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cGMP and epigenetic factor in the suppression of apoptosis in ovarian follicles

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Abstract

The role of cGMP (cyclic guanosine monophosphate) in the suppression of apoptosis in preantral and preovulatory follicles has been established. But the underlying mechanisms have not yet been established. The present study has been focused on revealing the mechanisms involved in the cGMP mediated suppression of apoptosis and in survival of ovarian follicle. cGMP reduces calcium burden of the cell by mediating Ca2+ channels, BK (Big Potassium) channels, phosphatidylinositol 3-kinase (PI3K)/Akt pathway thus, prevents the mitochondrial membrane pore formation and apoptosis. cGMP induces the expression of Trx (thioredoxin) protein and prevents the TNF-α (Tumour Necrosis factor) induced apoptosis. cGMP also induces the expression of cytoskeleton proteins which are involved in heterogeneous distribution of mitochondria and there by reduces the Ca2+ burden and apoptosis. Histone 3 lysine 4 methyltransferase (MLL2) is an epigenetic factor inhibits the transcription of genes involved apoptosis which acts as co-activator of Estrogen receptor-α. In conclusion the present review predicts some mechanisms underlying the cGMP mediated suppression of apoptosis in ovarian follicles.

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References

  • Abkenar, Z.O., Ganji, R., Khajehrahimi, A.E., and Bahadori, M.H., Vitrification and subsequent in vitro maturation of mouse preantral follicles in presence of growth factors, Cell J. (Yakhteh), 2014, vol. 16, no. 3, p. 271.

    Google Scholar 

  • Alarid, E.T., Bakopoulos, N., and Solodin, N., Proteasome–mediated proteolysis of estrogen receptor: a novel component in autologous down-regulation, Mol. Endocrinol., 1999, vol. 13, no. 9, pp. 1522–1534.

    Article  CAS  PubMed  Google Scholar 

  • Andrade, P.M., Chaves, R.N., Alves, A.M.C.V., Rocha, R.M.P., Lima, L.F., Carvalho, A.A., Rodrigues, A.P.R., Campello, C.C., Gastal, E.L., and Figueiredo, J.R., Effects of α-MEM and TCM-199 culture media and epidermal growth factor on survival and growth of goat and sheep preantral follicles cultured in vitro, Anim. Reprod., 2014, vol. 11, no. 4, pp. 567–572.

    Google Scholar 

  • Andreu-Vieyra, C.V., Chen, R., Agno, J.E., Glaser, S., Anastassiadis, K., Stewart, A.F., and Matzuk, M.M., MLL2 is required in oocytes for bulk histone 3 lysine 4 trimethylation and transcriptional silencing, PLoS Biol., 2010, vol. 8, no. 8, p. e1000453.

    Article  PubMed  PubMed Central  Google Scholar 

  • Arunakumari, G., Shanmugasundaram, N., and Rao, V.H., Development of morulae from the oocytes of cultured sheep preantral follicles, Theriogenology, 2010, vol. 74, no. 5, pp. 884–894.

    Article  CAS  PubMed  Google Scholar 

  • Berridge, M.J., Lipp, P., and Bootman, M.D., The versatility and universality of calcium signaling, Nature Rev. Mol. Cell Biol., 2000, vol. 1, no. 1, pp. 11–21.

    Article  CAS  Google Scholar 

  • Billig, H., Furuta, I.T.S.U.K.O., and Hsueh, A.J., Estrogens inhibit and androgens enhance ovarian granulosa cell apoptosis, Endocrinology, 1993, vol. 133, no. 5, pp. 2204–2212.

    CAS  PubMed  Google Scholar 

  • Birkhead, T.R. and Pizzari, T., Postcopulatory sexual selection, Nature Rev. Genet., 2002, vol. 3, no. 4, pp. 262–273.

    Article  CAS  PubMed  Google Scholar 

  • Birkhead, T.R., Cryptic female choice: criteria for establishing female sperm choice, Evolution, 1998, vol. 52, no. 4, pp. 1212–1218.

    Article  Google Scholar 

  • Butt, E., Geiger, J., Jarchau, T., Lohmann, S.M., and Walter, U., The cGMP-dependent protein kinase–gene, protein, and function, Neurochem. Res., 1993, vol. 18, no. 1, pp. 27–42.

