Mobilization of Ca2+ from Intracellular Stores in Sus scrofa domesticus Oocytes After Vitrification and Thawing

Vitaliy Yu. Denisenko, Tatiana I. Kuzmina

Abstract


Despite a significant progress in cryopreservation of embryos and male gametes, the vitrification of animal oocytes has been still a complicated and not fully resolved task due to a high sensitivity of female gamete cell compartments to the effects of ultralow temperatures and osmotic stress. This study was aimed to identify the intracellular mechanisms, determining the cryoresistance of animal oocytes. The features of Ca2 + mobilization from intracellular stores in vitrified porcine oocytes were studied using the fluorescent probe chlortetracycline. In these cells the relationship between different intracellular Ca2+ stores (IP3 and ryanodine sensitive), provided by microfilament participation, was established to be destroyed, and that between various intracellular Ca2+ stores, formed by microtubules, underwent certain changes. The guanosine triphosphate in vitrified oocytes became incapable of forming the bond between different intracellular stores, whereas the nanoparticles of highly dispersed silica preserved it. The bond between different intracellular Ca2+ stores in the oocytes, subjected to vitrification and thawing, was established to be provided not only by microtubules, but protein kinase C as well.

Probl Cryobiol Cryomed 2018; 28(2): 120-130


Keywords


calcium; vitrification; oocytes; calcium; Sus Scrofa Domesticus

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Albarracín J.L., Morató R., Rojas C. et al. Effects of vitrification in open pulled straws on the cytology of in vitro matured prepubertal and adult bovine oocytes. Theriogen 2005; 63(3): 890–901. CrossRef PubMed

Berridge M.J. The endoplasmic reticulum: a multifunctional signaling organelle. Cell Calcium 2002; 32(5-6): 235–249.

Boitseva E.N., Denisenko V.Yu., Kuzmina T.I. Evaluation of indicators of postejaculation maturation of spermatozoa of Bos taurus using a chlortetracycline test. Rus J Devel Biol 2015; 46(4): 362–367. CrossRef

Borini A., Cattoli M., Bulletti C. et al. Clinical efficiency of oocyte and embryo cryopreservation. Ann N Y Acad Sci 2008; 1127: 49–58. CrossRef PubMed

Bourguignon L.Y., Iida N., Jin H. The involvement of the cytoskeleton in regulating IP3 receptor-mediated internal Ca2+ release in human blood platelets. Cell Biol Int 1993; 17(8): 751–758. CrossRef PubMed

Chen S.U., Lien Y.R., Chao K.H. et al. Effects of cryopreservation on meiotic spindles of oocytes and its dynamics after thawing: clinical implications in oocyte freezing – a review article. Mol Cell Endocrinol 2003; 202: 101–107. CrossRef

Chuiko A.A. Medical chemistry and clinical application of silicon dioxide. Kyiv: Naukova Dumka; 2003.

Dawson R., Elliot D., Elliot W. et al. Handbook of biochemist. Moscow: Mir; 1991.

Denisenko V.Yu., Kuzmina T.I. Effects of guanine nucleotides and protein kinase C on prolactin-stimulated release of Са2+ from intracellular stores of pig oocytes. Rus J Devel Biol 2005; 36(3): 161–165. CrossRef

Denisenko V.Yu., Kuzmina T.I. Influence inhibiting of ryanodine and inositol triphosphate receptors, and protein kinase C in Са2+ exit from intracellular stores of porcine oocytes stimulation by prolactin and GTP. Tsitologiya 2007; 49(8): 685–689.

Denisenko V.Yu., Kuzmina T.I. The participation of the elements of cytoskeleton in the mobilization of Са2+ from intracellular stores of intact and devitrified porcine oocytes. R J Physiol 2016; 102(4): 480–489.

Diez C., Duque P., Gómez E. et al. Bovine oocyte vitrification before or after meiotic arrest: effects on ultrastructure and developmental ability. Theriogen 2005; 64(2): 317–333. CrossRef PubMed

Egerszegi I., Somfai T., Nakai M. et al. Comparison of cytoskeletal integrity, fertilization and developmental competence of oocytes vitrified before or after in vitro maturation in a porcine model. Criobiology 2013; 67(3): 287–292. CrossRef PubMed

FitzHarris G., Marangos P., Carroll J. Changes in endoplasmic reticulum structure during mouse oocyte maturation are controlled by the cytoskeleton and cytoplasmic dynein. Dev Biol 2007; 305(1): 133–144. CrossRef PubMed

Gertler A., Friesen H.G. Human growth hormone-stimulated mitogenesis of Nb2 node lymphoma cells is not mediated by an immediate acceleration of phosphoinositide metabolism. Mol Cell Endocrinol 1986; 48(2-3): 221–228.

