Modification of membrane cholesterol and desmosterol in chicken spermatozoa improves post-thaw survival and prevents impairment of sperm function after cryopreservation
Ai Ushiyama A , Atsushi Tajima B , Naoto Ishikawa B and Atsushi Asano B CA Graduate School for Life and Environmental Sciences, University of Tsukuba, Ibaraki 305-8577, Japan.
B Faculty of Life and Environmental Sciences, University of Tsukuba, Ibaraki 305-8577, Japan.
C Corresponding author. Email: asano.atsushi.ft@u.tsukuba.ac.jp
Reproduction, Fertility and Development 30(4) 591-599 https://doi.org/10.1071/RD17076
Submitted: 28 February 2017 Accepted: 16 August 2017 Published: 26 September 2017
Abstract
During cryopreservation, spermatozoa are subjected to cryodamage that leads to a decline in fertilisation ability. Due to the complex nature of this process, the initial trigger for cryodamage remains unknown. Recently, we demonstrated that cryopreservation induces early apoptotic changes characterised by phosphatidylserine (PS) translocation via sterol loss from the plasma membrane of chicken spermatozoa. This led us to hypothesise that sterol incorporation into membranes minimises cryodamage, thereby improving the quality of cryopreserved chicken spermatozoa. In the present study, treating spermatozoa with 1.5 mg mL−1 cholesterol- and 3 mg mL−1 desmosterol-loaded cyclodextrin (CLC and DLC respectively) increased post-thaw survival and motility. These effects appeared to be highly dependent the amount of sterol loaded into the spermatozoa. Localisation experiments confirmed the incorporation of exogenous cholesterol into the sperm head region. Detection of PS translocation showed that elevation of these sterols inhibited early apoptotic changes, thereby enhancing post-thaw survival. Furthermore, CLC and DLC treatment suppressed spontaneous acrosome reaction after cryopreservation, preserving the ability of spermatozoa to undergo acrosome reactions in response to physiological stimulation. These results demonstrate that loading sterols into chicken spermatozoa before cryopreservation enhances their quality by inhibiting early apoptotic changes and spontaneous acrosome reactions. The present study provides new mechanistic insight into cryodamage in chicken spermatozoa.
Additional keywords: acrosome reaction, cryodamage, fertilization, phosphatidylserine translocation, sterol.
References
Aitken, R. J. (2011). The capacitation–apoptosis highway: oxysterols and mammalian sperm function. Biol. Reprod. 85, 9–12.| The capacitation–apoptosis highway: oxysterols and mammalian sperm function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXotFOlsro%3D&md5=71bef7b536c653aae01fe220bfce477fCAS |
Amidi, F., Farshad, A., and Khor, A. K. (2010). Effects of cholesterol-loaded cyclodextrin during freezing step of cryopreservation with TCGY extender containing bovine serum albumin on quality of goat spermatozoa. Cryobiology 61, 94–99.
| Effects of cholesterol-loaded cyclodextrin during freezing step of cryopreservation with TCGY extender containing bovine serum albumin on quality of goat spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpvVGkt7Y%3D&md5=0187a4745e07f5577cbdb443e551f387CAS |
Anzar, M., He, L., Buhr, M. M., Kroetsch, T. G., and Pauls, K. P. (2002). Sperm apoptosis in fresh and cryopreserved bull semen detected by flow cytometry and its relationship with fertility. Biol. Reprod. 66, 354–360.
| Sperm apoptosis in fresh and cryopreserved bull semen detected by flow cytometry and its relationship with fertility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XotVSlsQ%3D%3D&md5=b8f3a4baa1878ba47e3b209c47e23821CAS |
Arashiki, N., Saito, M., Koshino, I., Kamata, K., Hale, J., Mohandas, N., Manno, S., and Takakuwa, Y. (2016). An unrecognized function of cholesterol: regulating the mechanism controlling membrane phospholipid asymmetry. Biochemistry 55, 3504–3513.