    Article  CAS  PubMed  Google Scholar 

  • Cavallini, L., Coassin, M., Borean, A., and Alexandre, A., Prostacyclin and sodium nitroprusside inhibit the activity of the platelet inositol 1,4,5-trisphosphate receptor and promote its phosphorylation, J. Biol. Chem., 1996, vol. 271, no. 10, pp. 5545–5551.

    Article  CAS  PubMed  Google Scholar 

  • Chakravarthi, V.P., Kona, S.S.R., Kumar, A.S., Bhaskar, M., and Rao, V.H., Quantitative expression of antiapoptotic and proapoptotic genes in sheep ovarian follicles grown in vivo or cultured in vitro, Theriogenology, 2015, vol. 83, no. 4, pp. 590–595.

    Article  Google Scholar 

  • Chun, S.Y. and Hsueh, A.J., Paracrine mechanisms of ovarian follicle apoptosis, J. Reprod. Immunol., 1998, vol. 39, no. 1, pp. 63–75.

    Article  CAS  PubMed  Google Scholar 

  • Chun, S.Y., Eisenhauer, K.M., Kubo, M., and Hsueh, A.J., Interleukin-1 beta suppresses apoptosis in rat ovarian follicles by increasing nitric oxide production, Endocrinology, 1995, vol. 136, no. 7, pp. 3120–3127.

    CAS  PubMed  Google Scholar 

  • Clapham, D.E., Calcium signaling, Cell, 1995, vol. 80, no. 2, pp. 259–268.

    Article  CAS  PubMed  Google Scholar 

  • Cortvrindt, R., Smitz, J., and Van Steirteghem, A.C., Assessment of the need for follicle stimulating hormone in early preantral mouse follicle culture in vitro, Human Reproduction, 1997, vol. 12, no. 4, pp. 759–768.

    Article  CAS  PubMed  Google Scholar 

  • Cossigny, D.A., Findlay, J.K., and Drummond, A.E., The effects of FSH and activin A on follicle development in vitro, Reproduction, 2012, vol. 143, no. 2, pp. 221–229.

    Article  CAS  PubMed  Google Scholar 

  • Demeestere, I., Streiff, A.K., Suzuki, J., Al-Khabouri, S., Mahrous, E., Tan, S.L., and Clarke, H.J., Folliclestimulating hormone accelerates mouse oocyte development in vivo, Biol. Reprod., 2012, vol. 87, no. 1, p. 3.

    Article  PubMed  Google Scholar 

  • Deng, W.P. and Ren, Z.R., Mitochondrial and oocyte development, Yi chuan = Hereditas/Zhongguo yi chuan xue hui bian ji, 2007, vol. 29, no. 12, pp. 1429–1433.

    CAS  Google Scholar 

  • Dimmeler, S., Fleming, I., Fisslthaler, B., Hermann, C., Busse, R., and Zeiher, A.M., Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation, Nature, 1999, vol. 399, no. 6736, pp. 601–605.

    Article  CAS  PubMed  Google Scholar 

  • Dou, Y., Milne, T.A., Tackett, A.J., Smith, E.R., Fukuda, A., Wysocka, J., Allis, C.D., Chait, B.T., Hess, J.L., and Roeder, R.G., Physical association and coordinate function of the H3 K4 methyltransferase MLL1 and the H4 K16 acetyltransferase MOF, Cell, 2005, vol. 121, no. 6, pp. 873–885.

    Article  CAS  PubMed  Google Scholar 

  • El Khissiin, A. and Leclercq, G., Implication of proteasome in estrogen receptor degradation, FEBS Lett., 1999, vol. 448, no. 1, pp. 160–166.

    Article  PubMed  Google Scholar 

  • Eppig, J.J. and O’Brien, M.J., Development in vitro of mouse oocytes from primordial follicles, Biol. Reprod., 1996, vol. 54, no. 1, pp. 197–207.

    Article  CAS  PubMed  Google Scholar 

  • Evans, J.P., Zane, L., Francescato, S., and Pilastro, A., Directional postcopulatory sexual selection revealed by artificial insemination, Nature, 2003, vol. 421, no. 6921, pp. 360–363.

