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HSP90 expression correlation with the freezing resistance of bull sperm

Published online by Cambridge University Press:  14 March 2013

Peng Wang ,
Yan-Feng Wang ,
Hong Wang ,
Chun-Wei Wang ,
Lin-Sen Zan ,
Jian-Hong Hu ,
Qing-Wang Li ,
Yong-Hong Jia  and
Guo-Ji Ma
Peng Wang
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.
Hong Wang
Affiliation:
College of Animal Science and Technology, Northwest A&F University, Yangling, Shaanxi 712100, P.R. China.
Chun-Wei Wang
Affiliation:
College of Animal Science and Technology, Northwest A&F University, Yangling, Shaanxi 712100, P.R. China.
Lin-Sen Zan
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.
Yong-Hong Jia
Affiliation:
Domestic Animal Improving Station, Jingyang, Shaanxi 713702, P.R. China.
Guo-Ji Ma
Affiliation:
Domestic Animal Improving Station, Jingyang, Shaanxi 713702, P.R. China.
*
Corresponding author: 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 address: hjh19732008@126.com or liqingwangysu@yahoo.com.cn
Corresponding author: 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 address: hjh19732008@126.com or liqingwangysu@yahoo.com.cn
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Summary

To date, there has been little improvement in cryopreservation of bull sperm due to lack of understanding of the freezing mechanisms. Therefore, this study set out to investigate expression levels of fertility-associated proteins in bull sperm, and in particular the relationship between the 90 kDa heat-shock protein (HSP90) and the sperm characteristics after freezing–thawing. Semen was collected from eight Holstein bulls by artificial vagina. Characteristics of these fresh semen, including sperm motility, morphology, viability and concentration, were evaluated. Sperm quality was also assessed after freezing–thawing. Eight ejaculates were divided into two groups based on freezing resistance and sperm motility. Sperm proteins were extracted and sodium dodecyl sulphate polyacrylamide gel electrophoresis (SDS-PAGE) analysis and western blotting were performed. SDS-PAGE results showed that there was substantial diversity in 90 kDa proteins in the frozen–thawed sperm and HSP90 was confirmed as one of the 90 kDa proteins by western blot. This study indicated that HSP90 expression correlated positively with sperm quality. The amount of expressed 90 kDa proteins in the high freezing resistance (HFR) group was significantly higher than that in the low freezing resistance (LFR) group (P < 0.05). Thus, higher expression of HSP90 could probably lead to the higher motility and freezing resistance of sperm found after freezing–thawing. Therefore, we concluded that level of HSP90 expression could be used to predict reliably and simply the freezing resistance of bull sperm.

Keywords

BullFreezing resistanceHSP90 expressionSperm characteristics
Type
Research Article
Information
Zygote , Volume 22 , Issue 2 , May 2014 , pp. 239 - 245
Copyright
Copyright © Cambridge University Press 2013 

