Ultrastructural localisation of calcium deposits in the mouse ovary
M. Sedmíková A C , R. Rajmon A , J. Petr B , M. Vaňková A , J. Rozinek A , D. Řehák B and F. Jílek AA Department of Veterinary Science, Czech University of Agriculture in Prague, 165 21 Prague 6, Czech Republic.
B Research Institute of Animal Production, Prague 10, Czech Republic.
C To whom correspondence should be addressed. email: sedmikova@af.czu.cz
Reproduction, Fertility and Development 15(8) 415-421 https://doi.org/10.1071/RD03040
Submitted: 27 June 2003 Accepted: 18 December 2003 Published: 17 February 2004
Abstract
Follicle-enclosed mouse oocytes contain numerous calcium deposits. The ultrastructural distribution of calcium deposits in the nuclei, mitochondria and cytoplasm of mouse oocytes and granulosa cells of primary, secondary and antral follicles was examined using the combined oxalate–pyroantimonate method. The mitochondria of oocytes from all types of follicles had the highest levels of calcium deposits of all oocyte compartments, with the exception of primary follicles, in which oocyte nuclei contained the same level of calcium deposits as the mitochondria. Calcium deposits in the cytoplasm of oocytes from primary follicles were significantly lower than those in the cytoplasm of oocytes from secondary and antral follicles. Calcium deposits in the cytoplasm of granulosa cells were significantly lower than calcium deposits in the mitochondria of granulosa cells and this difference persisted throughout all categories of follicles. Calcium deposits in the nuclei of granulosa cells did not differ from levels in the mitochondria in primary and secondary follicles. In contrast, the nuclei of granulosa cells from antral follicles had lower levels of calcium deposits than the mitochondria. The differences observed in calcium deposits in various cellular compartments in oocytes and granulosa cells in the follicles of ovaries of adult mice can be attributed to their acquisition of meiotic competence and follicular development.
Extra keywords: granulosa cells, oocyte.
Acknowledgments
We thank Mrs Lucy Westcott and Miss Lois Russell for editorial assistance with this manuscript. This work was supported by grants from MZeČR (M02-99-01, QD0085 and MSM412100003).
Andreucetti, P. , Denis-Donini, S. , Burrini, A. G. , and Campanella, C. (1984). Calcium ultrastructural localization in Xenopus laevis egg following activation by pricking or by calcium ionophore A 23187. J. Exp. Zool. 229, 295–308.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Bachs, O. , Agell, N. , and Carafoli, E. (1994). Calmodulin and calmodulin-binding proteins in the nucleus. Cell Calcium 16, 289–296.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Berridge, M. J. (1995). Capacitative calcium entry. Biochem. J. 312, 1–11.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Berruti, G. , Franchi, E. , and Camatini, M. (1986). Ca++ localization in boar spermatozoa by pyroantimonate technique and X-ray microanalysis. J. Exp. Zool. 237, 257–262.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Bertout, M. , Flament, S. , Browaeys-Poly, E. , and Vilain, J.-P. (1997). Ultrastructural localization of intracellular calcium stores in Xenopus ovarian follicles as revealed by cytochemistry and X-ray microanalysis. Dev. Growth Differ. 39, 249–256.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Borgers, M. , Thine, F. , and Van Nueten, J. (1981). The subcellular distribution of calcium and effect of calcium-antagonists as evaluated with combined oxalate–pyroantimonate technique. Acta Histochem. 24, 327–333.