    Article  CAS  PubMed  Google Scholar 

  • Fang, L., Chang, H.M., Cheng, J.C., Leung, P.C., and Sun, Y.P., Nitric oxide and cGMP induce COX-2 expression and PGE2 production in human granulosa cells through CREB signaling pathway, J. Clin. Endocrinol. Metab., 2014, vol. 100, no. 2, pp. E262–E269.

    Article  PubMed  Google Scholar 

  • Foerster, K., Delhey, K., Johnsen, A., et al., Females increase offspring heterozygosity and fitness through extra-pair matings, Nature, 2003, vol. 425, no. 6959, pp. 714–717.

    Article  CAS  PubMed  Google Scholar 

  • Fu, C.Q., Shi, F.X., Zhang, Z.H., Li, J.R., Huang, X.H., and Wang, Z.C., Changes in cyclic GMP level and phosphodiesterase activity during follicular development in the rat ovary, Genet. Mol. Res.: GMR, 2014, vol. 13, no. 3, p. 5919.

    Article  CAS  PubMed  Google Scholar 

  • Fukao, M., Mason, H.S., Britton, F.C., Kenyon, J.L., Horowitz, B., and Keef, K.D., Cyclic GMP-dependent protein kinase activates cloned BKCa channels expressed in mammalian cells by direct phosphorylation at serine 1072, J. Biol. Chem., 1999, vol. 274, no. 16, pp. 10927–10935.

    Article  CAS  PubMed  Google Scholar 

  • Ganji, R., Nabiuni, M., and Faraji, R., Development of mouse preantral follicle after in vitro culture in a medium containing melatonin, Cell J. (Yakhteh), 2015, vol. 16, no. 4, p. 546.

    Google Scholar 

  • Gomes, R.G., Lisboa, L.A., Silva, C.B., Max, M.C., Marino, P.C., Oliveira, R.L., González, S.M., Barreiros, T.R.R., Marinho, L.S.R., and Seneda, M.M., Improvement of development of equine preantral follicles after 6 days of in vitro culture with ascorbic acid supplementation, Theriogenology, 2015, vol. 84, no. 5, pp. 750–755.

    Article  CAS  PubMed  Google Scholar 

  • Gordo, A.C., Rodrigues, P., Kurokawa, M., Jellerette, T., Exley, G.E., Warner, C., and Fissore, R., Intracellular calcium oscillations signal apoptosis rather than activation in in vitro aged mouse eggs, Biol. Reprod., 2002, vol. 66, no. 6, pp. 1828–1837.

    Article  CAS  PubMed  Google Scholar 

  • Goud, A.P., Goud, P.T., Diamond, M.P., Gonik, B., and Abu-Soud, H.M., Activation of the cGMP signaling pathway is essential in delaying oocyte aging in diabetes mellitus, Biochemistry, 2006, vol. 45, no. 38, pp. 11366–11378.

    Article  CAS  PubMed  Google Scholar 

  • Gudi, T., Huvar, I., Meinecke, M., Lohmann, S.M., Boss, G.R., and Pilz, R.B., Regulation of gene expression by cGMP-dependent protein kinase transactivation of the c-fos promoter, J. Biol. Chem., 1996, vol. 271, no. 9, pp. 4597–4600.

    Article  CAS  PubMed  Google Scholar 

  • Gupta, P.S.P., Ramesh, H.S., Manjunatha, B.M., Nandi, S., and Ravindra, J.P., Production of buffalo embryos using oocytes from in vitro grown preantral follicles, Zygote, 2008, vol. 16, no. 1, pp. 57–63.

    Article  CAS  PubMed  Google Scholar 

  • Hanna, C.B., Yao, S., Wu, X., and Jensen, J.T., Identification of phosphodiesterase 9A as a cyclic guanosine monophosphate–specific phosphodiesterase in germinal vesicle oocytes: a proposed role in the resumption of meiosis, Fertil. Steril., 2012, vol. 98, no. 2, pp. 487–495.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hasegawa, A., Mochida, N., Ogasawara, T., and Koyama, K., Pup birth from mouse oocytes in preantral follicles derived from vitrified and warmed ovaries followed by in vitro growth, in vitro maturation, and in vitro fertilization, Fertil. Steril., 2006, vol. 86, no. 4, pp. 1182–1192.

