Role of Ca2+ in the IVM of spermatozoa from the sterlet Acipenser ruthenus
Olga Bondarenko A B , Borys Dzyuba A , Marek Rodina A and Jacky Cosson A
+ Author Affiliations
- Author Affiliations
A Faculty of Fisheries and Protection of Waters, University of South Bohemia in Ceske Budejovice, South Bohemian Research Center of Aquaculture and Biodiversity of Hydrocenoses, Zátiší 728/II, 389 25, Vodňany, Czech Republic.
B Corresponding author. Email: obondarenko@frov.jcu.cz
Reproduction, Fertility and Development 29(7) 1319-1328 https://doi.org/10.1071/RD16145
Submitted: 30 June 2015 Accepted: 20 April 2016 Published: 1 June 2016
Abstract
The role of Ca2+ in sturgeon sperm maturation and motility was investigated. Sperm from mature male sterlets (Acipenser ruthenus) were collected from the Wolffian duct and testis 24 h after hormone induction. Testicular spermatozoa (TS) were incubated in Wolffian duct seminal fluid (WDSF) for 5 min at 20°C and were designated ‘TS after IVM’ (TSM). Sperm motility was activated in media with different ion compositions, with motility parameters analysed from standard video microscopy records. To investigate the role of calcium transport in the IVM process, IVM was performed (5 min at 20°C) in the presence of 2 mM EGTA, 100 µM Verapamil or 100 µM Tetracaine. No motility was observed in the case of TS (10 mM Tris, 25 mM NaCl, 50 mM Sucr with or without the addition of 2 mM EGTA). Both incubation of TS in WDSF and supplementation of the activation medium with Ca2+ led to sperm motility. The minimal Ca2+ concentration required for motility activation of Wolffian duct spermatozoa, TS and TSM was determined (1–2 nM for Wolffian duct spermatozoa and TSM; approximately 0.6 mM for TS). Motility was obtained after the addition of verapamil to the incubation medium during IVM, whereas the addition of EGTA completely suppressed motility, implying Ca2+ involvement in sturgeon sperm maturation. Further studies into the roles of Ca2+ transport in sturgeon sperm maturation and motility are required.
Additional keywords: ion transport, Na+, sperm maturation, sperm motility.
References
Abbott, B. J., Fukuda, D. S., Dorman, D. E., Occolowitz, J. L., Debono, M., and Farhner, L. (1979). Microbial transformation of A23187, a divalent-cation ionophore antibiotic. Antimicrob. Agents Chemother. 16, 808–812.| Microbial transformation of A23187, a divalent-cation ionophore antibiotic.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXks1ymtbY%3D&md5=fe81ab2b396727f7bb0cc41310e998e8CAS | 119484PubMed |
Alavi, S. M. H., and Cosson, J. (2006). Sperm motility in fishes. (II) Effects of ions and osmolality: a review. Cell Biol. Int. 30, 1–14.
| Sperm motility in fishes. (II) Effects of ions and osmolality: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhsF2ntr8%3D&md5=a72db912a85ae47d208092432d630211CAS |
Alavi, S. M., Cosson, J., Karami, M., Amiri, B. M., and Akhoundzadeh, M. A. (2004). Spermatozoa motility in the Persian sturgeon, Acipenser persicus: effects of pH, dilution rate, ions and osmolality. Reproduction 128, 819–828.
| Spermatozoa motility in the Persian sturgeon, Acipenser persicus: effects of pH, dilution rate, ions and osmolality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFSqsA%3D%3D&md5=08156c45d69f1ec328581904a2a1306aCAS | 15579600PubMed |
Alavi, S. M. H., Gela, D., Rodina, M., and Linhart, O. (2011). Roles of osmolality, calcium–potassium antagonist and calcium in activation and flagellar beating pattern of sturgeon sperm. Comp. Biochem. Physiol., Part A Mol. Integr. Physiol. 160, 166–174.
| Roles of osmolality, calcium–potassium antagonist and calcium in activation and flagellar beating pattern of sturgeon sperm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXpsFaku7o%3D&md5=f16f2f8d4e402dceefdc410cabf6aefbCAS |
Almog, T., and Naor, Z. (2008). Mitogen activated protein kinases (MAPKs) as regulators of spermatogenesis and spermatozoa functions. Mol. Cell. Endocrinol. 282, 39–44.
| Mitogen activated protein kinases (MAPKs) as regulators of spermatogenesis and spermatozoa functions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXitVegt7c%3D&md5=00a5c0be0f62501f40efa5d5d659a81dCAS | 18177996PubMed |
Almog, T., and Naor, Z. (2010). The role of mitogen activated protein kinase (MAPK) in sperm functions. Mol. Cell. Endocrinol. 314, 239–243.
