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Seminal plasma fractions can protect common carp (Cyprinus carpio) sperm during cryopreservation

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Abstract

This study aimed to investigate the effect of fractionated seminal plasma on characteristics of common carp Cyprinus carpio cryopreserved sperm. Nanosep® centrifugal devices yielded four seminal plasma fractions with different total protein content ranging in molecular weight from less than 17 to almost 74 kDa. Each protein fraction was added to semen extender medium prior to freezing. Spermatozoon motility characteristics and DNA integrity were analyzed in supplemented and non-supplemented cryopreserved samples. The cryopreservation process strongly affected the swim-up sperm quality. Treatment with fractions 1, 2, 3, and 4 was associated with significantly higher spermatozoon motility rate and curvilinear velocity than seen in extender only, with highest values obtained with fraction 4 (78.21 ± 2.41% and 168.05 ± 4.46 μm/s, respectively). Significantly less DNA damage, expressed as percent tail DNA (12.23 ± 1.27) and olive tail moment (0.68 ± 0.12), was recorded in fraction 4. The findings indicated that addition of fractionated seminal plasma to cryopreservation medium can preserve the quality of common carp sperm. The protective effect of each fraction varied, suggesting the presence of distinct components exerting different effects on cryopreserved sperm function.

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References

  • Aurich JE, Kuhne A, Hoppe H, Aurich C (1996) Seminal plasma affects membrane integrity and motility of equine spermatozoa after cryopreservation. Theriogenology 46:791–797

    Article  CAS  Google Scholar 

  • Barrios B, Perez-Pe R, Gallego M, Tato A, Osada J, Muino-Blanco T, Cebrian-Perez JA (2000) Seminal plasma proteins revert the cold-shock damage on ram sperm membrane. Biol Reprod 63:1531–1537

    Article  CAS  Google Scholar 

  • Billard R (1983) Ultrastructure of trout spermatozoa: changes after dilution and deep freezing. Cell Tissue Res 228:205–218

    Article  CAS  Google Scholar 

  • Boryshpolets S, Sochorova D, Rodina M, Linhart O, Dzyuba B (2017) Cryopreservation of carp (Cyprinus carpio L.) sperm: impact of seeding and freezing rates on post–thaw outputs. Biopreserv Biobank 15(3):234–240

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  Google Scholar 

  • Cabrita E, Sarasquete C, Martinez-Paramo S, Robles V, Beirao J, Perez-Cerezales S, Herraez MP (2010) Cryopreservation of fish sperm: applications and perspectives. J Appl Ichthyol 26:623–635

    Article  CAS  Google Scholar 

  • Chen J, Godt D, Gunsalus K, Kiss I, Goldberg M, Laski FA (2001) Cofilin/ADF is required for cell motility during Drosophila ovary development and oogenesis. Nat Cell Biol 3:204–209

    Article  CAS  Google Scholar 

  • Dietrich MA, Ciereszko A (2018) Proteomic characterization of fresh spermatozoa and supernatant after cryopreservation in relation to freezability of carp (Cyprinus carpio L) semen. PLoS One 13:e0192972

    Article  Google Scholar 

  • Dietrich MA, Arnold GJ, Nynca J, Fröhlich T, Otte K, Ciereszko A (2014) Characterization of carp seminal plasma proteome in relation to blood plasma. Proteomics 98:218–232

    Article  CAS  Google Scholar 

  • Dietrich MA, Arnold GJT, Fröhlich KA, Otte G, Dietrich J, Ciereszko A (2015) Proteomic analysis of extracellular medium of cryopreserved carp (Cyprinus carpio L.) semen. Comp Biochem Physiol Part D: Genomics Proteomics 15:49–57

    CAS  Google Scholar 

  • Dietrich MA, Irnazarow I, Ciereszko A (2017) Proteomic identification of seminal plasma proteins related to the freezability of carp semen. J Proteome 162:52–61

    Article  CAS  Google Scholar 

  • Fu J, Li Y, Wang L, Zhen L, Yang Q, Li P, Li X (2017) Bovine serum albumin and skim-milk improve boar sperm motility by enhancing energy metabolism and protein modifications during liquid storage at 17 °C. Theriogenology 102:87–97

    Article  CAS  Google Scholar 

  • Gage MJG, Macfarlane CP, Yeates S, Ward RG, Searle JB, Parker GA (2004) Spermatozoal traits and sperm competition in Atlantic salmon: relative sperm velocity is the primary determinant of fertilization success. Curr Biol 14:44–47