Ghosh T.K., Mullaney J.M., Tarazy F.I. et al. GTP-activated communication between distinct inositol 1,4,5-trisphosphate-sensitive and -insensitive calcium pools. Nature 1989; 340: 236–239. CrossRef PubMed

Hajnoczky G., Lin C., Thomas A.P. Luminal communication between intracellular calcium stores modulated by GTP and the cytoskeleton. J Biol Chem 1994; 269(14): 10280–10287.

Hirose M., Kamoshita M., Fujiwara K. et al. Vitrification procedure decreases inositol 1,4,5-trisphophate receptor expression, resulting in low fertility of pig oocytes. Anim Sci J 2013; 84(10): 693–701. CrossRef

Ikeda M., Nelson C.S., Shinagawa H. et al. Cyclic AMP regulates the calcium transients released from IP3-sensitive stores by activation of rat kappa-opioid receptors expressed in CHO cells. Cell Calcium 2001; 29(1): 39–48. CrossRef PubMed

Kubota C., Yang X., Dinnyes A. et al. In vitro and in vivo survival of frozen-thawed bovine oocytes after IVF, nuclear transfer, and parthenogenetic activation. Mol Reprod Dev 1998; 51(3): 281–286. CrossRef

Larman M.G., Sheehan C.B., Gardner D.K. Calcium-free vitrification reduces cryoprotectant-induced zona pellucida hardening and increases fertilization rates in mouse oocytes. Reprod 2006; 131(1): 53–61. CrossRef PubMed

Lowther K.M., Weitzman V.N., Maier D. et al. Maturation, fertilization, and the structure and function of the endoplasmic reticulum in cryopreserved mouse oocytes. Biol Reprod 2009; 81(1): 147–154. CrossRef PubMed

Machaty Z., Funahashi H., Day B.N. et al. Developmental changes in the intracellular Ca2+ release mechanisms in porcine oocytes. Biol Reprod 1997; 56(4): 921–930. CrossRef PubMed

Michelangeli F., Ogunbayo O.A., Wootton L.L. A plethora of interacting organellar Са2+ stores. Cur Opin Cell Biol 2005; 17(2): 135–140. CrossRef PubMed

Mullaney J.M., Chueh S.H., Ghosh T.K. et al. Intracellular calcium uptake activated by GTP. Evidence for a possible guanine nucleotide-induced transmembrane conveyance of intracellular calcium. J Biol Chem 1987; 262(28): 13865–13872.

Ratovondrahona D., Fournier B., Odessa M.F. et al. Prolactin stimulation of phosphoinositide metabolism in CHO cells stably expressing the PRL receptor. Biochem Biophys Res Commun 1998; 243(1): 127–130. CrossRef PubMed

Ribeiro C.M., Reece J., Putney J.W.Jr. Role of the cytoskeleton in calcium signaling in NIH 3T3 cells. An intact cytoskeleton is required for agonist-induced [Ca2+]i signaling, but not for capacitative calcium entry. J Biol Chem 1997; 272(42): 26555–26561. CrossRef PubMed

Ribeiro C.M., McKay R.R., Hosoki E. et al. Effects of elevated cytoplasmic calcium and protein kinase C on endoplasmic reticulum structure and function in HEK293 cells. Cell Calcium 2000; 27(3): 175–185. CrossRef PubMed

Rojas C., Palomo M.J., Albarracin J.J. et al. Vitrification of immature and in vitro matured pig oocytes: study of distribution of chromosomes, microtubules and microfilaments. Criobiol 2004; 49(3): 211–220. CrossRef PubMed

Rubin R.P., Adolf M.A. Cyclic AMP regulation of calcium mobilization and amylase release from isolated permeabilized rat parotid cells. J Pharmacol Exp Ther 1994; 268(2): 600–606.

Sathananthan A.H., Ng S.C., Trounson A.O. et al. The effects of ultrarapid freezing on meiotic and mitotic spindles of mouse oocytes and embryos. Gamete Res 1988; 21(4): 385–401. CrossRef PubMed

Schlaitz A.L. Microtubules as key coordinators of nuclear envelope and endoplasmic reticulum dynamics during mitosis. Bioessays 2014; 36(7): 665-671. CrossRef PubMed

Somfai T., Kikuchi K., Nagai T. Factors affecting cryopreservation of porcine oocytes. J Reprod Dev 2012; 58(1): 17–24. CrossRef PubMed

Terasaki M., Chen L.B., Fujiwara K. Microtubules and the endoplasmic reticulum are highly interdependent structures. J Cell Biol 1986; 103(4): 1557–1568. CrossRef PubMed




DOI: https://doi.org/10.15407/cryo28.02.120

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