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Cryoprotective effects of low-density lipoproteins, trehalose and soybean lecithin on murine spermatogonial stem cells

Published online by Cambridge University Press:  14 September 2012

Peng Wang ,
Ying Li ,
Xiao-chen Hu ,
Xiao-Li Cai ,
Li-Peng Hou ,
Yan-Feng Wang ,
Jian-Hong Hu ,
Qing-Wang Li ,
Li-Juan Suo  and
Zhi-Guo Fan
...Show all authors
Peng Wang
Affiliation:
College of Animal Science and Technology, Northwest A & F University, Yangling, Shaanxi 712100, P.R. China.
Ying Li
Affiliation:
College of Animal Science and Technology, Northwest A & F University, Yangling, Shaanxi 712100, P.R. China.
Xiao-chen Hu
Affiliation:
College of Animal Science and Technology, Northwest A & F University, Yangling, Shaanxi 712100, P.R. China.
Xiao-Li Cai
Affiliation:
College of Animal Science and Technology, Northwest A & F University, Yangling, Shaanxi 712100, P.R. China.
Li-Peng Hou
Affiliation:
College of Animal Science and Technology, Northwest A & F University, Yangling, Shaanxi 712100, P.R. China.
Yan-Feng Wang
Affiliation:
College of Animal Science and Technology, Northwest A & F University, Yangling, Shaanxi 712100, P.R. China.
Jian-Hong Hu*
Affiliation:
College of Animal Science and Technology, Northwest A & F University, Yangling, Shaanxi 712100, P.R. China.
Qing-Wang Li*
Affiliation:
College of Animal Science and Technology, Northwest A & F University, Yangling, Shaanxi 712100, P.R. China.
Li-Juan Suo
Affiliation:
College of Animal Science and Technology, Northwest A & F University, Yangling, Shaanxi 712100, P.R. China.
Zhi-Guo Fan
Affiliation:
College of Animal Science and Technology, Northwest A & F University, Yangling, Shaanxi 712100, P.R. China.
Bo Zhang
Affiliation:
College of Animal Science and Technology, Northwest A & F University, Yangling, Shaanxi 712100, P.R. China.
*
All correspondence to: Jian-Hong Hu or Qing-Wang Li. College of Animal Science and Technology, Northwest A & F University, Yangling, Shaanxi 712100, P.R. China. Tel: +86 29 87092102. Fax: +86 29 87092164; e-mail: [email protected] or [email protected]
All correspondence to: Jian-Hong Hu or Qing-Wang Li. College of Animal Science and Technology, Northwest A & F University, Yangling, Shaanxi 712100, P.R. China. Tel: +86 29 87092102. Fax: +86 29 87092164; e-mail: [email protected] or [email protected]
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Summary

Spermatogonial stem cells (SSCs) have the ability to self-renew and offer a pathway for genetic engineering of the male germ line. Cryopreservation of SSCs has potential value for the treatment of male infertility, spermatogonial transplantation, and so on. In order to investigate the cryopreservation effects of different cryoprotectants on murine SSCs, 0.2 M of low-density lipoproteins (LDL), trehalose and soybean lecithin were added to the cryoprotective medium, respectively, and the murine SSCs were frozen at −80°C or −196°C. The results indicated that the optimal recovery rates of murine SSCs in the cryoprotective medium supplemented with LDL, trehalose and soybean lecithin were 92.53, 76.35 and 75.48% at −80°C, respectively. Compared with freezing at −196°C, the optimum temperature for improvement of recovery rates of frozen murine SSCs, cryopreservation in three different cryoprotectants at −80°C, were 17.11, 6.68 and 10.44% respectively. The recovery rates of murine SSCs in the cryoprotective medium supplemented with 0.2 M LDL were significantly higher than that of other cryoprotectants (P < 0.05). Moreover, the recovery rates were demonstrated to be greater at −80°C compared with at −196°C (P < 0.05). In conclusion, 0.2 M of LDL could significantly protect murine SSCs at −80°C. In the freezing–thawing process, LDL is responsible for the cryopreservation of murine SSCs because it can form a protective film at the surface of membranes. However, more research is needed to evaluate and understand the precise role of LDL during the freezing–thawing of SSCs.

Keywords

CryopreservationCryoprotectantsMurineRecovery ratesSpermatogonial stem cells
Type
Research Article
Information
Zygote , Volume 22 , Issue 2 , May 2014 , pp. 158 - 163
Copyright
Copyright © Cambridge University Press 2012 