    CAS  PubMed  Google Scholar 

  • Garcia-Lopez N, Ollero M, Cebrian-Perez JA, Muino-Blanco T (1996) Reversion of thermic-shock effect on ram spermatozoa by adsorption of seminal plasma proteins revealed by partition in aqueous two-phase systems. J Chromatogr B 680:137–143

    Article  CAS  Google Scholar 

  • Gómez-Fernández J, Gómez-Izquierdo E, Tomás C, González-Bulnes A, Sánchez-Sánchez R, de Mercado E (2012) Inclusion of seminal plasma in sperm cryopreservation of Iberian pig. Anim Reprod Sci 130:82–90

    Article  Google Scholar 

  • Hagedorn M, McCarthy M, Carter VL, Meyers SA (2012) Oxidative stress in zebrafish (Danio rerio) sperm. PLoS One 7(6):e39397

    Article  CAS  Google Scholar 

  • Hezavehei M, Sharafi M, Kouchesfahani HM, Henke R, Agarwa A, Esmaeili V, Shahverdi A (2018) Sperm cryopreservation: a review on current molecular cryobiology and advanced approaches. Reprod BioMed Online 37:327–339

    Article  CAS  Google Scholar 

  • Ivanova-Kicheva M, Dimox G (2011) Influence of selected seminal plasma proteins on mitochondrial integrity and speed parameters of ram sperm stored at low temperature. Biotechnol Biotec Eq 25:2591–2596

    Article  CAS  Google Scholar 

  • Kershaw-Young CM, Maxwell WM (2011) The effect of seminal plasma on alpaca sperm function. Theriogenology 76:1197–1206

    Article  CAS  Google Scholar 

  • Kopeika J, Kopeika E, Zhang T, Rawson DM, Holt WV (2004) Effect of DNA repair inhibitor (3-aminobenzamide) on genetic stability of loach (Misgurnus fossilis) embryos derived from cryopreserved sperm. Theriogenology 61:1661–1673

    Article  CAS  Google Scholar 

  • Labbe C, Martoriati A, Devaux A, Maisse G (2001) Effect of sperm cryopreservation on sperm DNA stability and progeny development in rainbow trout. Mol Reprod Dev 60:397–404

    Article  CAS  Google Scholar 

  • Lahnsteiner F (2007) Characterization of seminal plasma proteins stabilizing the sperm viability in rainbow trout (Oncorhynchus mykiss). Anim Reprod Sci 97:151–164

    Article  CAS  Google Scholar 

  • Lahnsteiner F, Mansour N, Berger B (2004) Seminal plasma proteins prolong the viability of rainbow trout (Oncorhynchus mykiss) spermatozoa. Theriogenology 62:801–808

    Article  CAS  Google Scholar 

  • Linhart O, Rodina M, Cosson J (2000) Cryopreservation of sperm in common carp Cyprinus carpio: sperm motility and hatching success of embryos. Cryobiology 41:241–250

    Article  CAS  Google Scholar 

  • Malo AF, Garde JJ, Soler AJ, Garcia AJ, Gomendio M, Roldan ERS (2005) Male fertility in natural populations of red deer is determined by sperm velocity and the proportion of normal spermatozoa. Biol Reprod 72:822–829

    Article  CAS  Google Scholar 

  • Mansour N, Richardson GF, McNiven MA (2008) Effect of seminal plasma protein on post-thaw viability and fertility of Arctic char spermatozoa. N Am J Aquac 70:92–97

    Article  Google Scholar 

  • Maxwell WMC, Long CR, Johnson LA (1998) The relationship between membrane status and fertility of boar spermatozoa after flow cytometric sorting in the presence or absence of seminal plasma. Reprod Fertil Develop 10:433–440

    Article  CAS  Google Scholar 

  • Megnagi B, Finkelstein M, Shabtay O, Breitbart H (2015) The role and importance of cofilin in human sperm capacitation and the acrosome reaction. Cell Tissue Res 362:665–675

    Article  CAS  Google Scholar 

  • Moore AI, Squires EL, Graham JK (2005) Effect of seminal plasma on the cryopreservation of equine spermatozoa. Theriogenology 63:2372–2381