| The role of mitogen activated protein kinase (MAPK) in sperm functions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFynurbJ&md5=afe2f7c256949eb21c0eca3e8fc3df1eCAS | 19467295PubMed |
Ardón, F., Rodríguez-Miranda, E., Beltrán, C., Hernández-Cruz, A., and Darszon, A. (2009). Mitochondrial inhibitors activate influx of external Ca2+ in sea urchin sperm. Biochim. Biophys. Acta 1787, 15–24.
| Mitochondrial inhibitors activate influx of external Ca2+ in sea urchin sperm.Crossref | GoogleScholarGoogle Scholar | 19000650PubMed |
Bading, H., and Greenberg, M. E. (1991). Stimulation of protein tyrosine phosphorylation by NMDA receptor activation. Science 253, 912–914.
| Stimulation of protein tyrosine phosphorylation by NMDA receptor activation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXlsFWmt7Y%3D&md5=82d6231c1ee28f7ffa64112dcc8826f2CAS | 1715095PubMed |
Baynes, S. M., Scott, A. P., and Dawson, A. P. (1981). Rainbow-trout, Salmo-Gairdnerii Richardson, spermatozoa: effects of cations and pH on motility. J. Fish Biol. 19, 259–267.
| Rainbow-trout, Salmo-Gairdnerii Richardson, spermatozoa: effects of cations and pH on motility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXls1Gqu7Y%3D&md5=30ccc6cece0e48f3941d8a906dd905e6CAS |
Boitano, S., and Omoto, C. K. (1992). Trout sperm swimming patterns and role of intracellular Ca2+. Cell Motil. Cytoskeleton 21, 74–82.
| Trout sperm swimming patterns and role of intracellular Ca2+.Crossref | GoogleScholarGoogle Scholar |
Bondarenko, O., Dzyuba, B., Cosson, J., Rodina, M., and Linhart, O. (2014). The role of Ca2+ and Na+ membrane transport in brook trout (Salvelinus fontinalis) spermatozoa motility. Fish Physiol. Biochem. 40, 1417–1421.
| The role of Ca2+ and Na+ membrane transport in brook trout (Salvelinus fontinalis) spermatozoa motility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXmt1WksLc%3D&md5=46c133fc5b59baa0b6de47c46748fef3CAS | 24718964PubMed |
Bordin, S., Carneiro, E. M., Bosqueiro, J. R., and Boschero, A. C. (1997). Tetracaine stimulates extracellular Ca2+-independent insulin release. Eur. J. Pharmacol. 327, 257–262.
| Tetracaine stimulates extracellular Ca2+-independent insulin release.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjtlWnt78%3D&md5=8c064bc0aff5e34211fb456e4b06e926CAS | 9200568PubMed |
Breitbart, H. (2002). Intracellular calcium regulation in sperm capacitation and acrosomal reaction. Mol. Cell. Endocrinol. 187, 139–144.
| Intracellular calcium regulation in sperm capacitation and acrosomal reaction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xjt1Sqtr8%3D&md5=427344ca3a97691742760aff7ff30b02CAS | 11988321PubMed |
Butler, D. M., Allen, K. M., Garrett, F. E., Lauzon, L. L., Lotfizadeh, A., and Koch, R. A. (1999). Release of Ca2+ from intracellular stores and entry of extracellular Ca2+ are involved in sea squirt sperm activation. Dev. Biol. 215, 453–464.
| Release of Ca2+ from intracellular stores and entry of extracellular Ca2+ are involved in sea squirt sperm activation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmvFyrtLc%3D&md5=10db00045f291f25020532d86ee12f58CAS | 10545251PubMed |
Cosson, J. (2004). The ionic and osmotic factors controlling motility of fish spermatozoa. Aquacult. Int. 12, 69–85.
| The ionic and osmotic factors controlling motility of fish spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhsFSjsro%3D&md5=c0d2394fb792398e51b5bacc74118fe8CAS |
Cosson, M. P., Billard, R., and Letellier, L. (1989). Rise of internal Ca2+ accompanies the initiation of trout sperm motility. Cell Motil. Cytoskeleton 14, 424–434.
| Rise of internal Ca2+ accompanies the initiation of trout sperm motility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXhvFWgug%3D%3D&md5=24739ad9ef8bfb7d11524343555b57e8CAS |
Cosson, M. P., Cosson, J., and Billard, R. (1991). Synchronous triggering of trout sperm is followed by an invariable set sequence of movement parameters whatever the incubation medium. Cell Motil. Cytoskeleton 20, 55–68.
