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Ultrastructural Localization of Intracellular Calcium During Spermatogenesis of Sterlet (Acipenser ruthenus)

Published online by Cambridge University Press:  21 November 2016

Amin Golpour*
Affiliation:
University of South Bohemia in České Budějovice, Faculty of Fisheries and Protection of Waters, South Bohemian Research Center of Aquaculture and Biodiversity of Hydrocenoses, Research Institute of Fish Culture and Hydrobiology, Zátiší 728/II, 389 25 Vodňany, Czech Republic
Martin Pšenička
Affiliation:
University of South Bohemia in České Budějovice, Faculty of Fisheries and Protection of Waters, South Bohemian Research Center of Aquaculture and Biodiversity of Hydrocenoses, Research Institute of Fish Culture and Hydrobiology, Zátiší 728/II, 389 25 Vodňany, Czech Republic
Hamid Niksirat*
Affiliation:
University of South Bohemia in České Budějovice, Faculty of Fisheries and Protection of Waters, South Bohemian Research Center of Aquaculture and Biodiversity of Hydrocenoses, Research Institute of Fish Culture and Hydrobiology, Zátiší 728/II, 389 25 Vodňany, Czech Republic
*
*Corresponding authors. [email protected]; [email protected]
*Corresponding authors. [email protected]; [email protected]
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Abstract

Calcium regulates many intracellular events such as growth and differentiation during different stages of gamete development. The aim of this study was to localize and quantify the intracellular distribution of calcium during different developmental stages of spermatogenesis in sterlet, Acipenser ruthenus, using a combined oxalate–pyroantimonate technique. The distribution of calcium was described in spermatogonium, spermatocyte, spermatid, and spermatozoon stages. In the spermatogonium and spermatocyte, calcium deposits were mainly localized in the nucleus and cytoplasm. The spermatid had calcium in the nucleus, developing acrosomal vesicle, and cytoplasm. Intracellular calcium transformed from scattered deposits in spermatogonia and spermatocyte stages into an unbound form in spermatid and the spermatozoon. The proportion of area covered by calcium increased significantly (p<0.05) from early to late stages of spermatogenesis. The largest proportion of area covered by calcium was observed in the nucleus of the spermatozoon. In conclusion, although most of the intracellular calcium is deposited in limited areas of the spermatogonium and spermatocyte, it is present an unbound form in the larger area of spermatids and spermatozoa which probably reflects changes in its physiological function and homeostasis during the process of male gamete production in spermatogenesis.