| An unrecognized function of cholesterol: regulating the mechanism controlling membrane phospholipid asymmetry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XptlCitLs%3D&md5=ee94366c119f2c1c3642f1bf9535db79CAS |
Asano, A., Selvaraj, V., Buttke, D. E., Nelson, J. L., Green, K. M., Evans, J. E., and Travis, A. J. (2009). Biochemical characterization of membrane fractions in murine sperm: identification of three distinct sub-types of membrane rafts. J. Cell. Physiol. 218, 537–548.
| Biochemical characterization of membrane fractions in murine sperm: identification of three distinct sub-types of membrane rafts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXit1Kht7w%3D&md5=5c275f94f876f2dfb0d32274416d8033CAS |
Asano, A., Nelson-Harrington, J. L., and Travis, A. J. (2013). Phospholipase B is activated in response to sterol removal and stimulates acrosome exocytosis in murine sperm. J. Biol. Chem. 288, 28104–28115.
| Phospholipase B is activated in response to sterol removal and stimulates acrosome exocytosis in murine sperm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsFens7fM&md5=4767fced66e8788c6c717c79faa187a4CAS |
Asano, A., Kanbe, H., Ushiyama, A., and Tajima, A. (2016). Organization of membrane rafts in chicken sperm. J. Poult. Sci. 53, 233–239.
| Organization of membrane rafts in chicken sperm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XitVyht77E&md5=5df27594859a558ddf5c9219f90f89a3CAS |
Ashizawa, K., Wishart, G. J., Ranasinghe, A. R. A. H., Katayama, S., and Tsuzuki, Y. (2004). Protein phosphatase-type 2B is involved in the regulation of the acrosome reaction but not in the temperature-dependent flagellar movement of fowl spermatozoa. Reproduction 128, 783–787.
| Protein phosphatase-type 2B is involved in the regulation of the acrosome reaction but not in the temperature-dependent flagellar movement of fowl spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFSrtw%3D%3D&md5=fbd2f571d8d4c906bc7b04c154fe081dCAS |
Bailey, J. L., Bilodeau, J. F., and Cormier, N. (2000). Semen cryopreservation in domestic animals: a damaging and capacitating phenomenon. J. Androl. 21, 1–7.
| 1:STN:280:DC%2BD3c7jtl2ktg%3D%3D&md5=f15c5c0759227ebd5ff682a9364ebdadCAS |
Bailey, J. L., Lessard, C., Jacques, J., Breque, C., Dobrinski, I., Zeng, W., and Galantino-Homer, H. L. (2008). Cryopreservation of boar semen and its future importance to the industry. Theriogenology 70, 1251–1259.
| Cryopreservation of boar semen and its future importance to the industry.Crossref | GoogleScholarGoogle Scholar |
Blanch, E., Tomas, C., Graham, J. K., and Moce, E. (2012). Response of boar sperm to the treatment with cholesterol-loaded cyclodextrins added prior to cryopreservation. Reprod. Domest. Anim. 47, 959–964.
| Response of boar sperm to the treatment with cholesterol-loaded cyclodextrins added prior to cryopreservation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvFKgtLw%3D&md5=abb734dc51c662917d010391c8b08ee9CAS |
Burrows, H. (1937). An operation for the correction of Madelung’s deformity and similar conditions. Proc. R. Soc. Med. XXX, 565–572.
Cerolini, S., Maldjian, A., Pizzi, F., and Gliozzi, T. M. (2001). Changes in sperm quality and lipid composition during cryopreservation of boar semen. Reproduction 121, 395–401.
| Changes in sperm quality and lipid composition during cryopreservation of boar semen.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXisFSqu7s%3D&md5=dbba0a11895ae6ae9ae6917b8d7d5d0fCAS |
Connor, W. E., Lin, D. S., Wolf, D. P., and Alexander, M. (1998). Uneven distribution of desmosterol and docosahexaenoic acid in the heads and tails of monkey sperm. J. Lipid Res. 39, 1404–1411.
| 1:CAS:528:DyaK1cXkslOqtbo%3D&md5=0e99f931d66c3769670f6f265f8c8bf6CAS |
Crockett, E. L. (1998). Cholesterol function in plasma membranes from ectotherms: membrane-specific roles in adaptation to temperature. Am. Zool. 38, 291–304.