![](../../media/share/OpenURL_Image.gif)
Canipari, R. , Epifano, O. , Siracusa, G. , and Salustri, A. (1995). Mouse oocytes inhibit plasminogen activator production by ovarian cumulus and granulosa cells. Dev. Biol. 167, 371–378.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Carnegie, J. A. , and Tsang, B. K. (1984). The calcium–calmodulin system: participation in the regulation of steroidogenesis at different stages of granulosa cell differentiation. Biol. Reprod. 30, 515–522.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Carroll, J. , Swann, K. , Whittingham, D. , and Whitaker, W. (1994). Spatiotemporal dynamics of intracellular (Ca2+)(i) oscillations during the growth and meiotic maturation of mouse oocytes. Development 120, 3507–3517.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Chesnel, F. , Wigglesworth, K. , and Eppig, J. J. (1994). Acquisition of meiotic competence by denuded mouse oocytes: participation of somatic-cell product(s) and cAMP. Dev. Biol. 161, 285–295.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Collona, R. , Cecconi, S. , Tatone, C. , Mangia, F. , and Buccione, R. (1989). Somatic cell–oocyte interactions in mouse oogenesis: stage-specific regulation of mouse oocyte protein phosphorylation by granulosa cells. Dev. Biol. 133, 305–308.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Dong, J. W. , Albertini, D. F. , Nishimori, K. , Kumar, T. R. , Lu, N. F. , and Matzuk, M. M. (1996). Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature 383, 531–535.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Eppig, J. J. , Schultz, R. M. , O’Brien, M. , and Chesnel, F. (1994). Relationships between the developmental programs controlling nuclear and cytoplasmic maturation in mouse oocytes. Dev. Biol. 164, 1–9.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Eppig, J. J. , O’Brien, M. , and Wigglesworth, K. (1996). Mammalian oocyte growth and development. Mol. Reprod. Dev. 44, 260–273.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Franchi, E. , and Camatini, M. (1985). Morphological evidence for calcium stores at Sertoli–Sertoli and Sertoli–spermatid interrelations. Cell Biol. Int. Rep. 9, 441–446.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Gilchrist, J. S. , Czubryt, M. P. , and Pierce, G. N. (1994). Calcium and calcium-binding proteins in the nucleus. Mol. Cell. Biochem. 135, 79–88.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Gomes, J. E. , Pesty, A. , Gouveia-Oliveira, A. , Cidadao, A. J. , Plancha, C. E. , and Lefevre, B. (1999). Age and gonadotropins control Ca2+-spike acquisition in mouse oocytes isolated from early preantral follicles. Int. J. Dev. Biol. 43, 839–842.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Greenwald, G. S. and Terranova, P. F. (1988). Follicular selection and its control. In
Gunter, K. K. , and Gunter, T. E. (1994). Transport of calcium by mitochondria. J. Bioenerg. Biomembr. 26, 471–485.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Han, J. K. , and Nuccitelli, R. (1990). Inositol 1,4,5-trisphosphate induced calcium release in the organelle layers of the stratified, intact egg of Xenopus laevis. J. Cell Biol. 110, 1103–1110.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Himpens, B. , de Smedt, H. , and Casteels, R. (1994). Relationship between (Ca2+) changes in nucleus and cytosol. Cell Calcium 16, 239–246.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Homa, S. T. , Carroll, J. , and Swan, K. (1993). The role of calcium in mammalian oocyte maturation and egg activation. Hum. Reprod. 8, 1274–1281.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Jayes, F. C. L. , Day, R. N. , Garmey, J. C. , Urban, R. J. , Zhang, G. , and Veldhuis, J. D. (2000). Calcium ions positively modulate follicle stimulating hormone- and exogenous cyclic 3′,5′-adenosine monophosphate-driven transcription of P450(scc) gene in porcine granulosa cells. Endocrinology 141, 2377–2384.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Jouaville, L. S. , Chas, F. , Holmuhamedov, E. L. , Camacho, P. , and Lechleiter, J. D. (1995). Synchronization of calcium waves by mitochondrial substrates in Xenopus laevis oocytes. Nature 377, 438–441.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Joyce, I. M. , Pendola, F. L. , Wigglesworth, K. , and Eppig, J. J. (1999). Oocyte regulation of kit ligand expression in mouse ovarian follicles. Dev. Biol. 214, 342–353.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Kline, D. (2000). Attributes and dynamics of the endoplasmic reticulum in mammalian eggs. Curr. Top. Dev. Biol. 50, 125–154.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Lebedeva, I. Y. , Denisenko, V. Y. , Lebedev, V. A. , and Kuzmina, T. I. (1998). Prolactin in follicular fluid and intracellular store calcium in follicular cells are related to morphological signs of ovarian follicle atresia in cows: work in progress. Theriogenology 49, 509–519.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Lefevre, B. , Nagyová, E. , Pesty, A. , and Testart, J. (1997). Acquisition of meiotic competence is related to the functionality of the phosphoinositide/calcium signalling pathway in the mouse oocyte. Exp. Cell Res. 236, 193–200.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Liu, L. , Hammar, K. , Smith, P. J. S. , Inoue, S. , and Keefe, D. L. (2001). Mitochondrial modulation of calcium signalling at the initiation of development. Cell Calcium 30, 423–433.