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References

Aires, V.A., Hinsch, K.D., Mueller-Schloesser, F., Bogner, K., Mueller-Schloesser, S. & Hinsch, E. (2003). In vitro and in vivo comparison of egg yolk-based and soybean lecithin-based extenders for cryopreservation of bovine semen. Theriogenology 60, 269–79.Google Scholar
Aisen, E.G., Medina, V.H. & Venturino, A. (2002). Cryopreservation and post-thawed fertility of ram semen frozen in different trehalose concentrations. Theriogenology 57, 1801–8.Google Scholar
Aisen, E., Quintana, M., Medina, V., Morello, H. & Venturino, A. (2005). Ultramicroscopic and biochemical changes in ram spermatozoa cryopreserved with trehalose-based hypertonic extenders. Cryobiology 50, 239–49.Google Scholar
Amirat, L., Tainturier, D., Jeanneau, L., Thorin, C., Gerard, O., Courtens, J.L. & Anton, M. (2004). Bull semen in vitro fertility after cryopreservation using egg yolk LDL: a comparison with Optidyl (R), a commercial egg yolk extender. Theriogenology 61, 895–907.Google Scholar
Anton, M., Martinet, V., Dalgalarrondo, M., Beaurnal, V., David-Briand, E. & Rabesona, H. (2003). Chemical and structural characterisation of low-density lipoproteins purified from hen egg yolk. Food Chem. 83, 175–83.Google Scholar
Avarbock, M.R., Brinster, C.J. & Brinster, R.L. (1996). Reconstitution of spermatogenesis from frozen spermatogonial stem cells. Nat. Med. 2, 693–6.Google Scholar
Bahadur, G., Chatterjee, R. & Ralph, D. (2000). Testicular tissue cryopreservation in boys. Ethical and legal issues. Hum. Reprod. 15, 1416–20.Google Scholar
Benson, C.M.K., Benson, J.D. & Critser, J.K. (2008). An improved cryopreservation method for a mouse embryonic stem cell line. Cryobiology 56, 120–30.Google Scholar
Bergeron, A., Crete, M.H., Brindle, Y. & Manjunath, P. (2004). Low-density lipoprotein fraction from hen's egg yolk decreases the binding of the major proteins of bovine seminal plasma to sperm and prevents lipid efflux from the sperm membrane. Biol. Reprod. 70, 708–17.Google Scholar
Brinster, R.L. & Nagano, M. (1998). Spermatogonial stem cell transplantation, cryopreservation and culture. Semin. Cell Dev. Biol. 9, 401–9.Google Scholar
Bucak, M.N., Atessahin, A., Varish, O., Yuce, A., Tekin, N. & Akcay, A. (2007). The influence of trehalose, taurine, cysteamine and hyaluronan on ram semen – microscopic and oxidative stress parameters after freeze-thawing process. Theriogenology 67, 1060–7.Google Scholar
Buhr, M.M., Fiser, P., Bailey, J.L. & Curtis, E.F. (2001). Cryopreservation in different concentrations of glycerol alters boar sperm and their membranes. J. Androl. 22, 961–9.Google Scholar
Cookson, A.D., Thomas, A.N. & Foulkes, J.A. (1984). Immunochemical investigation of the interaction of egg-yolk lipoproteins with bovine spermatozoa. J. Reprod. Fertil. 70, 599–604.Google Scholar
Dym, M. (1994). Spermatogonial stem-cells of the testis. Proc. Natl. Acad. Sci. USA 91, 11287–9.Google Scholar
Dym, M. & Fawcett, D.W. (1971). Further observations on the numbers of spermatogonia, spermatocytes, and spermatids connected by intercellular bridges in the mammalian testis. Biol. Reprod. 4, 195–215.Google Scholar
Encinas, M., Crowder, R.J., Milbrandt, J. & Johnson, E.M. (2004). Tyrosine 981, a novel ret autophosphorylation site, binds c-Src to mediate neuronal survival. J. Biol. Chem. 279, 18262–9.Google Scholar
Ghosh, C.K. & Graham, W.A.G. (1987). Efficient and selective carbon-hydrogen activation by a tris(pyrazolyl)borate rhodium complex. J. Am. Chem. Soc. 109, 4726–7.CrossRefGoogle Scholar
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.Google Scholar
Gouk, S.S., Loh, Y.F.J., Kumar, S.D., Watson, P.F. & Kuleshova, L.L. (2011). Cryopreservation of mouse testicular tissue: prospect for harvesting spermatogonial stem cells for fertility preservation. Fertil. Steril. 95, 2399–403.Google Scholar
Graham, J.K. & Foote, R.H. (1987). Effect of several lipids, fatty acyl chain length and degree of unsaturation on the motility of bull spermatozoa after cold shock and freezing. Cryobiology 24, 42–52.Google Scholar
Herrid, M., Davey, R.J. & Hill, J.R. (2007). Characterization of germ cells from pre-pubertal bull calves in preparation for germ cell transplantation. Cell Tissue Res. 330, 321–9.Google Scholar
Hofmann, M.C. (2008). Gdnf signaling pathways within the mammalian spermatogonial stem cell niche. Mol. Cell. Endocrinol. 288, 95–103.Google Scholar