    Article  PubMed  Google Scholar 

  • Haug, L.S., Jensen, V., Hvalby, Ø., Walaas, S.I., and Ostvold, A.C., Phosphorylation of the inositol 1,4,5-trisphosphate receptor by cyclic nucleotide-dependent kinases in vitro and in rat cerebellar slices in situ, J. Biol. Chem., 1999, vol. 274, no. 11, pp. 7467–7473.

    Article  CAS  PubMed  Google Scholar 

  • Hofmann, T., Schaefer, M., Schultz, G., and Gudermann, T., Transient receptor potential channels as molecular substrates of receptor-mediated cation entry, J. Mol. Med., 2000, vol. 78, no. 1, pp. 14–25.

    Article  CAS  PubMed  Google Scholar 

  • Hsueh, A.J., Billig, H., and Tsafriri, A., Ovarian follicle atresia: a hormonally controlled apoptotic process, Endocr. Rev., 1994, vol. 5, no. 6, pp. 707–724.

    Google Scholar 

  • Hughes, F.M., Jr. and Gorospe, W.C., Biochemical identification of apoptosis (programmed cell death) in granulosa cells: evidence for a potential mechanism underlying follicular atresia, Endocrinology, 1991, vol. 129, no. 5, pp. 2415–2422.

    Article  CAS  PubMed  Google Scholar 

  • Jackson, P.K., Eldridge, A.G., Freed, E., Furstenthal, L., Hsu, J.Y., Kaiser, B.K., and Reimann, J.D., The role the RINGs: substrate recognition and catalysis by ubiquitin ligases, Trends Cell Biol., 2000, vol. 10, no. 10, pp. 429–439.

    Article  CAS  PubMed  Google Scholar 

  • Jaiswal, A.K., Nrf2 signaling in coordinated activation of antioxidant gene expression, Free Rad. Biol. Med., 2004, vol. 36, no. 10, pp. 1199–1207.

    Article  CAS  PubMed  Google Scholar 

  • Jiang, L.H., Gawler, D.J., Hodson, N., Milligan, C.J., Pearson, H.A., Porter, V., and Wray, D., Regulation of cloned cardiac L-type calcium channels by cGMPdependent protein kinase, J. Biol. Chem., 2000, vol. 275, no. 9, pp. 6135–6143.

    Article  CAS  PubMed  Google Scholar 

  • Jiang, L.H., Gawler, D.J., Hodson, N., Milligan, C.J., Pearson, H.A., Porter, V., and Wray, D., Regulation of cloned cardiac L-type calcium channels by cGMPdependent protein kinase, J. Biol. Chem., 2000, vol. 275, no. 9, pp. 6135–6143.

    Article  CAS  PubMed  Google Scholar 

  • Jorssen, E.P.A., Langbeen, A., Marei, W.F.A., Fransen, E., Leroy, J.L.M.R., and Bols, P.E.J., Morphologic characterization of isolated bovine early preantral follicles during short-term individual in vitro culture, Theriogenology, 2015, vol. 84, no. 2, pp. 301–311.

    Article  CAS  PubMed  Google Scholar 

  • Kaneko, H., Kikuchi, K., Noguchi, J., Hosoe, M., and Akita, T., Maturation and fertilization of porcine oocytes from primordial follicles by a combination of xenografting and in vitro culture, Biol. Reprod., 2003, vol. 69, no. 5, pp. 1488–1493.

    Article  CAS  PubMed  Google Scholar 

  • Komatsu, K., Koya, T., Wang, J., Yamashita, M., Kikkawa, F., and Iwase, A., Analysis of the effect of leukemia inhibitory factor on follicular growth in cultured murine ovarian tissue, Biol. Reprod., 2015, pp. biolreprod–115.

    Google Scholar 

  • Kona, S.S.R., Chakravarthi, V.P., Kumar, A.S., Srividya, D., Padmaja, K., and Rao, V.H., Quantitative expression patterns of GDF9 and BMP15 genes in sheep ovarian follicles grown in vivo or cultured in vitro, Theriogenology, 2016, vol. 85, no. 2, pp. 315–322.