| Synchronous triggering of trout sperm is followed by an invariable set sequence of movement parameters whatever the incubation medium.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK38%2Fpslajuw%3D%3D&md5=aaeb43b3181363799f496d7e87930597CAS | 1756578PubMed |
Costello, S., Michelangeli, F., Nash, K., Lefievre, L., Morris, J., Machado-Oliveira, G., Barratt, C., Kirkman-Brown, J., and Publicover, S. (2009). Ca2+-stores in sperm: their identities and functions. Reproduction 138, 425–437.
| Ca2+-stores in sperm: their identities and functions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFOgtrvM&md5=ddd9092d16372731abaf66e0074a19a8CAS | 19542252PubMed |
Darszon, A., Beltran, C., Felix, R., Nishigaki, T., and Trevino, C. L. (2001). Ion transport in sperm signaling. Dev. Biol. 240, 1–14.
| Ion transport in sperm signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXptFegtr4%3D&md5=515fd15fac4ee0598c1a9a9d12fd1653CAS | 11784043PubMed |
Darszon, A., Nishigaki, T., Beltran, C., and Trevino, C. L. (2011). Calcium channels in the development, maturation, and function of spermatozoa. Physiol. Rev. 91, 1305–1355.
| Calcium channels in the development, maturation, and function of spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsVOjsbrK&md5=45a970587eb7e74c15f7d2999c383801CAS | 22013213PubMed |
Dragileva, E., Rubinstein, S., and Breitbart, H. (1999). Intracellular Ca2+–Mg2+-ATPase regulates calcium influx and acrosomal exocytosis in bull and ram spermatozoa. Biol. Reprod. 61, 1226–1234.
| Intracellular Ca2+–Mg2+-ATPase regulates calcium influx and acrosomal exocytosis in bull and ram spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmvFertrs%3D&md5=090a84560a73195ec77d4c01c1202c93CAS | 10529268PubMed |
Dzyuba, B., Boryshpolets, S., Cosson, J., Dzyuba, V., Fedorov, P., Saito, T., Psenicka, M., Linhart, O., and Rodina, M. (2014a). Motility and fertilization ability of sterlet Acipenser ruthenus testicular sperm after cryopreservation. Cryobiology 69, 339–341.
| Motility and fertilization ability of sterlet Acipenser ruthenus testicular sperm after cryopreservation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2cbltl2huw%3D%3D&md5=2d9252d4a33dc150d1135e006946d612CAS | 25058859PubMed |
Dzyuba, B., Cosson, J., Boryshpolets, S., Bondarenko, O., Dzyuba, V., Prokopchuk, G., Gazo, I., Rodina, M., and Linhart, O. (2014b). In vitro sperm maturation in sterlet, Acipenser ruthenus. Reprod. Biol. 14, 160–163.
| In vitro sperm maturation in sterlet, Acipenser ruthenus.Crossref | GoogleScholarGoogle Scholar | 24856476PubMed |
Fiore, R. S., Murphy, T. H., Sanghera, J. S., Pelech, S. L., and Baraban, J. M. (1993). Activation of p42 mitogen-activated protein kinase by glutamate receptor stimulation in rat primary cortical cultures. J. Neurochem. 61, 1626–1633.
| Activation of p42 mitogen-activated protein kinase by glutamate receptor stimulation in rat primary cortical cultures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXhtFGl&md5=9eb678c09fc47039ba776ee24873b160CAS | 7693864PubMed |
Fox, A. P., Nowycky, M. C., and Tsien, R. W. (1987). Single-channel recordings of three types of calcium channels in chick sensory neurones. J. Physiol. 394, 173–200.
| Single-channel recordings of three types of calcium channels in chick sensory neurones.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1c7nt1Wqug%3D%3D&md5=6e8429fb18955dbd78ec821a57b7fb77CAS | 2451017PubMed |
Fraser, L. R. (1998). Sperm capacitation and the acrosome reaction. Hum. Reprod. 13, 9–19.
| Sperm capacitation and the acrosome reaction.Crossref | GoogleScholarGoogle Scholar | 9663766PubMed |
Hatef, A., Alavi, S. M. H., Rodina, M., and Linhart, O. (2012). Morphology and fine structure of the Russian sturgeon, Acipenser gueldenstaedtii (Acipenseridae, Chondrostei) spermatozoa. J. Appl. Ichthyol. 28, 978–983.