| Cholesterol function in plasma membranes from ectotherms: membrane-specific roles in adaptation to temperature.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjt1yksb4%3D&md5=ac4734872661026994b11969b054134dCAS |
Cross, N. L. (1996). Effect of cholesterol and other sterols on human sperm acrosomal responsiveness. Mol. Reprod. Dev. 45, 212–217.
| Effect of cholesterol and other sterols on human sperm acrosomal responsiveness.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XmsFGmtbo%3D&md5=99bd71398b359e7df118519b6fe846d4CAS |
Cross, N. L. (1998). Role of cholesterol in sperm capacitation. Biol. Reprod. 59, 7–11.
| Role of cholesterol in sperm capacitation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXktFaksL0%3D&md5=78df121b8d9a70cb943611b83ea58f96CAS |
de Vries, K. J., Wiedmer, T., Sims, P. J., and Gadella, B. M. (2003). Caspase-independent exposure of aminophospholipids and tyrosine phosphorylation in bicarbonate responsive human sperm cells. Biol. Reprod. 68, 2122–2134.
| Caspase-independent exposure of aminophospholipids and tyrosine phosphorylation in bicarbonate responsive human sperm cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXks1GgsLY%3D&md5=57e75bc229b0b4896e12a1eca8b60098CAS |
Drobnis, E. Z., Crowe, L. M., Berger, T., Anchordoguy, T. J., Overstreet, J. W., and Crowe, J. H. (1993). Cold shock damage is due to lipid phase transitions in cell membranes: a demonstration using sperm as a model. J. Exp. Zool. 265, 432–437.
| Cold shock damage is due to lipid phase transitions in cell membranes: a demonstration using sperm as a model.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXksVKisrc%3D&md5=4755d4d252eaa21847436ea4e4f7e187CAS |
Flesch, F. M., Brouwers, J. F., Nievelstein, P. F., Verkleij, A. J., van Golde, L. M., Colenbrander, B., and Gadella, B. M. (2001). Bicarbonate stimulated phospholipid scrambling induces cholesterol redistribution and enables cholesterol depletion in the sperm plasma membrane. J. Cell Sci. 114, 3543–3555.
| 1:CAS:528:DC%2BD3MXotVSqtb4%3D&md5=38755fd77553cba3f39ce221b5dd0060CAS |
Gadella, B. M., and Harrison, R. A. (2002). Capacitation induces cyclic adenosine 3′,5′-monophosphate-dependent, but apoptosis-unrelated, exposure of aminophospholipids at the apical head plasma membrane of boar sperm cells. Biol. Reprod. 67, 340–350.
| Capacitation induces cyclic adenosine 3′,5′-monophosphate-dependent, but apoptosis-unrelated, exposure of aminophospholipids at the apical head plasma membrane of boar sperm cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XkvV2iurY%3D&md5=5a9823b582461b1b6c0766482f45ed9aCAS |
Galantino-Homer, H. L., Zeng, W.-x., Megee, S. O., Dallmeyer, M., Voelkl, D., and Dobrinski, I. (2006). Effects of 2-hydroxypropyl-β-cyclodextrin and cholesterol on porcine sperm viability and capacitation status following cold shock or incubation. Mol. Reprod. Dev. 73, 638–650.
| Effects of 2-hydroxypropyl-β-cyclodextrin and cholesterol on porcine sperm viability and capacitation status following cold shock or incubation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xjt1KitLY%3D&md5=ef354206928fc2e23e3356800e74cf0dCAS |
Giraud, M. N., Motta, C., Boucher, D., and Grizard, G. (2000). Membrane fluidity predicts the outcome of cryopreservation of human spermatozoa. Hum. Reprod. 15, 2160–2164.
| Membrane fluidity predicts the outcome of cryopreservation of human spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M%2Fltlartg%3D%3D&md5=1ea0676e59e58cf5beede0ef1bdd40bcCAS |
Holt, W. V. (2000). Fundamental aspects of sperm cryobiology: the importance of species and individual differences. Theriogenology 53, 47–58.
