Impact of various cryo-preservation steps on sperm rheotaxis and sperm kinematics in bull – Scientific Reports

  • Olaciregui, M. et al. Cryopreservation of epididymal stallion sperm. Cryobiology 68, 91–95 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Mota-Filho, A. C. et al. Cryopreservation of canine epididymal sperm using ACP-106c and TRIS. Cryobiology 69, 17–21 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Watson, P. F. The causes of reduced fertility with cryopreserved semen. Anim. Reprod. Sci. 60, 481–492 (2000).

    Article 
    PubMed 

    Google Scholar
     

  • Ramón, M. et al. Sperm cell population dynamics in ram semen during the cryopreservation process. PLoS ONE 8, e59189 (2013).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Holt, W. Basic aspects of frozen storage of semen. Anim. Reprod. Sci. 62, 3–22 (2000).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Parks, J. E. & Graham, J. K. Effects of cryopreservation procedures on sperm membranes. Theriogenology 38, 209–222 (1992).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Watson, P. The Effects of Cold Shock on Sperm Cell Membranes. Effects of Low Temperatures on Biological Membranes 189–218 (Springer, 1981).

  • Gao, D. et al. Andrology: Prevention of osmotic injury to human spermatozoa during addition and removal of glycerol. Hum. Reprod. 10, 1109–1122 (1995).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Watson, P. & Duncan, A. E. Effect of salt concentration and unfrozen water fraction on the viability of slowly frozen ram spermatozoa. Cryobiology 25, 131–142 (1988).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Watson, P. Recent developments and concepts in the cryopreservation of spermatozoa and the assessment of their post-thawing function. Reprod. Fertil. Dev. 7, 871–891 (1995).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • El-Sherry, T. M., Elsayed, M., Abdelhafez, H. K. & Abdelgawad, M. Characterization of rheotaxis of bull sperm using microfluidics. Integr. Biol. 6, 1111–1121 (2014).

    Article 

    Google Scholar
     

  • Nagata, M. B. et al. Bovine sperm selection procedure prior to cryopreservation for improvement of post-thawed semen quality and fertility. J. Anim. Sci. Biotechnol. 10, 1–14 (2019).

    Article 

    Google Scholar
     

  • De Martin, H. et al. Positive rheotaxis extended drop: A one-step procedure to select and recover sperm with mature chromatin for intracytoplasmic sperm injection. J. Assist. Reprod. Genet. 34, 1699–1708 (2017).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sarbandi, I. R., Lesani, A., Moghimi Zand, M. & Nosrati, R. Rheotaxis-based sperm separation using a biomimicry microfluidic device. Sci. Rep. 11, 18327 (2021).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Romero-Aguirregomezcorta, J. et al. Sperm selection by rheotaxis improves sperm quality and early embryo development. Reproduction 161, 343–352 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ataei, A., Lau, A. & Asghar, W. A microfluidic sperm-sorting device based on rheotaxis effect. Microfluidics Nanofluidics 25, 52 (2021).

    Article 
    CAS 

    Google Scholar
     

  • Hammerstedt, R. H., Graham, J. K. & Nolan, J. P. Cryopreservation of mammalian sperm: What we ask them to survive. J. Androl. 11, 73–88 (1990).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ardon, F. & Suarez, S. S. Cryopreservation increases coating of bull sperm by seminal plasma binder of sperm proteins BSP1, BSP3, and BSP5. Reproduction 146, 111–117 (2013).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Muiño, R., Peña, A., Rodríguez, A., Tamargo, C. & Hidalgo, C. Effects of cryopreservation on the motile sperm subpopulations in semen from Asturiana de los Valles bulls. Theriogenology 72, 860–868 (2009).

    Article 
    PubMed 

    Google Scholar
     

  • Yoon, S.-J., Kwon, W.-S., Rahman, M. S., Lee, J.-S. & Pang, M.-G. A novel approach to identifying physical markers of cryo-damage in bull spermatozoa. PLoS One 10, e0126232 (2015).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Du Sert, N. P. et al. Reporting animal research: Explanation and elaboration for the ARRIVE guidelines 20. PLoS Biol. 18, e3000411 (2020).