| Morphology and fine structure of the Russian sturgeon, Acipenser gueldenstaedtii (Acipenseridae, Chondrostei) spermatozoa.Crossref | GoogleScholarGoogle Scholar |
Hayashi, H., Yamamoto, K., Yonekawa, H., and Morisawa, M. (1987). Involvement of tyrosine protein kinase in the initiation of flagellar movement in rainbow trout spermatozoa. J. Biol. Chem. 262, 16 692–16 698.
| 1:CAS:528:DyaL2sXlvFensrw%3D&md5=86998806cadf30cfe8267ca1577d3b3eCAS |
Herrick, S. B., Schweissinger, D. L., Kim, S. W., Bayan, K. R., Mann, S., and Cardullo, R. A. (2005). The acrosomal vesicle of mouse sperm is a calcium store. J. Cell. Physiol. 202, 663–671.
| The acrosomal vesicle of mouse sperm is a calcium store.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFOntb4%3D&md5=11fb8d64bfa1843fa1500ea3decb9df6CAS | 15389568PubMed |
Hille, B. (1991). ‘Ionic channels of excitable membranes. Second edition.’ (Sinauer: Sunderland, MA.)
Ho, H. C., and Suarez, S. S. (2001). An inositol 1,4,5-trisphosphate receptor-gated intracellular Ca2+ store is involved in regulating sperm hyperactivated motility. Biol. Reprod. 65, 1606–1615.
| An inositol 1,4,5-trisphosphate receptor-gated intracellular Ca2+ store is involved in regulating sperm hyperactivated motility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnvVersb0%3D&md5=8766b0703c2c071d3f65bead454213b0CAS | 11673282PubMed |
Ho, H. C., and Suarez, S. S. (2003). Characterization of the intracellular calcium store at the base of the sperm flagellum that regulates hyperactivated motility. Biol. Reprod. 68, 1590–1596.
| Characterization of the intracellular calcium store at the base of the sperm flagellum that regulates hyperactivated motility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjt12lsbY%3D&md5=94cd6d625c56149a4b3b8bc0765846a0CAS | 12606347PubMed |
Huang, J. Y., Wang, G. L., and Kong, L. J. (2009). Effects of Ca2+ and HCO3– on capacitation, hyperactivation and protein tyrosine phosphorylation in guinea pig spermatozoa. Asian-Australas. J. Anim. Sci. 22, 181–186.
| Effects of Ca2+ and HCO3– on capacitation, hyperactivation and protein tyrosine phosphorylation in guinea pig spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjsF2hsbc%3D&md5=4a9f1f17e5f3307e2a6860ff18e32ac5CAS |
Ishii, T. M., Silvia, C., Hirschberg, B., Bond, C. T., Adelman, J. P., and Maylie, J. (1997). A human intermediate conductance calcium-activated potassium channel. Proc. Natl Acad. Sci. USA 94, 11 651–11 656.
| A human intermediate conductance calcium-activated potassium channel.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXmslejt78%3D&md5=9c5052c2aa57738380d14577c088ef11CAS |
Ishikawa, M., Tsutsui, H., Cosson, J., Oka, Y., and Morisawa, M. (2004). Strategies for sperm chemotaxis in the siphonophores and ascidians: a numerical simulation study. Biol. Bull. 206, 95–102.
| Strategies for sperm chemotaxis in the siphonophores and ascidians: a numerical simulation study.Crossref | GoogleScholarGoogle Scholar | 15111364PubMed |
Kansha, M., Nagata, T., Irita, K., and Takahashi, S. (1999). Dibucaine and tetracaine inhibit the activation of mitogen-activated protein kinase mediated by L-type calcium channels in PC12 cells. Anesthesiology 91, 1798–1806.
| 1:CAS:528:DC%2BD3cXivFKntw%3D%3D&md5=f95a1a10a1904189b9dbdfab1c89afeeCAS | 10598624PubMed |
Kharatmal, S. B., Singh, J. N., and Sharma, S. S. (2015). Voltage-gated sodium channels as therapeutic targets for treatment of painful diabetic neuropathy. Mini Rev. Med. Chem. 15, 1134–1147.
| Voltage-gated sodium channels as therapeutic targets for treatment of painful diabetic neuropathy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhs1Ont7nO&md5=ad0ffcb0d493b3423b02c39cff0c9c2eCAS | 26202189PubMed |
Kho, K. H., Tanimoto, S., Inaba, K., Oka, Y., and Morisawa, M. (2001). Transmembrane cell signaling for the initiation of trout sperm motility: roles of ion channels and membrane hyperpolarization for cyclic AMP synthesis. Zoolog. Sci. 18, 919–928.