| Fundamental aspects of sperm cryobiology: the importance of species and individual differences.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c7pvFagtA%3D%3D&md5=ac06630b72b77a73de79f79b9765c516CAS |
Huster, D., Scheidt, H. A., Arnold, K., Herrmann, A., and Müller, P. (2005). Desmosterol may replace cholesterol in lipid membranes. Biophys. J. 88, 1838–1844.
| Desmosterol may replace cholesterol in lipid membranes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXis1Whtbk%3D&md5=6d563ee19787cc8302999c5e71d1cc32CAS |
Khan, D. R., Ahmad, N., Anzar, M., and Channa, A. A. (2009). Apoptosis in fresh and cryopreserved buffalo sperm. Theriogenology 71, 872–876.
| Apoptosis in fresh and cryopreserved buffalo sperm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXitVSgsL4%3D&md5=53e006e7bc2351e20c4e97bffe69c749CAS |
Kido, S., and Doi, Y. (1988). Separation and properties of the inner and outer layers of the vitelline membrane of hen’s eggs. Poult. Sci. 67, 476–486.
| Separation and properties of the inner and outer layers of the vitelline membrane of hen’s eggs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXkt1Snt74%3D&md5=06f86d505e5d6c00e90682ecf4aae16aCAS |
Kiso, W. K., Asano, A., Travis, A. J., Schmitt, D. L., Brown, J. L., and Pukazhenthi, B. S. (2012). Pretreatment of Asian elephant (Elephas maximus) spermatozoa with cholesterol-loaded cyclodextrins and glycerol addition at 4°C improves cryosurvival. Reprod. Fertil. Dev. 24, 1134–1142.
| Pretreatment of Asian elephant (Elephas maximus) spermatozoa with cholesterol-loaded cyclodextrins and glycerol addition at 4°C improves cryosurvival.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVKrt7%2FI&md5=a8e55e928841e1e99a6f0c592d94ec1eCAS |
Lee, Y. S., Lee, S., Lee, S. H., Yang, B. K., and Park, C. K. (2015). Effect of cholesterol-loaded-cyclodextrin on sperm viability and acrosome reaction in boar semen cryopreservation. Anim. Reprod. Sci. 159, 124–130.
| Effect of cholesterol-loaded-cyclodextrin on sperm viability and acrosome reaction in boar semen cryopreservation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtVegtb%2FN&md5=6bf31ce200fa3882a71a5debab18b8cbCAS |
Lemoine, M., Grasseau, I., Brillard, J. P., and Blesbois, E. (2008). A reappraisal of the factors involved in in vitro initiation of the acrosome reaction in chicken spermatozoa. Reproduction 136, 391–399.
| A reappraisal of the factors involved in in vitro initiation of the acrosome reaction in chicken spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlSrtr7F&md5=21b4b5a1277fc2cee078a3f5caa7cd28CAS |
Martin, G., Sabido, O., Durand, P., and Levy, R. (2004). Cryopreservation induces an apoptosis-like mechanism in bull sperm. Biol. Reprod. 71, 28–37.
| Cryopreservation induces an apoptosis-like mechanism in bull sperm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltFKktLo%3D&md5=4b0689bcf4e4199dc03d85fa717983efCAS |
Maxwell, W. M., and Johnson, L. A. (1997). Chlortetracycline analysis of boar spermatozoa after incubation, flow cytometric sorting, cooling, or cryopreservation. Mol. Reprod. Dev. 46, 408–418.
| Chlortetracycline analysis of boar spermatozoa after incubation, flow cytometric sorting, cooling, or cryopreservation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhsFKhsr0%3D&md5=40d0db04bfba89860caf2427b12c2eb8CAS |
Medeiros, C. M., Forell, F., Oliveira, A. T., and Rodrigues, J. L. (2002). Current status of sperm cryopreservation: why isn’t it better? Theriogenology 57, 327–344.
| Current status of sperm cryopreservation: why isn’t it better?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XktFyltA%3D%3D&md5=52f443e099cdbda802d94414cf920f66CAS |
Mocé, E., Blanch, E., Tomás, C., and Graham, J. K. (2010a). Use of cholesterol in sperm cryopreservation: present moment and perspectives to future. Reprod. Domest. Anim. 45, 57–66.