    Article 

    Google Scholar
     

  • El-sherry, T., Abdel-Ghani, M., Abou-Khalil, N., Elsayed, M. & Abdelgawad, M. Effect of pH on rheotaxis of bull sperm using microfluidics. Reprod. Domest. Anim. 52, 781–790 (2017).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Murphy, E. M. et al. Influence of bull age, ejaculate number, and season of collection on semen production and sperm motility parameters in Holstein Friesian bulls in a commercial artificial insemination centre. J. Anim. Sci. 96, 2408–2418 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Baracaldo, M. I., Barth, A. & Bertrand, W. Steps for Freezing Bovine Semen: From Semen Collection to the Liquid Nitrogen Tank (IVIS, 2006).

  • Nasser, G. A., Fath El-Bab, A. M., Abdel-Mawgood, A. L., Mohamed, H. & Saleh, A. M. CO2 laser fabrication of PMMA microfluidic double T-junction device with modified inlet-angle for cost-effective PCR application. Micromachines 10, 678 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Duffy, D. C., McDonald, J. C., Schueller, O. J. & Whitesides, G. M. Rapid prototyping of microfluidic systems in poly (dimethylsiloxane). Anal. Chem. 70, 4974–4984 (1998).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Haubert, K., Drier, T. & Beebe, D. PDMS bonding by means of a portable, low-cost corona system. Lab Chip 6, 1548–1549 (2006).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Moscovici, M., Chien, W.-Y., Abdelgawad, M. & Sun, Y. Electrical power free, low dead volume, pressure-driven pumping for microfluidic applications. Biomicrofluidics 4, 046501 (2010).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Munson, B., Young, D. & Okiishi, T. Fundamentals of Fluids Mechanics, Edisi 4 (Wiley, 2002).


    Google Scholar
     

  • Shah, R. & Al, L. Laminar Flow Forced Convection in Ducts. A Source Book Compact Heat Exchanger Analytical Data (Springer, 1978).

  • Elsayed, M., El-Sherry, T. M. & Abdelgawad, M. Development of computer-assisted sperm analysis plugin for analyzing sperm motion in microfluidic environments using Image-J. Theriogenology 84, 1367–1377 (2015).

    Article 
    PubMed 

    Google Scholar
     

  • Yoon, S. J. et al. Proteomic identification of cryostress in epididymal spermatozoa. J. Anim. Sci. Biotechnol. 7, 1–12 (2016).

    Article 

    Google Scholar
     

  • Hyakutake, T., Suzuki, H. & Yamamoto, S. Effect of non-Newtonian fluid properties on bovine sperm motility. J. Biomech. 48, 2941–2947 (2015).

    Article 
    PubMed 

    Google Scholar
     

  • Said, T. M., Gaglani, A. & Agarwal, A. Implication of apoptosis in sperm cryoinjury. Reprod. Biomed. Online 21, 456–462 (2010).

    Article 
    PubMed 

    Google Scholar
     

  • Sarıözkan, S., Bucak, M. N., Tuncer, P. B., Ulutaş, P. A. & Bilgen, A. The influence of cysteine and taurine on microscopic–oxidative stress parameters and fertilizing ability of bull semen following cryopreservation. Cryobiology 58, 134–138 (2009).

    Article 
    PubMed 

    Google Scholar
     

  • De Lamirande, E. & Gagnon, C. Reactive oxygen species and human spermatozoa: I. Effects on the motility of intact spermatozoa and on sperm axonemes. J. Androl. 13, 368–378 (1992).

    Article 
    PubMed 

    Google Scholar
     

  • Yoon, S.-J., Rahman, M. S., Kwon, W.-S., Park, Y.-J. & Pang, M.-G. Addition of cryoprotectant significantly alters the epididymal sperm proteome. PLoS One 11, e0152690 (2016).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Barbas, J., Leahy, T., Horta, A. & García-Herreros, M. Sperm kinematics and subpopulational responses during the cryopreservation process in caprine ejaculates. Cryobiology 82, 137–147 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Bravo, M. et al. Changes in tyrosine phosphorylation associated with true capacitation and capacitation-like state in boar spermatozoa. Mol. Reprod. Dev.: Incorporat. Gamete Res. 71, 88–96 (2005).