| Transmembrane cell signaling for the initiation of trout sperm motility: roles of ion channels and membrane hyperpolarization for cyclic AMP synthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXptVegs7c%3D&md5=b5ab34957d9c86711bf42480dc130d49CAS |
Krasznai, Z., Marian, T., Izumi, H., Damjanovich, S., Balkay, L., Tron, L., and Morisawa, M. (2000). Membrane hyperpolarization removes inactivation of Ca2+ channels, leading to Ca2+ influx and subsequent initiation of sperm motility in the common carp. Proc. Natl Acad. Sci. USA 97, 2052–2057.
| Membrane hyperpolarization removes inactivation of Ca2+ channels, leading to Ca2+ influx and subsequent initiation of sperm motility in the common carp.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhslKhsLc%3D&md5=06deeefde585ae77e935f68bb86ffd3fCAS | 10688893PubMed |
Krasznai, Z., Morisawa, M., Krasznai, Z. T., Morisawa, S., Inaba, K., Bazsane, Z. K., Rubovszky, B., Bodnar, B., Borsos, A., and Marian, T. (2003a). Gadolinium, a mechano-sensitive channel blocker, inhibits osmosis-initiated motility of sea- and freshwater fish sperm, but does not affect human or ascidian sperm motility. Cell Motil. Cytoskeleton 55, 232–243.
| Gadolinium, a mechano-sensitive channel blocker, inhibits osmosis-initiated motility of sea- and freshwater fish sperm, but does not affect human or ascidian sperm motility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmsl2ktb4%3D&md5=56c27d7f86d8f46b90eea18d580572b2CAS | 12845597PubMed |
Krasznai, Z., Morisawa, M., Morisawa, S., Krasznai, Z. T., Tron, L., Gaspar, R., and Marian, T. (2003b). Role of ion channels and membrane potential in the initiation of carp sperm motility. Aquat. Living Resour. 16, 445–449.
| Role of ion channels and membrane potential in the initiation of carp sperm motility.Crossref | GoogleScholarGoogle Scholar |
Kumar, S., and Hall, R. J. C. (2003). Drug treatment of stable angina pectoris in the elderly: defining the place of calcium channel antagonists. Drugs Aging 20, 805–815.
| Drug treatment of stable angina pectoris in the elderly: defining the place of calcium channel antagonists.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXotlSms7w%3D&md5=1ed525955773ded17196220c4ee80013CAS | 12964887PubMed |
Kuroda, Y., Kaneko, S., Yoshimura, Y., Nozawa, S., and Mikoshiba, K. (1999). Are there inositol 1,4,5-triphosphate (IP3) receptors in human sperm? Life Sci. 65, 135–143.
| Are there inositol 1,4,5-triphosphate (IP3) receptors in human sperm?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXktFais74%3D&md5=2dc3493288013a4dbfb94fb20a95076fCAS | 10416819PubMed |
Lasko, J., Schlingmann, K., Klocke, A., Mengel, G. A., and Turner, R. (2012). Calcium/calmodulin and cAMP/protein kinase-A pathways regulate sperm motility in the stallion. Anim. Reprod. Sci. 132, 169–177.
| Calcium/calmodulin and cAMP/protein kinase-A pathways regulate sperm motility in the stallion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XosFWks7w%3D&md5=81565b59bbe081c2d9f575a5c8b13699CAS | 22687341PubMed |
Laver, D. R., and van Heiden, D. F. (2011). Three independent mechanisms contribute to tetracaine inhibition of cardiac calcium release channels. J. Mol. Cell. Cardiol. 51, 357–369.
| Three independent mechanisms contribute to tetracaine inhibition of cardiac calcium release channels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXpvFWqs7k%3D&md5=dec71d9cc1acda08e00055e322e246b5CAS | 21624373PubMed |
Li, P., Li, Z. H., Hulak, M., Rodina, M., and Linhart, O. (2012). Regulation of spermatozoa motility in response to cations in Russian sturgeon Acipenser gueldenstaedtii. Theriogenology 78, 102–109.
| Regulation of spermatozoa motility in response to cations in Russian sturgeon Acipenser gueldenstaedtii.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XksFeisbc%3D&md5=26157a6ce13953fdd3e8b44a68504a18CAS | 22444559PubMed |
Linhart, O., Cosson, J., Mims, S. D., Shelton, W. L., and Rodina, M. (2002). Effects of ions on the motility of fresh and demembranated paddlefish (Polyodon spathula) spermatozoa. Reproduction 124, 713–719.