    Article  CAS  PubMed  Google Scholar 

  • Lakshminarayana, B.N.V., Chakravarthi, V.P., Brahmaiah, K.V., and Rao, V.H., Quantification of P450 aromatase gene expression in cultured and in vivo grown ovarian follicles in sheep, Small Ruminant Res., 2014, vol. 117, no. 1, pp. 66–72.

    Article  Google Scholar 

  • Lan, T., Chen, Y., Sang, J., Wu, Y., Wang, Y., Jiang, L., and Tao, Y., Type II cGMP-dependent protein kinase inhibits EGF-induced MAPK/JNK signal transduction in breast cancer cells, Oncol. Rep., 2012, vol. 27, no. 6, pp. 2039–2044.

    CAS  PubMed  Google Scholar 

  • Lee, S.Y., Andoh, T., Murphy, D.L., and Chiueh, C.C., 17β-Estradiol activates ICI 182,780-sensitive estrogen receptors and cyclic GMP-ependent thioredoxin expression for neuroprotection, FASEB J., 2003, vol. 17, no. 8, pp. 947–948.

    CAS  PubMed  Google Scholar 

  • Lee, S.Y., Andoh, T., Murphy, D.L. and Chiueh, C.C., 17β-Estradiol activates ICI 182,780-ensitive estrogen receptors and cyclic GMP-dependent thioredoxin expression for neuroprotection, FASEB J., 2003, vol. 17, no. 8, pp. 947–948.

    CAS  PubMed  Google Scholar 

  • Leitao, C.C.F., Costa, J.J.D.N., Brito, I.R., Magalhães-Padilha, D.D.M., Almeida, A.P., Figueiredo, J.R.D., van den Hurk, R., and Silva, J.R.V., Effects of GDF-9 and FSH on mRNA expression for FSH-R, GDF-9 and BMPs in in vitro cultured goat preantral follicles, Braz. Arch. Biol. Technol., 2014, vol. 57, no. 2, pp. 200–208.

    Article  CAS  Google Scholar 

  • Lincoln, T.M., Dey, N., and Sellak, H., Invited review: cGMP-dependent protein kinase signaling mechanisms in smooth muscle: from the regulation of tone to gene expression, J. Appl. Physiol., 2001, vol. 91, no. 3, pp. 1421–1430.

    CAS  PubMed  Google Scholar 

  • Lincoln, T.M. and Komalavilas, P., Cyclic GMP-mediated signaling mechanisms in smooth muscle, in Nitric Oxide, Ignarro, L.J., Ed., New York: Academic, 2000, pp. 401–4425.

    Chapter  Google Scholar 

  • Liou, J.Y., Jeng, K.S., Lin, C.G., Hu, C.P., and Chang, C., A novel regulator inhibits HBV gene expression, J. Biomed. Sci., 1998, vol. 5, no. 5, pp. 343–354.

    Article  CAS  PubMed  Google Scholar 

  • Liu, H., Chang, H.C., Zhang, J., Grifo, J., and Krey, L.C., Metaphase II nuclei generated by germinal vesicle transfer in mouse oocytes support embryonic development to term, Hum. Reprod., 2003, vol. 18, no. 9, pp. 1903–1907.

    Article  PubMed  Google Scholar 

  • Magalhães, D.M., Duarte, A.B.G., Araújo, V.R., Brito, I.R., Soares, T.G., Lima, I.M.T., Lopes, C.A.P., Campello, C.C., Rodrigues, A.P.R. and Figueiredo, J.R., In vitro production of a caprine embryo from a preantral follicle cultured in media supplemented with growth hormone, Theriogenology, vol. 2011, no. 75, pp. 182–188.

    Article  PubMed  Google Scholar 

  • Mani, S.K. and Oyola, M.G., Progesterone signaling mechanisms in brain and behavior, Neurosteroids, 2012, p. 149.

    Google Scholar 

  • Markstrom, E., Svensson, E., Shao, R., Svanberg, B., and Billig, H., Survival factors regulating ovarian apoptosisdependence on follicle differentiation, Reproduction, 2002, vol. 123, no. 1, pp. 23–30.

    Article  CAS  PubMed  Google Scholar 

  • McGee, E., Spears, N., Minami, S., Hsu, S.Y., Chun, S.Y., Billig, H., and Hsueh, A.J., Preantral ovarian follicles in serum-free culture: suppression of apoptosis after activation of the cyclic guanosine 3′,5′-monophosphate pathway and stimulation of growth and differentiation by follicle-stimulating hormone, Endocrinology, 1997, vol. 138, no. 6, pp. 2417–2424.