    Article 
    CAS 

    Google Scholar
     

  • Herreros, M. G. et al. Boar sperm velocity and motility patterns under capacitating and non-capacitating incubation conditions. Theriogenology 63, 795–805 (2005).

    Article 

    Google Scholar
     

  • Gil, M. et al. Morphometry of porcine spermatozoa and its functional significance in relation with the motility parameters in fresh semen. Theriogenology 71, 254–263 (2009).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Cormier, N., Sirard, M. A. & Bailey, J. L. Premature capacitation of bovine spermatozoa is initiated by cryopreservation. J. Androl. 18, 461–468 (1997).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Chamberland, A. et al. The effect of heparin on motility parameters and protein phosphorylation during bovine sperm capacitation. Theriogenology 55, 823–835 (2001).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Rahman, M. S., Lee, J.-S., Kwon, W.-S. & Pang, M.-G. Sperm proteomics: Road to male fertility and contraception. Int. J. Endocrinol. 2013, 1–11 (2013).

    Article 

    Google Scholar
     

  • Kwon, W.-S., Rahman, M. S. & Pang, M.-G. Diagnosis and prognosis of male infertility in mammal: The focusing of tyrosine phosphorylation and phosphotyrosine proteins. J. Proteome Res. 13, 4505–4517 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Farrell, P., Presicce, G., Brockett, C. & Foote, R. Quantification of bull sperm characteristics measured by computer-assisted sperm analysis (CASA) and the relationship to fertility. Theriogenology 49, 871–879 (1998).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Lemma, A. Effect of cryopreservation on sperm quality and fertility. Artif. Insemin. Farm Anim. 12, 191–216 (2011).


    Google Scholar
     

  • Roca, J. et al. Non-viable sperm in the ejaculate: Lethal escorts for contemporary viable sperm. Anim. Reprod. Sci. 169, 24–31 (2016).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Kantsler, V., Dunkel, J., Blayney, M. & Goldstein, R. E. Rheotaxis facilitates upstream navigation of mammalian sperm cells. Elife 3, e02403 (2014).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Miki, K. & Clapham, D. E. Rheotaxis guides mammalian sperm. Curr. Biol. 23, 443–452 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Marcos-Fu, H. C., Powers, T. R. & Stocker, R. Bacterial rheotaxis. Proc. Natl. Acad. Sci. 109, 4780–4785 (2012).

    Article 
    ADS 

    Google Scholar
     

  • Zhang, Z. et al. Human sperm rheotaxis: A passive physical process. Sci. Rep. 6, 23553 (2016).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Tung, C.-K. et al. Emergence of upstream swimming via a hydrodynamic transition. Phys. Rev. Lett. 114, 108102 (2015).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Mannowetz, N., Naidoo, N. M., Choo, S.-A.S., Smith, J. F. & Lishko, P. V. Slo1 is the principal potassium channel of human spermatozoa. elife 2, e01009 (2013).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Phillips, D. M. & Kalay, D. Mechanisms of flagellar motility deduced from backward-swimming bull sperm. J. Exp. Zool. 231, 109–116 (1984).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Alapati, R. et al. Comparison of the permeability properties and post-thaw motility of ejaculated and epididymal bovine spermatozoa. Cryobiology 59, 164–170 (2009).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Kantsler, V., Dunkel, J., Polin, M. & Goldstein, R. E. Ciliary contact interactions dominate surface scattering of swimming eukaryotes. Proc. Natl. Acad. Sci. 110, 1187–1192 (2013).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Purcell, E. M. Life at low Reynolds number. Am. J. Phys. 45, 3–11 (1977).

    Article 
    ADS 

    Google Scholar
     

  • Drescher, K., Goldstein, R. E., Michel, N., Polin, M. & Tuval, I. Direct measurement of the flow field around swimming microorganisms. Phys. Rev. Lett. 105, 168101 (2010).

    Article 
    ADS 
    PubMed 

    Google Scholar
     

  • Singh, A. V. et al. Mechanical coupling of puller and pusher active microswimmers influences motility. Langmuir 36, 5435–5443 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Daddi-Moussa-Ider, A., Lisicki, M. & Mathijssen, A. J. Tuning the upstream swimming of microrobots by shape and cargo size. Phys. Rev Appl. 14, 024071 (2020).

    Article 
    ADS 
    CAS 

    Google Scholar