| Effects of ions on the motility of fresh and demembranated paddlefish (Polyodon spathula) spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXht1KktA%3D%3D&md5=d47a94e20ed33f53ffa73294c29a28c3CAS | 12417010PubMed |
Liu, Z., Wang, B., Ruijun, H., Zhao, Y., and Miao, L. (2014). Calcium signalling and the MAPK cascade are required for sperm activation in Caenorhabditis elegans. Biochim. Biophys. Acta 1843, 299–308.
| Calcium signalling and the MAPK cascade are required for sperm activation in Caenorhabditis elegans.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXltlOi&md5=6696f09bb39df531c9e6dbfeb436dc86CAS | 24239721PubMed |
Marquez, B., Ignotz, G., and Suarez, S. (2007). Contributions of extracellular and intracellular Ca2+ to regulation of sperm motility: release of intracellular stores can hyperactivate CatSper1 and CatSper2 null sperm. Dev. Biol. 303, 214–221.
| Contributions of extracellular and intracellular Ca2+ to regulation of sperm motility: release of intracellular stores can hyperactivate CatSper1 and CatSper2 null sperm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhvVGgsbw%3D&md5=202cdd907b70d08405f9bdfe57c53849CAS | 17174296PubMed |
McCormack, J. G., and Denton, R. M. (1993). Mitochondrial Ca2+ transport and the role of intramitochondrial Ca2+ in the regulation of energy-metabolism. Dev. Neurosci. 15, 165–173.
| Mitochondrial Ca2+ transport and the role of intramitochondrial Ca2+ in the regulation of energy-metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXmtlCqsA%3D%3D&md5=eba7a303e2521c17a5043bcad2b0b626CAS | 7805568PubMed |
Michaut, M., Tomes, C. N., De Blas, G., Yunes, R., and Mayorga, L. S. (2000). Calcium-triggered acrosomal exocytosis in human spermatozoa requires the coordinated activation of Rab3A and N-ethylmaleimide-sensitive factor. Proc. Natl Acad. Sci. USA 97, 9996–10 001.
| Calcium-triggered acrosomal exocytosis in human spermatozoa requires the coordinated activation of Rab3A and N-ethylmaleimide-sensitive factor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmtlehs7k%3D&md5=df7532609a0bac790a4c50943d5d3efdCAS | 10954749PubMed |
Miura, T., Kasugai, T., Nagahama, Y., and Yamauchi, K. (1995). Acquisition of potential for sperm motility in vitro in Japanese eel Anguilla japonica. Fish. Sci. 61, 533–534.
| Acquisition of potential for sperm motility in vitro in Japanese eel Anguilla japonica.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXmsFerur0%3D&md5=11a5c7a3c9ddf847cd444dc8cb6a3302CAS |
Morisawa, S., and Morisawa, M. (1986). Acquisition of potential for sperm motility in rainbow trout and chum salmon. J. Exp. Biol. 126, 89–96.
| 1:STN:280:DyaL2s7htFemug%3D%3D&md5=d04daea34108cd1b5ee966c9b3b6484bCAS | 3806005PubMed |
Morisawa, S., and Morisawa, M. (1988). Induction of potential for sperm motility by bicarbonate and pH in rainbow trout and chum salmon. J. Exp. Biol. 136, 13–22.
| 1:STN:280:DyaL1c3pvFykug%3D%3D&md5=3f31b75295adc73e5cfc2685d5f6455eCAS | 3404073PubMed |
Morisawa, M., and Suzuki, K. (1980). Osmolality and potassium ion: their roles in initiation of sperm motility in teleosts. Science 210, 1145–1147.
| Osmolality and potassium ion: their roles in initiation of sperm motility in teleosts.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3M%2FnvVOntQ%3D%3D&md5=d41d0bc43d9c761e3e087b302d106a86CAS | 7444445PubMed |
Morita, M., Takemura, A., and Okuno, M. (2003). Requirement of Ca2+ on activation of sperm motility in euryhaline tilapia Oreochromis mossambicus. J. Exp. Biol. 206, 913–921.
| Requirement of Ca2+ on activation of sperm motility in euryhaline tilapia Oreochromis mossambicus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXislKmtb8%3D&md5=384af9d0c96343f0268261bff076c0d8CAS | 12547946PubMed |
Morita, M., Fujinoki, M., and Okuno, M. (2005). K+-independent initiation of motility in chum salmon sperm treated with an organic alcohol, glycerol. J. Exp. Biol. 208, 4549–4556.