| Use of cholesterol in sperm cryopreservation: present moment and perspectives to future.Crossref | GoogleScholarGoogle Scholar |
Mocé, E., Grasseau, I., and Blesbois, E. (2010b). Cryoprotectant and freezing-process alter the ability of chicken sperm to acrosome react. Anim. Reprod. Sci. 122, 359–366.
| Cryoprotectant and freezing-process alter the ability of chicken sperm to acrosome react.Crossref | GoogleScholarGoogle Scholar |
Moore, A. I., Squires, E. L., and Graham, J. K. (2005). Adding cholesterol to the stallion sperm plasma membrane improves cryosurvival. Cryobiology 51, 241–249.
| Adding cholesterol to the stallion sperm plasma membrane improves cryosurvival.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlShsLbP&md5=107e3bb7b1d107175eed36642e5c86b8CAS |
Moraes, E. A., Graham, J. K., Torres, C. A., Meyers, M., and Spizziri, B. (2010). Delivering cholesterol or cholestanol to bull sperm membranes improves cryosurvival. Anim. Reprod. Sci. 118, 148–154.
| Delivering cholesterol or cholestanol to bull sperm membranes improves cryosurvival.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVGltbs%3D&md5=aed99c87a12bd442b44b06a97819d2e0CAS |
Motamed Khorasani, A., Cheung, A. P., and Lee, C. Y. (2000). Cholesterol inhibitory effects on human sperm-induced acrosome reaction. J. Androl. 21, 586–594.
| 1:STN:280:DC%2BD3M%2FgvVyksw%3D%3D&md5=c17b76bc16765209a515ca10a6c30c2aCAS |
Müller, K., Müller, P., Pincemy, G., Kurz, A., and Labbe, C. (2008). Characterization of sperm plasma membrane properties after cholesterol modification: consequences for cryopreservation of rainbow trout spermatozoa. Biol. Reprod. 78, 390–399.
| Characterization of sperm plasma membrane properties after cholesterol modification: consequences for cryopreservation of rainbow trout spermatozoa.Crossref | GoogleScholarGoogle Scholar |
Oliveira, C. H., Vasconcelos, A. B., Souza, F. A., Martins-Filho, O. A., Silva, M. X., Varago, F. C., and Lagares, M. A. (2010). Cholesterol addition protects membrane intactness during cryopreservation of stallion sperm. Anim. Reprod. Sci. 118, 194–200.
| Cholesterol addition protects membrane intactness during cryopreservation of stallion sperm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVGltbc%3D&md5=8242461049537c807c61c3c7330a4c06CAS |
Parks, J. E., and Lynch, D. V. (1992). Lipid composition and thermotropic phase behavior of boar, bull, stallion, and rooster sperm membranes. Cryobiology 29, 255–266.
| Lipid composition and thermotropic phase behavior of boar, bull, stallion, and rooster sperm membranes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xitlaktr0%3D&md5=03071c34c331e7f07fd6f18831e4239fCAS |
Partyka, A., Bonarska-Kujawa, D., Sporniak, M., Strojecki, M., and Nizanski, W. (2016). Modification of membrane cholesterol and its impact on frozen–thawed chicken sperm characteristics. Zygote 24, 714–723.
| Modification of membrane cholesterol and its impact on frozen–thawed chicken sperm characteristics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhsFaku7fE&md5=b8beac3e696a48906cbffccef7f2866aCAS |
Pinho, R. O., Lima, D. M., Shiomi, H. H., Siqueira, J. B., Silveira, C. O., Faria, V. R., Lopes, P. S., Guimaraes, S. E., and Guimaraes, J. D. (2016). Effect of cyclodextrin-loaded cholesterol conjugates on plasma membrane viability of Piau swine breed frozen/thawed spermatozoa. Cryobiology 73, 1–6.
