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Modification of membrane cholesterol and its impact on frozen–thawed chicken sperm characteristics

Published online by Cambridge University Press:  03 May 2016

Agnieszka Partyka ,
Dorota Bonarska-Kujawa ,
Marta Sporniak ,
Maciej Strojecki  and
Wojciech Niżański
Agnieszka Partyka*
Affiliation:
Wroclaw University of Environmental and Life Sciences, Faculty of Veterinary Medicine, Department of Reproduction and Clinic of Farm Animals, pl. Grunwaldzki 49, 50–366 Wrocław, Poland.
Dorota Bonarska-Kujawa
Affiliation:
Wroclaw University of Environmental and Life Sciences, Faculty of Life Sciences and Technology, Department of Physics and Biophysics, ul. Norwida 25, 50–375 Wroclaw, Poland.
Marta Sporniak
Affiliation:
Wroclaw University of Environmental and Life Sciences, Faculty of Veterinary Medicine, Department of Reproduction and Clinic of Farm Animals, pl. Grunwaldzki 49, 50–366 Wroclaw, Poland.
Maciej Strojecki
Affiliation:
Wroclaw University of Environmental and Life Sciences, Faculty of Veterinary Medicine, Department of Reproduction and Clinic of Farm Animals, pl. Grunwaldzki 49, 50–366 Wroclaw, Poland.
Wojciech Niżański
Affiliation:
Wroclaw University of Environmental and Life Sciences, Faculty of Veterinary Medicine, Department of Reproduction and Clinic of Farm Animals, pl. Grunwaldzki 49, 50–366 Wroclaw, Poland.
*
All correspondence to: Agnieszka Partyka. Wroclaw University of Environmental and Life Sciences, Faculty of Veterinary Medicine, Department of Reproduction and Clinic of Farm Animals, pl. Grunwaldzki 49, 50–366 Wrocław, Poland. Tel: +48 71 32 05 300. Fax: +48 71 32 01 006. E-mail address: [email protected]
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Summary

This study was conducted to determine the changes in chicken sperm plasma membranes fluidity and polarity as lipid packing arrangement induced by cholesterol-loaded cyclodextrin (CLC) and 2-hydroxypropyl-β-cyclodextrin (HBCD) and how sperm cryopreservation outcomes are improved by these changes. Treatment with 2 mg HBCD supported the highest (P < 0.01) percentage of viable spermatozoa compared with the control and CLCs groups after cryopreservation. The percentage of post-thaw progressive and rapid sperm motility was highest in 2 mg HBCD (P < 0.01). After thawing, sperm treated with 1 or 2 mg CLC showed the highest anisotropy at 5, 21, 25 and 40°C (P < 0.01). At 25°C, the lowest anisotropy was observed in the thawed semen from the control group. The highest value (P < 0.01) of generalized polarization (GP) (0.5) at 5°C was observed in the 1 mg CLC treated sample. After 2 h of incubation, the highest percentage of viable spermatozoa was observed in the HBCD group in relation to the other treatments (P < 0.01). Exposure to 1 mg or 2 mg of CLC significantly decreased the percentage of live spermatozoa after thawing (P < 0.01). In conclusion, HBCD appears to play a role in the modification of sperm membranes, increasing their fluidity and preventing them against membrane phase transition to gel, thus minimizing freezing-thaw sperm damage. HBCD treatment enhances chicken sperm viability and motility after cryopreservation and subsequent storage. This novel procedure may be useful for improving the technology for cryopreservation of fowl spermatozoa.