    CAS  PubMed  Google Scholar 

  • McGee, E.A. and Hsueh, A.J., Initial and cyclic recruitment of ovarian follicles 1, Endocrine Rev., 2000, vol. 21, no. 2, pp. 200–214.

    CAS  Google Scholar 

  • Milne, T.A., Briggs, S.D., Brock, H.W., Martin, M.E., Gibbs, D., Allis, C.D., and Hess, J.L., MLL targets SET domain methyltransferase activity to Hox gene promoters, Mol. Cell, 2002, vol. 10, no. 5, pp. 1107–1117.

    Article  CAS  PubMed  Google Scholar 

  • Mo, R., Rao, S.M., and Zhu, Y.J., Identification of the MLL2 complex as a coactivator for estrogen receptor α, J. Biol. Chem., 2006, vol. 281, no. 23, pp. 15714–15720.

    Article  CAS  PubMed  Google Scholar 

  • Nakamura, T., Mori, T., Tada, S., Krajewski, W., Rozovskaia, T., Wassell, R., Dubois, G., Mazo, A., Croce, C.M., and Canaani, E., ALL-1 is a histone methyltransferase that assembles a supercomplex of proteins involved in transcriptional regulation, Mol. Cell, 2002, vol. 10, no. 5, pp. 1119–1128.

    Article  CAS  PubMed  Google Scholar 

  • Nawaz, Z., Lonard, D.M., Dennis, A.P., Smith, C.L., and O’Malley, B.W., Proteasome-dependent degradation of the human estrogen receptor, Proc. Natl. Acad. Sci. U. S. A., 1999, vol. 96, no. 5, pp. 1858–1862.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nelson, M.T., Cheng, H., Rubart, M., Santana, L.F., Bonev, A.D., Knot, H.J., and Lederer, W.J., Relaxation of arterial smooth muscle by calcium sparks, Science, 1995, vol. 270, no. 5236, pp. 633–637.

    Article  CAS  PubMed  Google Scholar 

  • Norris, R.P., Ratzan, W.J., Freudzon, M., Mehlmann, L.M., Krall, J., Movsesian, M.A., Wang, H., Ke, H., Nikolaev, V.O., and Jaffe, L.A., Cyclic GMP from the surrounding somatic cells regulates cyclic AMP and meiosis in the mouse oocyte, Development, 2009, vol. 136, no. 11, pp. 1869–1878.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oliveira, C.J., Schindler, F., Ventura, A.M., Morais, M.S., Arai, R.J., Debbas, V., Stern, A., and Monteiro, H.P., Nitric oxide and cGMP activate the Ras-MAP kinase pathway-stimulating protein tyrosine phosphorylation in rabbit aortic endothelial cells, Free Rad. Biol. Med., 2003, vol. 35, no. 4, pp. 381–396.

    Article  CAS  PubMed  Google Scholar 

  • Ozawa, M., Nagai, T., Somfai, T., Nakai, M., Maedomari, N., Fahrudin, M., Karja, N.W.K., Kaneko, H., Noguchi, J., Ohnuma, K., and Yoshimi, N., Comparison between effects of 3-isobutyl-1-methylxanthine and FSH on gap junctional communication, LH-receptor expression, and meiotic maturation of cumulus-oocyte complexes in pigs, Mol. Reprod. Dev., 2008, vol. 75, no. 5, pp. 857–866.

    Article  CAS  PubMed  Google Scholar 

  • Palmon, S.C., Williams, M.J., Littleton-Kearney, M.T., Traystman, R.J., Kosk-Kosicka, D., and Hurn, P.D., Estrogen increases cGMP in selected brain regions and in cerebral microvessels, J. Cerebr. Blood Flow Metab., 1998, vol. 18, no. 11, pp. 1248–1252.

    Article  CAS  Google Scholar 

  • Rossetto, R., Santos, R.R., Silva, G.M., Duarte, A.B.G., Silva, C.M.G., Campello, C.C., and Figueiredo, J.R., Comparative study on the in vitro development of caprine and bovine preantral follicles, Small Ruminant Res., 2013, vol. 113, no. 1, pp. 167–170.