| K+-independent initiation of motility in chum salmon sperm treated with an organic alcohol, glycerol.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xot1emtw%3D%3D&md5=6435a3bbab0c21996e4c42fd00257ed9CAS | 16339873PubMed |
Morita, M., Takemura, A., Nakajima, A., and Okuno, M. (2006). Microtubule sliding movement in tilapia sperm flagella axoneme is regulated by Ca2+/calmodulin-dependent protein phosphorylation. Cell Motil. Cytoskeleton 63, 459–470.
| Microtubule sliding movement in tilapia sperm flagella axoneme is regulated by Ca2+/calmodulin-dependent protein phosphorylation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XotlSktrg%3D&md5=7e02ffb3c625254624567407af4290a1CAS | 16767745PubMed |
Naaby-Hansen, S., Wolkowicz, M. J., Klotz, K., Bush, L. A., Westbrook, V. A., Shibahara, H., Shetty, J., Coonrod, S. A., Reddi, P. P., Shannon, J., Kinter, M., Sherman, N. E., Fox, J., Flickinger, C. J., and Herr, J. C. (2001). Co-localization of the inositol 1,4,5-trisphosphate receptor and calreticulin in the equatorial segment and in membrane bounded vesicles in the cytoplasmic droplet of human spermatozoa. Mol. Hum. Reprod. 7, 923–933.
| Co-localization of the inositol 1,4,5-trisphosphate receptor and calreticulin in the equatorial segment and in membrane bounded vesicles in the cytoplasmic droplet of human spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnvVGhsbY%3D&md5=91390375f0f8b331cc8b0088c201b634CAS | 11574661PubMed |
Oda, S., and Morisawa, M. (1993). Rises of intracellular Ca2+ and pH mediate the initiation of sperm motility by hyperosmolality in marine teleosts. Cell Motil. Cytoskeleton 25, 171–178.
| Rises of intracellular Ca2+ and pH mediate the initiation of sperm motility by hyperosmolality in marine teleosts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXlslOqsb0%3D&md5=1c63161d2ac2574f425ebab97cded677CAS | 8324831PubMed |
Ohta, H., Ikeda, K., and Izawa, T. (1997). Increases in concentrations of potassium and bicarbonate ions promote acquisition of motility in vitro by Japanese eel spermatozoa. J. Exp. Zool. 277, 171–180.
| Increases in concentrations of potassium and bicarbonate ions promote acquisition of motility in vitro by Japanese eel spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhvFOks74%3D&md5=061d1588e279fbed9ef47ae8756d4f25CAS |
Padan, E., Venturi, M., Gerchman, Y., and Dover, N. (2001). Na+/H+ antiporters. Biochim. Biophys. Acta 1505, 144–157.
| Na+/H+ antiporters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhvVagtrs%3D&md5=c87afe02e263b2b2a96e1c1d04a46ee5CAS | 11248196PubMed |
Perry Gardner, H., Rajan, J. V., Ha, S. I., Copeland, N. G., Gilbert, D. J., Jenkins, N. A., Marquis, S. T., and Chodosh, L. A. (2000). Cloning, characterization, and chromosomal localization of Pnck, a Ca2+/calmodulin-dependent protein kinase. Genomics 63, 279–288.
| Cloning, characterization, and chromosomal localization of Pnck, a Ca2+/calmodulin-dependent protein kinase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhtVKis78%3D&md5=a7a22ccfc65759b5708f3d2149819ecaCAS |
Rahman, M. S., Kwon, W. S., and Pang, M. G. (2014). Calcium influx and male fertility in the context of the sperm proteome: an update. BioMed Res. Int. , .
| Calcium influx and male fertility in the context of the sperm proteome: an update.Crossref | GoogleScholarGoogle Scholar | 24877140PubMed |
Rossato, M., Di Virgilio, F., Rizzuto, R., Galeazzi, C., and Foresta, C. (2001). Intracellular calcium store depletion and acrosome reaction in human spermatozoa: role of calcium and plasma membrane potential. Mol. Hum. Reprod. 7, 119–128.
| Intracellular calcium store depletion and acrosome reaction in human spermatozoa: role of calcium and plasma membrane potential.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhsFahsbs%3D&md5=850a930eb0a503f12b18c09670e64dd9CAS | 11160837PubMed |
Siegel, S., and Tukey, J. W. (1960). A nonparametric sum of ranks procedure for relative spread in unpaired samples. J. Am. Stat. Assoc. 55, 429–445.
| A nonparametric sum of ranks procedure for relative spread in unpaired samples.Crossref | GoogleScholarGoogle Scholar |
Tash, J. S., and Means, A. R. (1987). Ca2+ regulation of sperm axonemal motility. Methods Enzymol. 139, 808–823.