    Article  CAS  Google Scholar 

  • Perez-Pe R, Barrios B, Muino-Blanco T, Cebrian-Perez JA (2001) Seasonal differences in ram seminal plasma revealed by partition in an aqueous two-phase system. J Chromatogr B Biomed Sci Appl 760:113–121

    Article  CAS  Google Scholar 

  • Rodina M, Dzyuba B, Boryshpolets S (2010) Zmrazování spermatu kapra obecného (Cyprinus carpio L.) pro potřeby uchování genofondu v praktických podmínkách. Vodňany: Edice metodik (technologická řada) FROV JU, 25

  • Rurangwa E, Kime DE, Ollevier F, Nash JP (2004) The measurement of sperm motility and factors affecting sperm quality in cultured fish. Aquaculture 234:1–28

    Article  Google Scholar 

  • Saravia F, Wallgren M, Johannisson A, Rodriguez-Martinez H (2007) Controlled cooling during semen cryopreservation does not induce capacitation of spermatozoa from two portions of the boar ejaculate. Int J Androl 30:485–499

    Article  CAS  Google Scholar 

  • Shaliutina-Kolesova A, Cosson J, Lebeda I, Gazo I, Shaliutina O, Dzyuba B, Linhart O (2015) The influence of cryoprotectants on sturgeon (Acipenser ruthenus) sperm quality, DNA integrity, antioxidant responses, and resistance to oxidative stress. Anim Reprod Sci 159:66–76

    Article  CAS  Google Scholar 

  • Shaliutina-Kolesova A, Xian M, Nian R (2019a) Antioxidant defence system in protein fractions of common carp (Cyprinus carpio) seminal plasma. Czech J Anim Sci 64:265–271

    Article  CAS  Google Scholar 

  • Shaliutina-Kolesova A, Dietrich M, Xian M, Nian R (2019b) Seminal plasma transferrin effects on cryopreserved common carp Cyprinus carpio sperm and comparison with bovine serum albumin and antifreeze proteins. Anim Reprod Sci 204:125–130

    Article  CAS  Google Scholar 

  • Tiersch TR, Yang H, Jenkins JA, Dong Q (2007) Sperm cryopreservation in fish and shellfish. In: Roldan ERS, Gomendio M (eds) Spermatology. Nottingham University Press, Nottingham, pp 493–508

    Google Scholar 

  • Vadnais ML, Roberts KP (2007) Effects of seminal plasma on cooling-induced capacitative changes in boar sperm. J Androl 28(3):416–422

    Article  CAS  Google Scholar 

  • Xin M, Sterba J, Shaliutina-Kolesova A, Dzyuba B, Lieskovska J, Boryshpolets S, Siddique MAM, Kholodnyy V, Lebeda I, Linhart O (2018) Protective role of antifreeze proteins on sterlet (Acipenser ruthenus) sperm during cryopreservation. Fish Physiol Biochem 44:1527–1533

    Article  CAS  Google Scholar 

  • Xu X-R, Zhu J-Q, Ye T, Wang C-L, Zhu Y-F, Dahms H-U, Jin F, Yang W-X (2013) Improvement of single-cell gel electrophoresis (SCGE) alkaline comet assay. Aquat Biol 18:293–295

    Article  Google Scholar 

  • Zhou B, Liu W, Siu WHL, O’Toole D, Lam PKS, Wu RSS (2006) Exposure of spermatozoa to duroquinone may impair reproduction of the common carp (Cyprinus carpio) through oxidative stress. Aquat Toxicol 77:136–142

    Article  CAS  Google Scholar 

Download references

Funding

This study is supported by the Ministry of Education, Youth and Sports of the Czech Republic, projects CENAKVA (LM2018099), and Biodiversity (CZ.02.1.01/0.0/0.0/16_025/0007370) as well as by the CAS President’s International Fellowship for Postdoctoral Researchers (2017 PB0060), National Natural Science Foundation of China (21676286), and Primary Research Development Plan of Shandong Province (2016GSF121006). The Lucidus Consultancy, UK is gratefully acknowledged for the English correction.

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Correspondence to Anna Shaliutina-Kolešová or Rui Nian.

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Shaliutina-Kolešová, A., Ashtiani, S., Xian, M. et al. Seminal plasma fractions can protect common carp (Cyprinus carpio) sperm during cryopreservation. Fish Physiol Biochem 46, 1461–1468 (2020). https://doi.org/10.1007/s10695-020-00805-9

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