Keywords

Chicken sperm cholesterolCryopreservationCyclodextrinSemen analysisSperm membrane fluidity
Type
Research Article
Information
Zygote , Volume 24 , Issue 5 , October 2016 , pp. 714 - 723
Copyright
Copyright © Cambridge University Press 2016 

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References

Amann, R.P. & Pickett, B.W. (1987). Principles of cryopreservation and a review of cryopreservation of stallion spermatozoa. J. Equine Vet. Sci. 7, 145–73.CrossRefGoogle Scholar
Ambrosini, A., Zolese, G., Balercia, G., Bertoli, E., Arnaldi, G. & Mantero, F. (2001). Laurdan fluorescence: a simple method to evaluate sperm plasma membrane alterations. Fert. Steril. 76, 501–5.CrossRefGoogle ScholarPubMed
Ambrosini, A., Zolese, G., Wozniak, M., Genga, D., Boscaro, M., Mantero, F. & Balercia, G. (2003). Idiopathic infertility: susceptibility of spermatozoa to in-vitro capacitation, in the presence and the absence of palmitylethanolamide (a homologue of anandamide), is strongly correlated with membrane polarity studied by Laurdan fluorescence. Mol. Hum. Reprod. 9, 381–8.CrossRefGoogle ScholarPubMed
Amidi, F., Farshad, A. & 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, 94–9.CrossRefGoogle ScholarPubMed
Award, M.M. & Graham, J.K. (2002). Effect of adding cholesterol to bovine spermatozoa on motility parameters and cell viability after cryopreservation. Cryobiology 45, 256–7.Google Scholar
Bailey, J.L., Bilodeau, J.F. & Cormier, N. (2000). Semen cryopreservation in domestic animals: a damaging and capacitating phenomenon. J. Androl. 21, 1–7.CrossRefGoogle ScholarPubMed
Blanch, E., Tomás, C., Graham, J.K. & Mocé, E. (2012). Response of boar sperm to the treatment with cholesterol-loaded cyclodextrins added prior to cryopreservation. Reprod. Domest. Anim. 47, 959–64.CrossRefGoogle Scholar
Blesbois, E., Lessire, M. & Hermier, D. (1997). Effect of cryopreservation and diet on lipids of fowl sperm and fertility. Poult. Avian Biol. Rev. 8, 149–54.Google Scholar
Blesbois, E., Grasseau, I. & Seigneurin, F. (2005). Membrane fluidity and the ability of domestic bird spermatozoa to survive cryopreservation. Reproduction 129, 371–8.CrossRefGoogle ScholarPubMed
Blesbois, E., Grasseau, I., Seigneurin, F., Mignon-Grasteau, S., Saint Jalme, M. & Mialon-Richard, M.M. (2008). Predictors of success of semen cryopreservation in chickens. Theriogenology 69, 252–61.CrossRefGoogle ScholarPubMed
Burrows, W.H. & Quinn, J.P. (1937). The collection of spermatozoa from the domestic fowl and turkey. Poult. Sci. 16, 19–24.CrossRefGoogle Scholar
Chakrabarty, J., Banerjee, D., Pal, D., De, J., Ghosh, A. & Majumder, G.C. (2007). Shedding off specific lipid constituents from sperm cell membrane during cryopreservation. Cryobiology 54, 27–35.CrossRefGoogle ScholarPubMed
Christian, A.E., Haynes, M.P., Phillips, M.C. & Rothblat, G.H. (1997). Use of cyclodextrins for manipulating cellular cholesterol content. J. Lipid. Res. 38, 2264–72.CrossRefGoogle ScholarPubMed
Cormier, N. & Bailey, J.L. (2003). A differential mechanism is involved during heparin- and cryopreservation-induced capacitation of bovine spermatozoa. Biol. Reprod. 69, 177–85.CrossRefGoogle ScholarPubMed
Crockett, E.L. (1998). Cholesterol function in plasma membranes from ectotherms: membrane-specific roles in adaptation to temperature. Am. Zool. 38, 291–304.CrossRefGoogle Scholar