Type
Biological Applications
Copyright
© Microscopy Society of America 2016 

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References

Amemiya, K., Hirabayashi, M., Ishikawa, H., Fukui, Y. & Hochi, S. (2007). The ability of whale haploid spermatogenic cells to induce calcium oscillations and its relevance to oocyte activation. Zygote 15, 103108.Google Scholar
Biagi, F., Piras, F., Farina, V., Zedda, M., Mura, E., Floris, A., Franzoi, P., Fausto, A.M., Taddei, A.R. & Carcupino, M. (2015). Testis structure, spermatogenesis and sperm morphology in pipefishes of the genus Syngnathus . Acta Zool 97, 90101.Google Scholar
Boutinard Roueue-Rosier, V., Biggiogera, M. & Fakan, S. (1993). Ultrastructural detection of calcium and magnesium in the chromatoid body of mouse spermatids by electron spectroscopic imaging and electron energy loss spectroscopy. J Histochem Cytochem 41, 11551162.Google Scholar
Breitbart, H. (2002). Intracellular calcium regulation in sperm capacitation and acrosomal reaction. Mol Cell Endocrinol 187, 139144.Google Scholar
Chiarella, P., Puglisi, R., Sorrentino, V., Boitani, C. & Stefanini, M. (2004). Ryanodine receptors are expressed and functionally active in mouse spermatogenic cells and their inhibition interferes with spermatogonial differentiation. J Cell Sci 117, 41274134.Google Scholar
Dan, J.C. (1956). The acrosome reaction. Int Rev Cytol 5, 365393.Google Scholar
Darszon, A., Labarca, P., Nishigaki, T. & Espinosa, F. (1999). Ion channels in sperm physiology. Physiol Rev 79, 481510.Google Scholar
Feng, H.L., Hershlag, A., Han, Y.B. & Zheng, L.J. (2006). Localizations of intracellular calcium and Ca2+-ATPase in hamster spermatogenic cells and spermatozoa. Microsc Res Tech 69, 618623.Google Scholar
Feng, H.L., Han, Y.B., Hershlag, A. & Zheng, L.J. (2007). Impact of Ca2+ flux inhibitors on acrosome reaction of hamster spermatozoa. J Androl 28, 561564.Google Scholar
Forer, A., Gupta, B.L. & Hall, T.A. (1980). Electron probe X-ray microanalysis of calcium and other elements in meiotic spindles, in frozen sections of spermatocytes from crane fly testes. Exp Cell Res 126, 217226.Google Scholar
Ghanayem, B.I. & Chapin, R.E. (1990). Calcium channel blockers protect against ethylene glycol monomethyl ether (2-methoxyethanol)-induced testicular toxicity. Exp Mol Pathol 52, 279290.Google Scholar
Golpour, A., Pšenička, M. & Niksirat, H. (2016). Subcellular localization of calcium deposits during zebrafish (Danio rerio) oogenesis. Micron 80, 613.Google Scholar
Hagiwara, S. & Kawa, K. (1984). Calcium and potassium currents in spermatogenic cells dissociated from rat seminiferous tubules. J Physiol 356, 135149.Google Scholar
Lee, J.H., Ahn, H.J., Lee, S.J., Gye, M.C. & Min, C.K. (2011). Effects of L- and T-type Ca2+ channel blockers on spermatogenesis and steroidogenesis in the prepubertal mouse testis. J Assist Reprod Genet 28, 2330.Google Scholar
Li, P., Nijhawan, D., Budihardjo, I., Srinivasula, S.M., Ahmad, M., Alnemri, E.S. & Wang, X. (1997). Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91, 479489.Google Scholar
Lizama, C., Alfaro, I., Reyes, J.G. & Moreno, R.D. (2007). Up-regulation of CD95 (Apo-1/Fas) is associated with spermatocyte apoptosis during the first round spermatogenesis in the rat. Apoptosis 12, 499512.Google Scholar
Mattei, X. (1991). Spermatozoon ultrastructure and its systematic implications in fishes. Can J Zool 69, 30383055.Google Scholar
Means, A.R. & Rasmussen, C.D. (1988). Calcium, calmodulin, and cell proliferation. Cell Calcium 9, 313319.Google Scholar
Mojazi Amiri, B. & Takahashi, H. (2006). Fine structure of spermatogenesis in a hybrid sturgeon, bester (Huso huso female x Acipenser ruthenus male). J Appl Ichthyol 22, 406410.Google Scholar
Nakamura, M., Moriya, M., Baba, T., Michikawa, Y., Yamanobe, T., Arai, K., Okinaga, S. & Kobayashi, T. (1993). An endoplasmic reticulum protein, calreticulin, is transported into the acrosome of rat sperm. Exp Cell Res 205, 101110.Google Scholar