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Mattioli, M. , Barboni, B. , and Seren, E. (1991). Luteinizing-hormone inhibits potassium outward currents in swine granulosa-cells by intracellular calcium mobilization. Endocrinology 129, 2740–2743.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Menon, G. K. , Grayson, S. , and Elias, P. M. (1985). Ionic calcium reservoirs in mammalian epidermis, ultrastructural localisation by ion-capture cytochemistry. J. Invest. Dermatol. 84, 508–512.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Moore, G. P. M. , Lintern-Moore, S. , Peters, H. , and Faber, M. (1974). RNA synthesis in mouse oocyte. J. Cell Biol. 60, 416–422.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Nicotera, P. , Zhivotovsky, B. , and Orrenius, S. (1994). Nuclear calcium transport and the role of calcium in apoptosis. Cell Calcium 16, 279–288.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Petr, J. , Rozinek, J. , and Jílek, F. (1997). Cyclopiazonic acid induces accelerated progress of meiosis in pig oocytes. Zygote 5, 193–205.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Petr, J. , Rozinek, J. , Vaňourková, Z. , and Jílek, F. (1999). Cyclopiazonic acid, an inhibitor of calcium-dependent ATPases, induces exit from metaphase I arrest in growing pig oocytes. Reprod. Fertil. Dev. 11, 235–246.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Petr, J. , Rozinek, J. , Jílek, F. , and Urbánková, D. (2000). Activation of porcine oocytes using cyclopiazonic acid, an inhibitor of calcium-dependent ATPases. J. Exp. Zool. 287, 304–315.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Petr, J. , Rozinek, J. , Hruban, V. , Jílek, F. , Sedmíková, M. , Vaňourková, Z. , and Němeček, Z. (2001). Ultrastructural localization of calcium deposits during in vitro culture of pig oocytes. Mol. Reprod. Dev. 58, 196–204.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Poenie, M. , and Epel, D. (1987). Ultrastructural localization of intracellular calcium stores by a new cytochemical method. J. Histochem. Cytochem. 35, 939–959.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Ravindranath, N. , Papadopoulos, V. , Vornberger, W. , Zitzmann, D. , and Dym, M. (1994). Ultrastructural distribution of calcium in the rat testis. Biol. Reprod. 51, 50–62.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
SAS Institute Inc. (2001).
Sorensen, R. A. , and Wassarman, P. M. (1976). Relationship between growth and meiotic maturation of the mouse oocyte. Dev. Biol. 50, 531–536.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Sousa, M. , and Azevedo, C. (1989). Ultrastructural localization of calcium in the acrosome and jelly coat of starfish gametes. Dev. Growth Differ. 31, 227–232.
![](../../media/share/OpenURL_Image.gif)
Sousa, M. , Barros, A. , Silva, J. , and Tesarik, J. (1997). Developmental changes in calcium content of ultrastructurally distinct subcellular compartments of preimplantation human embryos. Mol. Hum. Reprod. 3, 83–90.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Szybek, K. (1972). In vitro maturation of oocytes from sexually immature mice. J. Endocrinol. 54, 527–528.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Terasaki, M. , and Sardet, C. (1991). Demonstration of calcium uptake and release by sea urchin egg cortical endoplasmic reticulum. J. Cell Biol. 115, 1031–1037.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Tirone, E. , D’Allesandris, C. , Hascall, V. C. , Siracusa, G. , and Salustri, A. (1997). Hyaluronan synthesis by mouse cumulus cell is regulated by interaction between follicle-stimulating hormone (or epidermal growth factor) and soluble oocyte factor (or transforming growth factor β1). J. Biol. Chem. 272, 4787–4794.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Tsafriri, A. , and Channing, C. P. (1975). An inhibitory influence of granulosa cells and follicular fluid upon oocyte meiosis in vitro. Endocrinology 96, 922–927.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Vanderhyden, B. C. , Caron, P. J. , Buccione, R. , and Eppig, J. J. (1990). Developmental pattern of the secretion of cumulus expansion-enabling factor by mouse oocytes and the role of oocytes in promoting granulosa cell differentiation. Dev. Biol. 140, 307–317.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Vanderhyden, B. C. , Telfer, E. E. , and Eppig, J. J. (1992). Mouse oocytes promote proliferation of granulosa cells from preantral and antral follicles in vitro. Biol. Reprod. 46, 1196–1204.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Vanderhyden, B. C. , Cohen, J. N. , and Morley, P. (1993). Mouse oocytes regulate granulosa cell steroidogenesis. Endocrinology 133, 423–426.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Van Reempts, J. , Borgers, M. , and Offner, F. (1982). Ultrastructural localization of calcium in the rat retina with a combined oxalate–pyroantimonate technique. Histochem. J. 14, 517–522.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Wassarman, P. M. (1988). The mammalian ovum. In
Wick, S. M. , and Hepler, P. K. (1982). Selective localization of intracellular Ca2+ with potassium pyroantimonate. J. Histochem. Cytochem. 30, 1190–1204.
| PubMed |
![](../../media/share/OpenURL_Image.gif)