| Effect of cyclodextrin-loaded cholesterol conjugates on plasma membrane viability of Piau swine breed frozen/thawed spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhtFCiurbE&md5=f473c5e1f313dfbbc4daca9872c969e3CAS |
Purdy, P. H., and Graham, J. K. (2004a). Effect of adding cholesterol to bull sperm membranes on sperm capacitation, the acrosome reaction, and fertility. Biol. Reprod. 71, 522–527.
| Effect of adding cholesterol to bull sperm membranes on sperm capacitation, the acrosome reaction, and fertility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmtFWgtbk%3D&md5=4a5354326abcec2f8aa0465e5c1c9e85CAS |
Purdy, P. H., and Graham, J. K. (2004b). Effect of cholesterol-loaded cyclodextrin on the cryosurvival of bull sperm. Cryobiology 48, 36–45.
| Effect of cholesterol-loaded cyclodextrin on the cryosurvival of bull sperm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXht1yiur8%3D&md5=2cbfe8e4381a7c056c1a5239ece42095CAS |
Salmon, V. M., Leclerc, P., and Bailey, J. L. (2016). Cholesterol-loaded cyclodextrin increases the cholesterol content of goat sperm to improve cold and osmotic resistance and maintain sperm function after cryopreservation. Biol. Reprod. 94, 85.
| Cholesterol-loaded cyclodextrin increases the cholesterol content of goat sperm to improve cold and osmotic resistance and maintain sperm function after cryopreservation.Crossref | GoogleScholarGoogle Scholar |
Shen, H. M., Dai, J., Chia, S. E., Lim, A., and Ong, C. N. (2002). Detection of apoptotic alterations in sperm in subfertile patients and their correlations with sperm quality. Hum. Reprod. 17, 1266–1273.
| Detection of apoptotic alterations in sperm in subfertile patients and their correlations with sperm quality.Crossref | GoogleScholarGoogle Scholar |
Sieme, H., Oldenhof, H., and Wolkers, W. F. (2015). Sperm membrane behaviour during cooling and cryopreservation. Reprod. Domest. Anim. 50, 20–26.
| Sperm membrane behaviour during cooling and cryopreservation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhsFGru7%2FI&md5=1db0c76ec6b694d933ee4da5708d8e3bCAS |
Sion, B., Grizard, G., and Boucher, D. (2001). Quantitative analysis of desmosterol, cholesterol and cholesterol sulfate in semen by high-performance liquid chromatography. J. Chromatogr. A 935, 259–265.
| Quantitative analysis of desmosterol, cholesterol and cholesterol sulfate in semen by high-performance liquid chromatography.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXot1Oiu78%3D&md5=8b599d5dc2d2a3c1d4f5276fff422399CAS |
Spizziri, B. E., Fox, M. H., Bruemmer, J. E., Squires, E. L., and Graham, J. K. (2010). Cholesterol-loaded-cyclodextrins and fertility potential of stallions spermatozoa. Anim. Reprod. Sci. 118, 255–264.
| Cholesterol-loaded-cyclodextrins and fertility potential of stallions spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVGlurs%3D&md5=1a1ab55495204f71cd3ee233507dd6e5CAS |
Tajima, A., Graham, E. F., and Hawkins, D. M. (1989). Estimation of the relative fertilizing ability of frozen chicken spermatozoa using a heterospermic competition method. J. Reprod. Fertil. 85, 1–5.
| Estimation of the relative fertilizing ability of frozen chicken spermatozoa using a heterospermic competition method.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1M7isFCrtg%3D%3D&md5=76aed938a0826231648532bf008eede9CAS |
Tomás, C., Blanch, E., Hernández, M., Gil, M. A., Roca, J., Vázquez, J. M., Martínez, E. A., and Mocé, E. (2011). Treating boar sperm with cholesterol-loaded cyclodextrins widens the sperm osmotic tolerance limits and enhances the in vitro sperm fertilising ability. Anim. Reprod. Sci. 129, 209–220.