    Article  Google Scholar 

  • Saitoh, M., Nishitoh, H., Fujii, M., Takeda, K., Tobiume, K., Sawada, Y., Kawabata, M., Miyazono, K., and Ichijo, H., Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1, EMBO J., 1998, vol. 17, no. 9, pp. 2596–2606.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sakuta, H., Okamoto, K., and Watanabe, Y., Modification by cGMP of glibenclamide-sensitive K+ currents in Xenopus oocytes, Jpn. J. Pharmacol., 1993, vol. 61, no. 3, pp. 259–262.

    Article  CAS  PubMed  Google Scholar 

  • Schlossmann, J., Ammendola, A., Ashman, K., Zong, X., Huber, A., Neubauer, G., Wang, G.X., Allescher, H.D., Korth, M., Wilm, M., and Hofmann, F., Regulation of intracellular calcium by a signalling complex of IRAG, IP3 receptor and cGMP kinase Iβ, Nature, 2000, vol. 404, no. 6774, pp. 197–201.

    Article  CAS  PubMed  Google Scholar 

  • Sellak, H., Yang, X., Cao, X., Cornwell, T., Soff, G.A., and Lincoln, T., Sp1 transcription factor as a molecular target for nitric oxide- and cyclic nucleotide–mediated suppression of cGMP-dependent protein kinase-Iα expression in vascular smooth muscle cells., Circ. Res., 2002, vol. 90, no. 4, pp. 405–412.

    Article  CAS  PubMed  Google Scholar 

  • Sharma, G.T., Dubey, P.K., and Kumar, G.S., Effects of IGF-1, TGF-α plus TGF-β 1 and bFGF on in vitro survival, growth and apoptosis in FSH-stimulated buffalo (Bubalis bubalus) preantral follicles, Growth Hormone IGF Res., 2010, vol. 20, no. 4, pp. 319–325.

    Article  CAS  Google Scholar 

  • Soff, G.A., Cornwell, T.L., Cundiff, D.L., Gately, S., and Lincoln, T.M., Smooth muscle cell expression of type I cyclic GMP-dependent protein kinase is suppressed by continuous exposure to nitrovasodilators, theophylline, cyclic GMP, and cyclic AMP, J. Clin. Invest., 1997, vol. 100, no. 10, p. 2580.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stoica, G.E., Franke, T.F., Moroni, M., Mueller, S., Morgan, E., Iann, M.C., Winder, A.D., Reiter, R., Wellstein, A., Martin, M.B., and Stoica, A., Effect of estradiol on estrogen receptor-α gene expression and activity can be modulated by the ErbB2/PI 3-K/Akt pathway, Oncogene, 2003, vol. 22, no. 39, pp. 7998–8011.

    Article  PubMed  Google Scholar 

  • Stratton, R.C., Squires, P.E., and Green, A.K., 17β-Estradiol elevates cGMP and, via plasma membrane recruitment of protein kinase GIα, stimulates Ca2+ efflux from rat hepatocytes, J. Biol. Chem., 2010, vol. 285, no. 35, pp. 27201–27212.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun, Q.Y., Wu, G.M., Lai, L., Park, K.W., Cabot, R., Cheong, H.T., Day, B.N., Prather, R.S., and Schatten, H., Translocation of active mitochondria during pig oocyte maturation, fertilization and early embryo development in vitro, Reproduction, 2001, vol. 122, no. 1, pp. 155–163.

    Article  CAS  PubMed  Google Scholar 

  • Tamura, T., Nakanishi, T.O.H.R.U., Kimura, Y.U.S.U.K.E., Hattori, T.A.K.A.K.O., Sasaki, K., Norimatsu, H.I.R.O.M.I.C.H.I., Takahashi, K., and Takigawa, M.A.S.A.H.A.R.U., Nitric oxide mediates interleukin- 1-induced matrix degradation and basic fibroblast growth factor release in cultured rabbit articular chondrocytes: a possible mechanism of pathological neovascularization in arthritis, Endocrinology, 1996, vol. 137, no. 9, pp. 3729–3737.