Curry, M.R. (2000). Cryopreservation of semen from domestic livestock. Rev. Reprod. 5, 46–52.CrossRefGoogle ScholarPubMed
Darin-Bennett, A. & White, I. G. (1977). Influence of the cholesterol content of mammalian spermatozoa on susceptibility to cold-shock. Cryobiology 14, 466–70.CrossRefGoogle ScholarPubMed
Drobnis, E.Z., Crowe, L.M., Berger, T., Anchordoguy, T.J., Overstreet, J.W. & 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, 432–37.CrossRefGoogle ScholarPubMed
Farshad, A., Amidi, F., Koohi Khor, A. & Rashidi, A. (2011). Effect of cholesterol-loaded-cyclodextrin in presence and absence of egg yolk during freezing step on quality of Markhoz buck's spermatozoa. Asian. Australas. J. Anim. Sci. 24, 181–9.CrossRefGoogle Scholar
Gadella, B.M., Lopes-Cardozo, M., van Golde, L.M., Colenbrander, B. & Gadella, T.W. Jr (1995). Glycolipid migration from the apical to the equatorial subdomains of the sperm head plasma membrane precedes the acrosome reaction. Evidence for a primary capacitation event in boar spermatozoa. J. Cell. Sci. 108, 935–46.CrossRefGoogle Scholar
Galantino-Homer, H.L., Zeng, W.X., Megee, S.O., Dallmeyer, M., Voelkl, D. & Dobrinski, I. (2006). Effects of 2-hydroxypropyl-betacyclodextrin and cholesterol on porcine sperm viability and capacitation status following cold shock or incubation. Mol. Reprod. Dev. 73, 638–50.CrossRefGoogle ScholarPubMed
Giraud, M.N., Motta, C., Boucher, D. & Grizard, G. (2000). Membrane fluidity predicts the outcome of cryopreservation of human spermatozoa. Hum. Reprod. 15, 2160–4.CrossRefGoogle ScholarPubMed
Hammerstedt, R.H., Graham, J.K. & Nolan, J.P. (1990). Cryopreservation of mammalian sperm: what we ask them to survive. J. Androl. 11, 73–88.CrossRefGoogle ScholarPubMed
Holt, W.V. (2000). Fundamental aspects of sperm cryobiology: the importance of species and individual differences. Theriogenology 53, 47–58.CrossRefGoogle ScholarPubMed
Howarth, B. Jr (1970). An examination for sperm capacitation in the fowl. Biol. Reprod. 3, 338–41.CrossRefGoogle ScholarPubMed
Konyali, C., Tomás, C., Blanch, E., Gómez, E.A., Graham, J.K. & Mocé, E. (2013). Optimizing conditions for treating goat semen with cholesterol-loaded cyclodextrins prior to freezing to improve cryosurvival. Cryobiology 67, 124–31.CrossRefGoogle ScholarPubMed
Lemoine, M., Grasseau, I., Brillard, J.P. & Blesbois, E. (2008). A reappraisal of the factors involved in in vitro initiation of the acrosome reaction in chicken spermatozoa. Reproduction 136, 391–9.CrossRefGoogle ScholarPubMed
Łukaszewicz, E., Jerysz, A., Partyka, A. & Siudzińska, A. (2008). Efficacy of evaluation of rooster sperm morphology using different staining methods. Res. Vet. Sci. 85, 583–88.CrossRefGoogle ScholarPubMed
Mazur, P. (1984). Freezing of living cells: mechanisms and implications. Am. J. Physiol. 247, 125–42.CrossRefGoogle ScholarPubMed
Mocé, E. & Graham, J.K. (2006). Cholesterol-loaded cyclodextrins added to fresh bull ejaculates improve sperm cryosurvival. J. Anim. Sci. 84, 826–33.CrossRefGoogle ScholarPubMed
Mocé, E., Blanch, E., Tomás, C. & Graham, J. (2010a). Use of cholesterol in sperm cryopreservation: present moment and perspectives to future. Reprod. Domest. Anim. 45, 57–66.CrossRefGoogle ScholarPubMed