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References

Aboagla, E.M.E. & Terada, T. (2003). Trehalose-enhanced fluidity of the goat sperm membrane and its protection during freezing. Biol. Reprod. 69, 1245–50.CrossRefGoogle ScholarPubMed
Alvarez, J.G. & Storey, B.T. (1992). Evidence for increased lipid peroxidative damage and loss of superoxide-dismutase activity as a mode of sublethal cryodamage to human sperm during cryopreservation. J. Androl. 13, 232–41.CrossRefGoogle ScholarPubMed
Borkovich, K.A., Farrelly, F.W., Finkelstein, D.B., Taulien, J. & Lindquist, S. (1989). Hsp82 is an essential protein that is required in higher concentrations for growth of cells at higher temperatures. Mol. Cell Biol. 9, 3919–30.Google ScholarPubMed
Cao, W.L., Wang, Y.X., Xiang, Z.Q. & Li, Z. (2003). Cryopreservation-induced decrease in heat-shock protein 90 in human spermatozoa and its mechanism. Asian J. Androl. 5, 43–6.Google ScholarPubMed
Casas, I., Sancho, S., Briz, A., Pinart, E., Bussalleu, E., Yeste, M. & Bonet, S. (2009). Freezability prediction of boar ejaculates assessed by functional sperm parameters and sperm proteins. Theriogenology 72, 930–48.CrossRefGoogle ScholarPubMed
Casas, I., Sancho, S., Ballester, J., Briz, M., Pinart, E., Bussalleu, E., Yeste, M., Fabrega, A., Rodriguez-Gil, J.E. & Bonet, S. (2010). The HSP90AA1 sperm content and the prediction of the boar ejaculate freezability. Theriogenology 74, 940–50.CrossRefGoogle ScholarPubMed
Desrosiers, P., Legare, C., Leclerc, P. & Sullivan, R. (2006). Membranous and structural damage that occur during cryopreservation of human sperm may be time-related events. Fertil. Steril. 85, 1744–52.Google Scholar
Dixit, V.D. & Parvizi, N. (2001). Nitric oxide and the control of reproduction. Anim. Reprod. Sci. 65, 1–16.Google Scholar
Ecroyd, H., Jones, R.C. & Aitken, R.J. (2003). Tyrosine phosphorylation of HSP-90 during mammalian sperm capacitation. Biol. Reprod. 69, 1801–7.Google Scholar
Flores, E., Cifuentes, D., Fernandez-Novell, J.M., Medrano, A., Bonet, S., Briz, M.D., Pinart, E., Pena, A., Rigau, T. & Rodriguez-Gil, J.E. (2008). Freeze-thawing induces alterations in the protamine-1/DNA overall structure in boar sperm. Theriogenology 69, 1083–94.CrossRefGoogle ScholarPubMed
Freeman, B.C. & Morimoto, R.I. (1996). The human cytosolic molecular chaperones hsp90, Hsp70 (hsc70) and hdj-1 have distinct roles in recognition of a non-native protein and protein refolding. EMBO J. 15, 2969–79.CrossRefGoogle ScholarPubMed
Fukuda, A., Osawa, T., Oda, H., Tanaka, T., Toyokuni, S. & Uchida, K. (1996). Oxidative stress response in iron-induced acute nephrotoxicity: Enhanced expression of heat-shock protein 90. Biochem. Biophys. Res. Co. 219, 76–81.Google Scholar
Garcia-Cardena, G., Fan, R., Shah, V., Sorrentino, R., Cirino, G., Papapetropoulos, A. & Sessa, W.C. (1998). Dynamic activation of endothelial nitric oxide synthase by Hsp90. Nature 392, 821–4.Google Scholar
Gaviraghi, A., Deriu, F., Soggiu, A., Galli, A., Bonacina, C., Bonizzi, L. & Roncada, P. (2010). Proteomics to investigate fertility in bulls. Vet. Res. Commun. 34, S33–6.Google Scholar
Guthrie, H.D., Welch, G.R. & Long, J.A. (2008). Mitochondrial function and reactive oxygen species action in relation to boar motility. Theriogenology 70, 1209–15.CrossRefGoogle ScholarPubMed
Gutierrez-Perez, O., de Lourdes Juarez-Mosqueda, M., Uribe Carvajal, S. & Trujillo Ortega, M.E. (2009). Boar spermatozoa cryopreservation in low glycerol/trehalose enriched freezing media improves cellular integrity. Cryobiology 58, 287–92.Google Scholar
Hu, J.H., Zhao, X.L, Tian, W.Q., Zan, L.S. & Li, Q.W. (2011). Effects of vitamin E supplementation in the extender on frozen-thawed bovine semen preservation. Animal 5, 107–12.CrossRefGoogle ScholarPubMed
Huang, S.Y., Kuo, Y.H., Lee, W.C., Tsou, H.L., Lee, Y.P., Chang, H.L., Wu, J.J. & Yang, P.C. (1999). Substantial decrease of heat-shock protein 90 precedes the decline of sperm motility during cooling of boar spermatozoa. Theriogenology 51, 1007–16.Google Scholar