Nijima, L. & Dan, J. (1985). The acrosome reaction in mytilus edulis. J Cell Biol 5, 243248.Google Scholar
Niksirat, H., Kouba, A. & Kozák, P. (2015). Ultrastructure of egg activation and cortical reaction in the noble crayfish Astacus astacus . Micron 68, 115121.Google Scholar
Niksirat, H. & Kouba, A. (2016). Subcellular localization of calcium deposits in the noble crayfish Astacus astacus spermatophore: implications for post‐mating spermatophore hardening and spermatozoon maturation. J Morphol 277, 445452.Google Scholar
Petr, J., Rozinek, J., Hruban, V., Jiâlek, F., Sedmiâkovâ, M., Vanourkovâ, Z. & Nemecek, Z. (2001). Ultrastructural localization of calcium deposits during in vitro culture of pig oocytes. Mol Reprod Dev 58, 196204.Google Scholar
Pšenička, M., Vancová, M., Koubek, P., Těšitel, J. & Linhart, O. (2009). Fine structure and morphology of sterlet (Acipenser ruthenus L. 1758) spermatozoa and acrosin localization. Anim Reprod Sci 111, 316.Google Scholar
Ravindranath, N., Papadopoulos, V., Vornberger, W., Zitzmann, D. & Dym, M. (1994). Ultrastructural distribution of calcium in the rat testis. Biol Reprod 51, 5062.Google Scholar
Rozinek, J., Rajmon, R., Petr, J., Rohlik, J., Jeseta, M., Sedmikova, M., Rehak, D. & Jilek, F. (2006). Ultrastructural localization of calcium deposits in pig ovarian follicles. Anim Reprod Sci 91, 123132.Google Scholar
Sakata, Y., Saegusa, H., Zong, S., Osanai, M., Murakoshi, T., Shimizu, Y., Noda, T., Aso, T. & Tanabe, T. (2002). Cav2.3 (ɑ1E) Ca2+ channel participates in the control of sperm function. FEBS Lett 516, 229233.Google Scholar
Santi, C.M., Darszon, A. & Hernandez-Cruz, A. (1996). A dihydropyridine-sensitive T-type Ca2+ current is the main Ca2+ current carrier in mouse primary spermatocytes. Am J Physiol 271, C1583C1593.Google Scholar
Santi, C.M., Santos, T., Hernandez, A. & Darszon, A. (1998). Properties of a novel pH-dependent Ca+2 permeation pathway present in male germ cells with possible roles in spermatogenesis and mouse sperm function. J Gen Physiol 112, 3353.Google Scholar
Schulz, R.W., Franca, L.R., Lareyre, J.J., Legac, F., Chiarini-Garcia, H., Nobrega, R.H. & Miura, T. (2010). Spermatogenesis in fish. Gen Comp Endocrinol 165, 390411.CrossRefGoogle ScholarPubMed
Sedmiâkovâ, M., Rajmon, R., Petr, J., Vancová, M., Rozinek, J., Rehak, D. & Jilek, F. (2003). Ultrastructural localization of calcium deposits in the mouse ovary. Reprod Fertil Dev 15, 415422.Google Scholar
Serranoa, J.R., Perez-Reyesb, E. & Stephen, W. (1999). Jones state-dependent inactivation of the α1g T-type calcium channel. J Gen Physiol 114, 185202.Google Scholar
Sokolov, L.I. & Vasilev, V.P. (1989). Acipenser ruthenus Linneaus 1758. In The Freshwater Fishes of Europe. General Introduction to Fishes, Acipenseriformes, Holcik, J. (Ed.), pp. 227–262. Wiesbaden: ATULA-Verlag.Google Scholar
Spungin, B. & Breitbart, H. (1996). Calcium mobilization and influx during sperm exocytosis. J Cell Sci 109, 19471955.Google Scholar
Stricker, S.A. (1999). Comparative biology of calcium signaling during fertilization and egg activation in animals. Dev Biol 211, 157176.Google Scholar
Suarez, S.S. & Ho, H.C. (2003). Hyperactivated motility in sperm. Reprod Domest Anim 38, 119124.Google Scholar
Talbot, P., Summers, R.G., Hylander, B.L., Keough, E.M. & Franklin, L.E. (1976). The role of calcium in the acrosome reaction: an analysis using Ionophore A231.87. J Exp Zool 198, 383392.CrossRefGoogle Scholar
Treviño, C.L., Santi, C.M., Beltrán, C., Hernández-Cruz, A., Darszon, A. & Lomeli, H. (1998). Localization of inositol trisphosphate and ryanodine receptors during mouse spermatogenesis: possible functional implications. Zygote 6, 159172.Google Scholar
Walensky, L.D. & Snyder, S.H. (1995). Inositol 1, 4, 5-trisphosphate receptors selectively localized to the acrosomes of mammalian sperm. J Cell Biol 130, 857869.Google Scholar
Williot, P., Sabeau, L., Gessner, J., Arlati, G., Bronzi, P., Gulyas, T. & Berni, P. (2001). Sturgeon farming in Western Europe: recent developments and perspectives. Aquat Living Res 14, 367374.Google Scholar