    CAS  PubMed  Google Scholar 

  • Tiwari, M., Prasad, S., Tripathi, A., Pandey, A.N., Ali, I., Singh, A.K., Shrivastav, T.G., and Chaube, S.K., Apoptosis in mammalian oocytes: a review, Apoptosis, 2015, vol. 20, no. 8, pp. 1019–1025.

    Article  CAS  PubMed  Google Scholar 

  • Torner, H., Brüssow, K.P., Alm, H., Ratky, J., Pöhland, R., Tuchscherer, A., and Kanitz, W., Mitochondrial aggregation patterns and activity in porcine oocytes and apoptosis in surrounding cumulus cells depends on the stage of pre–ovulatory maturation, Theriogenology, 2004, vol. 61, no. 9, pp. 1675–1689.

    Article  CAS  PubMed  Google Scholar 

  • Vaccari, S., Weeks, J.L., Hsieh, M., Menniti, F.S., and Conti, M., Cyclic GMP signaling is involved in the luteinizing hormone-dependent meiotic maturation of mouse oocytes, Biol. Reprod., 2009, vol. 81, no. 3, pp. 595–604.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vasconcelos, G.L., Saraiva, M.V.A., Costa, J.J.N., Passos, M.J., Silva, A.W.B., Rossi, R.O.D.S., Portela, A.M.L.R., Duarte, A.B.G., Magalhães-Padilha, D.M., Campelo, C.C., and Figueiredo, J.R., Effects of growth differentiation factor-9 and FSH on in vitro development, viability and mRNA expression in bovine preantral follicles, Reprod., Fertil. Dev., 2013, vol. 25, no. 8, pp. 1194–1203.

    Article  CAS  Google Scholar 

  • Vaux, D.L. and Silke, J., IAPs, RINGs and ubiquitylation, Nature Rev. Mol. Cell Biol., 2005, vol. 6, no. 4, pp. 287–297.

    Article  CAS  Google Scholar 

  • Wang, X. and Schwarz, T.L., The mechanism of Ca2+- dependent regulation of kinesin-mediated mitochondrial motility, Cell, 2009, vol. 136, no. 1, pp. 163–174.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wigglesworth, K., Lee, K.B., O’Brien, M.J., Peng, J., Matzuk, M.M., and Eppig, J.J., Bidirectional communication between oocytes and ovarian follicular somatic cells is required for meiotic arrest of mammalian oocytes, Proc. Natl. Acad. Sci. U. S. A., 2013, vol. 110, no. 39, pp. E3723–E3729.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu, J., Emery, B.R., and Carrell, D.T., In vitro growth, maturation, fertilization, and embryonic development of oocytes from porcine preantral follicles, Biol. Reprod., 2001, vol. 64, no. 1, pp. 375–381.

    Article  CAS  PubMed  Google Scholar 

  • Wu, Y., Chen, Y., Qu, R., Lan, T., and Sang, J., Type II cGMP-dependent protein kinase inhibits EGF-triggered signal transduction of the MAPK/ERK-mediated pathway in gastric cancer cells, Oncol. Rep., 2012, vol. 27, no. 2, pp. 553–558.

    CAS  PubMed  Google Scholar 

  • Xu, M., Kreeger, P.K., Shea, L.D., and Woodruff, T.K., Tissue-engineered follicles produce live, fertile offspring, Tissue Eng., 2006, vol. 12, no. 10, pp. 2739–2746.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, M., Su, Y.Q., Sugiura, K., Wigglesworth, K., Xia, G., and Eppig, J.J., Estradiol promotes and maintains cumulus cell expression of natriuretic peptide receptor 2 (NPR2) and meiotic arrest in mouse oocytes in vitro, Endocrinology, 2011, vol. 152, no. 11, pp. 4377–4385.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng, W., Zhang, H., Gorre, N., Risal, S., Shen, Y., and Liu, K., Two classes of ovarian primordial follicles exhibit distinct developmental dynamics and physiological functions, Hum. Mol. Genet., 2013, p. ddt486.

    Google Scholar 

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Correspondence to V. Praveen Chakravarthi.

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Chakravarthi, V.P., Sireesha, Y., Kumar, Y.N. et al. cGMP and epigenetic factor in the suppression of apoptosis in ovarian follicles. Russ J Dev Biol 47, 303–312 (2016). https://doi.org/10.1134/S1062360416060059

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