Huang, S.Y., Kuo, Y.H., Tsou, H.L., Lee, Y.P., King, Y.T., Huang, H.C., Yang, P.C. & Lee, W.C. (2000). The decline of porcine sperm motility by geldanamycin, a specific inhibitor of heat- shock protein 90 (HSP90). Theriogenology 53, 1177–84.Google Scholar
Osinowo, O.A., Bale, J.O., Oyedipe, E.O. & Eduvie, L.O. (1982). Motility and eosin uptake of formaldehyde-treated ram spermatozoa. J. Reprod. Fertil. 65, 389–94.Google Scholar
Lewis, S.E., Donnelly, E.T., Sterling, E.S., Kennedy, M.S., Thompson, W. & Chakravarthy, U. (1996). Nitric oxide synthase and nitrite production in human spermatozoa: evidence that endogenous nitric oxide is beneficial to sperm motility. Mol. Hum. Reprod. 2, 873–8.CrossRefGoogle ScholarPubMed
Martin, G., Cagnon, N., Sabido, O., Sion, B., Grizard, G., Durand, P. & Levy, R. (2007). Kinetics of occurrence of some features of apoptosis during the cryopreservation process of bovine spermatozoa. Hum. Reprod. 22, 380–8.CrossRefGoogle ScholarPubMed
Pearl, L.H. & Prodromou, C. (2000). Structure and in vivo function of Hsp90. Curr. Opin. Struct. Biol. 10, 46–51.Google Scholar
Peddinti, D., Nanduri, B., Kaya, A., Feugang, J.M., Burgess, S.C. & Memili, E. (2008). Comprehensive proteomic analysis of bovine spermatozoa of varying fertility rates and identification of biomarkers associated with fertility. Bmc. Syst. Biol. 2, 19.Google Scholar
Pena, F.J., Rodriguez Martinez, H., Tapia, J.A., Orteag Ferrusola, C., Gonzalez Fernandez, L. & Macias Garcia, B. (2009). Mitochondria in mammalian sperm physiology and pathology: a review. Reprod. Domest. Anim. 44, 345–9.CrossRefGoogle ScholarPubMed
Powers, M.V., Clarke, P.A. & Workman, P. (2008). Dual targeting of HSC70 and HSP72 inhibits HSP90 function and induces tumor-specific apoptosis. Cancer Cell 14, 250–62.CrossRefGoogle ScholarPubMed
Pratt, W.B. (1998). The hsp90-based chaperone system: Involvement in signal transduction from a variety of hormone and growth factor receptors. Proc. Soc. Exp. Biol. Med. 217, 420–34.Google Scholar
Pratt, W.B., Galigniana, M.D., Harrell, J.M. & DeFranco, D.B. (2004). Role of hsp90 and the hsp90-binding immunophilins in signalling protein movement. Cell Signal. 16, 857–72.Google Scholar
Prodromou, C., Roe, S.M., Obrien, R., Ladbury, J.E., Piper, P.W. & Pearl, L.H. (1997). Identification and structural characterization of the ATP/ADP-binding site in the Hsp90 molecular chaperone. Cell 90, 65–75.Google Scholar
Roca, J., Hernandez, M., Carvajal, G., Vazquez, J.M. & Martinez, E.A. (2006). Factors influencing boar sperm cryosurvival. J. Anim. Sci. 84: 2692–9.CrossRefGoogle ScholarPubMed
Ruiz-Pesini, E., Diez, C., Lapena, A.C., Perez-Martos, A., Montoya, J., Alvarez, E., Arenas, J. & Lopez-Perez, M.J. (1998). Correlation of sperm motility with mitochondrial enzymatic activities. Clin. Chem. 44, 1616–20.Google Scholar
Vijayaraghavan, S., Stephens, D.T., Trautman, K., Smith, G.D., Khatra, B., Silva, E. & Greengard, P. (1996). Sperm motility development in the epididymis is associated with decreased glycogen synthase kinase-3 and protein phosphatase 1 activity. Biol. Reprod. 54, 709–18.CrossRefGoogle ScholarPubMed
Wang, P.T., Shu, Z.Q., He, L.Q., Cui, X.D., Wang, Y.Z. & Gao, D.Y. (2005). The pertinence of expression of heat-shock proteins (HSPs) to the efficacy of cryopreservation in HELAS. Cryoletters 26, 7–16.Google Scholar
Watson, P.F. (1981). The effects of cold shock on sperm cell membranes. In: Effects of Low Temperature on Biological Membranes (Morris, G.J. & Clarke, A., eds). London: Academic Press, pp. 189–218.Google Scholar
Yue, L., Karr, T.L., Nathan, D.F., Swift, H., Srinivasan, S. & Lindquist, S. (1999). Genetic analysis of viable Hsp90 alleles reveals a critical role in Drosophila spermatogenesis. Genetics 151, 1065–79.CrossRefGoogle ScholarPubMed