| Ca2+ regulation of sperm axonemal motility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXksFGhtLw%3D&md5=a3a90a98be71e78da35043c6b15cba35CAS | 3587047PubMed |
Treviño, C. L., Santi, C. M., Beltrán, C., Hernández-Cruz, A., Darszon, A., and Lomeli, H. (1998). Localisation of inositol trisphosphate and ryanodine receptors during mouse spermatogenesis: possible functional implications. Zygote 6, 159–172.
| Localisation of inositol trisphosphate and ryanodine receptors during mouse spermatogenesis: possible functional implications.Crossref | GoogleScholarGoogle Scholar | 9770782PubMed |
Vines, C. A., Yoshida, K., Griffin, F. J., Pillai, M. C., Morisawa, M., Yanagimachi, R., and Cherr, G. N. (2002). Motility initiation in herring sperm is regulated by reverse sodium-calcium exchange. Proc. Natl Acad. Sci. USA 99, 2026–2031.
| Motility initiation in herring sperm is regulated by reverse sodium-calcium exchange.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XitVSrsb8%3D&md5=08ca08b5e8745a5ddbeb762f0f3f80ecCAS | 11842223PubMed |
Walensky, L. D., and Snyder, S. H. (1995). Inositol 1,4,5-trisphosphate receptors selectively localized to the acrosomes of mammalian sperm. J. Cell Biol. 130, 857–869.
| Inositol 1,4,5-trisphosphate receptors selectively localized to the acrosomes of mammalian sperm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXnsVymtL8%3D&md5=3be7d970ab612c7d90334b1660d92d98CAS | 7642703PubMed |
Watanabe, H., Chopra, N., Laver, D., Hwang, H. S., Davies, S. S., Roach, D. E., Duff, H. J., Roden, D. M., Wilde, A. A. M., and Knollmann, B. C. (2009). Flecainide prevents catecholaminergic polymorphic ventricular tachycardia in mice and humans. Nat. Med. 15, 380–383.
| Flecainide prevents catecholaminergic polymorphic ventricular tachycardia in mice and humans.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjslart7Y%3D&md5=90f19a8ef93f7e470fa78168a542c11dCAS | 19330009PubMed |
White, D., Lamirande, E., and Gagnon, C. (2007). Proteine kinase C is an important signalling mediator associated with motility of intact sea urchin spermatozoa. J. Exp. Biol. 210, 4053–4064.
| Proteine kinase C is an important signalling mediator associated with motility of intact sea urchin spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFKmu7w%3D&md5=dd6a617b75330009a43f34f946695b7eCAS | 17981873PubMed |
Xia, J. S., Reigada, D., Mitchell, C. H., and Ren, D. (2007). CATSPER channel-mediated Ca2+ entry into mouse sperm triggers a tail-to-head propagation. Biol. Reprod. 77, 551–559.
| CATSPER channel-mediated Ca2+ entry into mouse sperm triggers a tail-to-head propagation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpvFCrurk%3D&md5=4ed064ba94a7578d2779f1014391458cCAS |
Yoshida, M., Inaba, K., Ishida, K., and Morisawa, M. (1994). Calcium and cyclic AMP mediate sperm activation, but Ca2+ alone contributes sperm chemotaxis in the ascidian, Ciona savignyi. Dev. Growth Differ. 36, 589–595.
| Calcium and cyclic AMP mediate sperm activation, but Ca2+ alone contributes sperm chemotaxis in the ascidian, Ciona savignyi.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXjvVOjtLk%3D&md5=d021b67ae877921288ada839d3c90cceCAS |
Yoshida, M., Ishikawa, M., Izumi, H., De Santis, R., and Morisawa, M. (2003). Store-operated calcium channel regulates the chemotactic behavior of ascidian sperm. Proc. Natl Acad. Sci. USA 100, 149–154.
| Store-operated calcium channel regulates the chemotactic behavior of ascidian sperm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXktlOhuw%3D%3D&md5=fb44a528ac2efedd658ce39633dd77bfCAS | 12518063PubMed |
Zapata, O., Ralston, J., Beltran, C., Parys, J. B., Chen, J. L., Longo, F. J., and Darszon, A. (1997). Inositol triphosphate receptors in sea urchin sperm. Zygote 5, 355–364.
| Inositol triphosphate receptors in sea urchin sperm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXisVGjsLw%3D&md5=7652ef8499a733b10f5c2f68f92caba5CAS | 9563683PubMed |