Mocé, E., Purdy, P.H. & Graham, J.K. (2010b). Treating ram sperm with cholesterol-loaded cyclodextrins improves cryosurvival. Anim. Reprod. Sci. 118, 236–47.CrossRefGoogle ScholarPubMed
Moore, A.I., Squires, E.L. & Graham, J.K. (2005). Adding cholesterol to the stallion sperm plasma membrane improves cryosurvival. Cryobiology 51, 241–9.CrossRefGoogle Scholar
Moraes, E.A., Graham, J.K., Torres, C. A., Meyers, M. & Spizziri, B. (2010). Delivering cholesterol or cholestanol to bull sperm membranes improves cryosurvival. Anim. Reprod. Sci. 118, 148–54.CrossRefGoogle ScholarPubMed
Motamedi-Mojdehi, R., Roostaei-Ali Mehr, M. & Rajabi-Toustani, R. (2014). Effect of different levels of glycerol and cholesterol-loaded cyclodextrin on cryosurvival of ram spermatozoa. Reprod. Domest. Anim. 49, 65–70.CrossRefGoogle ScholarPubMed
Müller, K., Müller, P., Pincemy, G., Kurz, A. & Labbe, C. (2008). Characterization of sperm plasma membrane properties after cholesterol modification: consequences for cryopreservation of rainbow trout spermatozoa. Biol. Reprod. 78, 390–9.CrossRefGoogle ScholarPubMed
Murphy, C., English, A. M., Holden, S. A. & Fair, S. (2014) Cholesterol-loaded-cyclodextrins improve the post-thaw quality of stallion sperm. Anim. Reprod. Sci. 145, 123–9.CrossRefGoogle ScholarPubMed
Oliveira, C.H., Vasconcelos, A.B., Souza, F.A., Martins-Filho, O.A., Silva, M.X., Varago, F.C. & Lagares, M.A. (2010). Cholesterol addition protects membrane intactness during cryopreservation of stallion sperm. Anim. Reprod. Sci. 118, 194–200.CrossRefGoogle ScholarPubMed
Pamornsakda, T., Pojprasath, T., Suwimonteerabutr, J. & Tharasanit, T. (2011). Effects of cholesterol-loaded cyclodextrins on the quality of frozen–thawed equine epididymal sperm. Cryobiology 63, 90–5.CrossRefGoogle ScholarPubMed
Palleschi, S. & Silvestroni, L. (1996). Laurdan fluorescence spectroscopy reveals a single liquid-crystalline lipid phase and lack of thermotropic phase transitions in the plasma membrane of living human sperm. Biochim. Biophys. Acta. 1279, 197–202.CrossRefGoogle ScholarPubMed
Parasassi, T., Loiero, M., Raimondi, M., Ravagnan, G. & Gratton, E. (1993). Absence of lipid gel-phase domains in seven mammalian cell lines and in four primary cell types. Biochim. Biophys. Acta. 1153, 143–54.CrossRefGoogle ScholarPubMed
Parasassi, T., Di Stefano, M., Loiero, M., Ravagnan, G. & Gratton, E. (1994). Influence of cholesterol on phospholipid bilayers phase domains as detected by Laurdan fluorescence. Biophys. J. 66, 120–32.CrossRefGoogle ScholarPubMed
Parks, J.E. & Graham, J.K. (1992). Effects of cryopreservation procedures on sperm membranes. Theriogenology 38, 209–22.CrossRefGoogle ScholarPubMed
Parks, J.E. & Lynch, D.V. (1992). Lipid composition and thermotropic phase behavior of boar, bull, stallion, and rooster sperm membranes. Cryobiology 29, 255–66.CrossRefGoogle ScholarPubMed
Partyka, A., Niżański, W. & Łukaszewicz, E. (2010). Evaluation of fresh and frozen–thawed fowl semen by flow cytometry. Theriogenology 74, 1019–27.CrossRefGoogle ScholarPubMed
Partyka, A., Niżański, W., Bajzert, J., Łukaszewicz, E. & Ochota, M. (2013). The effect of cysteine and superoxide dismutase on the quality of post-thawed chicken sperm. Cryobiology 67, 132–6.CrossRefGoogle ScholarPubMed
