergaard L, Byskov AG. Ultrastructure of human cumulus–oocyte complexes from healthy and atretic follicles. Hum Reprod 1986;1:153–7.
  • Garris DR. Diabetes (db/db) mutation-induced endometrial epithelial lipoapoptosis: Ultrastructural and cytochemical analysis of reproductive tract atrophy. Reprod Boil Endocrinol 2005;3:15–26.
  • Bonilla E, Hernandez F, Cortes L, et al. Effects of the insecticides malathion and diazinon on the early oogenesis in mice in vitro. Environ Toxicol 2007;23:240–5.
  • Videira RA, Antunes-Madeira MC, Madeira VM. Ethylazinphos interaction with membrane lipid organization induces increase of proton permeability and impairment of mitochondrial bioenergetic functions. Toxicol Appl Pharmacol 2001;175:209–16.
  • Ricci JE, Muñoz-Pinedo C, Fitzgerald P, et al. Disruption of mitochondrial function during apoptosis is mediated by caspase cleavage of the p75 subunit of complex I of the electron transport chain. Cell 2004;117:773–86.
  • Maiuri MC, Zalckvar E, Kimchi A, et al. Self-eating and self-killing: Crosstalk between autophagy and apoptosis. Nat Rev Mol Cell Biol 2007;8:741–52.
  • Moss DK, Betin VM, Malesinski SD, et al. A novel role for microtubules in apoptotic chromatin dynamics and cellular fragmentation. J Cell Sci 2006;119(11): 2362–74.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.