Holt, W.V. (2000). Basic aspects of frozen storage of semen. Anim. Reprod. Sci. 62, 3–22.Google Scholar
Hovatta, O. (2001). Cryopreservation of testicular tissue in young cancer patients. Hum. Reprod. Update 7, 378–83.Google Scholar
Hu, J.H., Li, Q.W., Gang, L., Chen, X.Y., Hai, Y., Zhang, S.S. & Wang, L.Q. (2006). The cryoprotective effect on frozen–thawed boar semen of egg yolk low density lipoproteins. Asian Australas. J. Anim. Sci. 19, 486–94.Google Scholar
Hu, J.H., Li, Q.W., Jiang, Z.L., Yang, H., Zhang, S.S. & Zhao, H.W. (2009). The cryoprotective effect of trehalose supplementation on boar spermatozoa quality. Reprod. Domest. Anim. 44, 571–5.Google Scholar
Hu, J.H., Li, Q.W., Zan, L.S., Jiang, Z.L., An, J.H., Wang, L.Q. & Jia, Y.H. (2010). The cryoprotective effect of low-density lipoproteins in extenders on bull spermatozoa following freezing–thawing. Anim. Reprod. Sci. 117, 11–7.Google Scholar
Hu, J.H., Jiang, Z.L., Lv, R.K., Li, Q.W., Zhang, S.S., Zan, L.S., Li, Y.K. & Li, X. (2011). The advantages of low-density lipoproteins in the cryopreservation of bull semen. Cryobiology 62, 83–7.Google Scholar
Jahnukainen, K., Ehmcke, J., Hergenrother, S.D. & Schlatt, S. (2007). Effect of cold storage and cryopreservation of immature non-human primate testicular tissue on spermatogonial stem cell potential in xenografts. Hum. Reprod. 22, 1060–7.Google Scholar
Jiang, Z.L., Li, Q.W., Hu, J.H., Li, W.Y., Zhao, H.W. & Zhang, S.S. (2007). Improvement of the quality of boar cryopreservation semen by supplementing with low density lipoprotein in diluents. Cryobiology 54, 301–4.Google Scholar
Jones, A.R., Chantrill, L.A. & Cokinakis, A. (1992). Metabolism of glycerol by mature boar spermatozoa. J. Reprod. Fertil. 194, 129–34.Google Scholar
Keros, V., Rosenlund, B., Hultenby, K., Aghajanova, L., Levkov, L. & Hovatta, O. (2005). Optimizing cryopreservation of human testicular tissue: comparison of protocols with glycerol, propanediol and dimethylsulphoxide as cryoprotectants. Hum. Reprod. 20, 1676–87.Google Scholar
Moussa, M., Martinet, V., Trimeche, A., Tainturier, D. & Anton, M. (2002). Low density lipoproteins extracted from hen egg yolk by an easy method: cryoprotective effect on frozen–thawed bull semen. Theriogenology 57, 1695–706.Google Scholar
Nagano, M.C., Ebata, K.T., Yeh, J.R. & Zhang, X.F. (2011). Soluble growth factors stimulate spermatogonial stem cell divisions that maintain a stem cell pool and produce progenitors in vitro. Exp. Cell Res. 317, 1319–29.Google Scholar
Prathalingam, N.S., Holt, W.V., Revell, S.G., Mirczuk, S., Fleck, R.A. & Watson, P.F. (2006). Impact of antifreeze proteins and antifreeze glycoproteins on bovine sperm during freeze-thaw. Theriogenology 66, 1894–1900.Google Scholar
Quinn, P.J., Chow, P.Y.W. & White, I.G. (1980). Evidence that phospholipids protect ram spermatozoa from cold shock at a plasma membrane site. J. Reprod. Fertil. 60, 403–7.Google Scholar
Redden, E., Davey, R., Borjigin, U., Hutton, K., Hinch, G., Hope, S., Hill, J. & Herrid, M. (2009). Large quantity cryopreservation of bovine testicular cells and its effect on enrichment of type A spermatogonia. Cryobiology 58, 190–5.Google Scholar
Schlatt, S. (2002). Spermatogonial stem cell preservation and transplantation. Mol. Cell. Endocrinol. 187, 107–11.Google Scholar
Seo, J.M., Sohn, M.Y., Suh, J.S., Atala, A., Yoo, J.J. & Shon, Y.H. (2011). Cryopreservation of amniotic fluid-derived stem cells using natural cryoprotectants and low concentrations of dimethylsulfoxide. Cryobiology 62, 167–73.Google Scholar
Storey, B.T., Noiles, E.E. & Thompson, K.A. (1998). Comparison of glycerol, other polyols, trehalose, and raffinose to provide a defined cryoprotectant medium for mouse sperm cryopreservation. Cryobiology 37, 46–58.Google Scholar
Thun, R., Hurtado, M. & Janett, F. (2002). Comparison of Biociphos-Plus (R) and TRIS-egg yolk extender for cryopreservation of bull semen. Theriogenology 57, 1087–94.Google Scholar
Vogel, E.W. & Natarajan, A.T. (1995). DNA damage and repair in somatic and germ cells in vivo. Mutat. Res.-Fundam. Mol. Mech. Mutagen. 330, 183–208.Google Scholar
Waterhouse, K.E., Hofmo, P.O., Tverdal, A. & Miller, R.R. (2006). Within and between breed differences in freezing tolerance and plasma membrane fatty acid composition of boar sperm. Reproduction 131, 887–94.Google Scholar