Purdy, P.H. & Graham, J.K. (2004a). Effect of adding cholesterol to bull sperm membranes on sperm capacitation, the acrosome reaction, and fertility. Biol. Reprod. 71, 522–7.CrossRefGoogle ScholarPubMed
Purdy, P.H. & Graham, J.K. (2004b). Effect of cholesterol-loaded cyclodextrin on the cryosurvival of bull sperm. Cryobiology 48, 36–45.CrossRefGoogle ScholarPubMed
Purdy, P.H., Fox, M.H. & Graham, J.K. (2005). The fluidity of Chinese hamster ovary cell and bull sperm membranes after cholesterol addition. Cryobiology 51, 102–12.CrossRefGoogle ScholarPubMed
Sheriff, D.S. & Ali, E.F. (2010). Perspective on plasma membrane cholesterol efflux and spermatozoal function. J. Hum. Reprod. Sci. 3, 68–75.CrossRefGoogle ScholarPubMed
Sinha, S., Kumar, G.P. & Laloraya, M. (1994). Abnormal physical architecture of the lipophilic domains of human sperm membrane in oligospermia: a logical cause for low fertility profiles. Biochem. Biophys. Res. Commun. 198, 266–73.CrossRefGoogle ScholarPubMed
Spizziri, B.E., Fox, M.H., Bruemmer, J.E., Squires, E.L. & Graham, J.K. (2010). Cholesterol-loaded-cyclodextrins and fertility potential of stallions spermatozoa. Anim. Reprod. Sci. 118, 255–64.CrossRefGoogle ScholarPubMed
Tomás, C., Blanch, E., Hernandez, M., Gil, M.A., Roca, J., Vazquez, J. M., Martinez, E.A. & 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, 209–20.CrossRefGoogle ScholarPubMed
Tomás, C., Blanch, E., Fazeli, A. & Mocé, E. (2013). Effect of a pre-freezing treatment with cholesterol-loaded cyclodextrins on boar sperm longevity, capacitation dynamics, ability to adhere to porcine oviductal epithelial cells in vitro and DNA fragmentation dynamics. Reprod. Fertil. Dev. 25, 935–46.CrossRefGoogle ScholarPubMed
Travis, A.J. & Kopf, G.S. (2002). The role of cholesterol efflux in regulating the fertilization potential of mammalian spermatozoa. J. Clin. Invest. 110, 731–6.CrossRefGoogle ScholarPubMed
Tselutin, K., Narubina, L., Mavrodina, T. and Tur, B. (1995). Cryopreservation of poultry semen., Brit. Poult. Sci. 36 805–11.CrossRefGoogle ScholarPubMed
Visconti, P.E., Galantino-Homer, H., Ning, X., Moore, G.D., Valenzuela, J.P., Jorgez, C.J., Alvarez, J.G. & Kopf, G.S. (1999). Cholesterol efflux-mediated signal transduction in mammalian sperm. Beta-cyclodextrins initiate transmembrane signaling leading to an increase in protein tyrosine phosphorylation and capacitation. J. Biol. Chem. 274, 3235–42.CrossRefGoogle Scholar
Watson, P.F. (1995). Recent developments and concepts in the cryopreservation of spermatozoa and the assessment of their post-thawing function. Reprod. Fertil. Dev. 7, 871–91.CrossRefGoogle ScholarPubMed
Watson, P.F. (2000). The causes of reduced fertility with cryopreserved semen. Anim. Reprod. Sci. 60–61, 481–92.CrossRefGoogle ScholarPubMed
Yu, W., So, P.T., French, T. & Gratton, E. (1996). Fluorescence generalized polarization of cell membranes: a two-photon scanning microscopy approach. Biophys. J. 70, 626–36.CrossRefGoogle ScholarPubMed
Zeng, W.X. & Terada, T. (2001a). Effects of methyl-beta-cyclodextrin on cryosurvival of boar spermatozoa. J. Androl. 22, 111–8.CrossRefGoogle ScholarPubMed
Zeng, W.X. & Terada, T. (2001b). Protection of boar spermatozoa from cold shock damage by 2-hydroxypropyl-beta-cyclodextrin. Theriogenology 55, 615–27.CrossRefGoogle ScholarPubMed