| Treating boar sperm with cholesterol-loaded cyclodextrins widens the sperm osmotic tolerance limits and enhances the in vitro sperm fertilising ability.Crossref | GoogleScholarGoogle Scholar |
Tsai, P. S., De Vries, K. J., De Boer-Brouwer, M., Garcia-Gil, N., Van Gestel, R. A., Colenbrander, B., Gadella, B. M., and Van Haeften, T. (2007). Syntaxin and VAMP association with lipid rafts depends on cholesterol depletion in capacitating sperm cells. Mol. Membr. Biol. 24, 313–324.
| Syntaxin and VAMP association with lipid rafts depends on cholesterol depletion in capacitating sperm cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXls1Sgsr4%3D&md5=00c5c7001437f848a2300b3020058da1CAS |
Ushiyama, A., Ishikawa, N., Tajima, A., and Asano, A. (2016). Comparison of membrane characteristics between freshly ejaculated and cryopreserved sperm in the chicken. J. Poult. Sci. 53, 305–312.
| Comparison of membrane characteristics between freshly ejaculated and cryopreserved sperm in the chicken.Crossref | GoogleScholarGoogle Scholar |
Vadnais, M. L., and Althouse, G. C. (2011). Characterization of capacitation, cryoinjury, and the role of seminal plasma in porcine sperm. Theriogenology 76, 1508–1516.
| Characterization of capacitation, cryoinjury, and the role of seminal plasma in porcine sperm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht12isbnK&md5=c84f889f0251d62700e7acb0a6fba710CAS |
Vainio, S., Jansen, M., Koivusalo, M., Róg, T., Karttunen, M., Vattulainen, I., and Ikonen, E. (2006). Significance of sterol structural specificity: desmosterol cannot replace cholesterol in lipid rafts. J. Biol. Chem. 281, 348–355.
| Significance of sterol structural specificity: desmosterol cannot replace cholesterol in lipid rafts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1ekug%3D%3D&md5=b3888f060f486a2f62e47d7933645593CAS |
Watson, P. F. (2000). The causes of reduced fertility with cryopreserved semen. Anim. Reprod. Sci. 60–61, 481–492.
| The causes of reduced fertility with cryopreserved semen.Crossref | GoogleScholarGoogle Scholar |
Yildiz, C., Yavas, I., Bozkurt, Y., and Aksoy, M. (2015). Effect of cholesterol-loaded cyclodextrin on cryosurvival and fertility of cryopreserved carp (Cyprinus carpio) sperm. Cryobiology 70, 190–194.
| Effect of cholesterol-loaded cyclodextrin on cryosurvival and fertility of cryopreserved carp (Cyprinus carpio) sperm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXis1anur4%3D&md5=df93d362fcda59accdb6a7129921b34eCAS |
Zahn, F. S., Papa, F. O., and Dell’Aqua, J. A. (2002). Cholesterol incorporation on equine sperm membrane: effects on post-thaw sperm parameters and fertility. Theriogenology 58, 237–240.
| Cholesterol incorporation on equine sperm membrane: effects on post-thaw sperm parameters and fertility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XkvFyntbY%3D&md5=9c6ba3fd2d5571171f18854e3991d1bfCAS |
Zarintash, R. J., and Cross, N. L. (1996). Unesterified cholesterol content of human sperm regulates the response of the acrosome to the agonist, progesterone. Biol. Reprod. 55, 19–24.
| Unesterified cholesterol content of human sperm regulates the response of the acrosome to the agonist, progesterone.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XltlKns7c%3D&md5=097b012d9fe8b32e78e97059331e4d19CAS |
Zeng, W. X., and Terada, T. (2001a). Effects of methyl-beta-cyclodextrin on cryosurvival of boar spermatozoa. J. Androl. 22, 111–118.
| 1:CAS:528:DC%2BD3MXkvFyjtA%3D%3D&md5=23a9666544c313d2dc15b42ef16d621eCAS |
Zeng, W. X., and Terada, T. (2001b). Protection of boar spermatozoa from cold shock damage by 2-hydroxypropyl-beta-cyclodextrin. Theriogenology 55, 615–627.
| Protection of boar spermatozoa from cold shock damage by 2-hydroxypropyl-beta-cyclodextrin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhsFCqu7k%3D&md5=73802ce0148f552be78c628d9c115120CAS |