Animal Reproduction (AR)
https://www.animal-reproduction.org/article/doi/10.1590/1984-3143-AR2022-0127
Animal Reproduction (AR)
ORIGINAL ARTICLE

Rapid thawing of frozen bull spermatozoa by transient exposure to 70 °C improves the viability, motility and mitochondrial health

Hai Thanh Nguyen; Son Quang Do; Rukmali Athurupana; Takuya Wakai; Hiroaki Funahashi

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Abstract

Abstract: Up to now, the definitive conclusion of the positive effects of rapid transient thawing at higher temperatures for shorter durations has not been obtained yet and is still under discussion due to some contradictory findings and limited assessment of post-thawed parameters. The purpose of the current study was to evaluate the effectiveness of rapid thawing in water at 70 °C by using various post-thawed parameters of frozen bull spermatozoa. Experiment 1, monitoring the change of temperature inside frozen bull straw thawed in water at different temperatures. Experiment 2, evaluation of various post-thawed characteristics of frozen bull spermatozoa thawed in water at different temperatures by using a computer-assisted sperm analysis, flow cytometry and immunocytochemistry. The time it took for the temperature inside the straw to warm up to 15 °C was nearly twice as faster when the straw was thawed in 70 °C water compared with 39 °C. Although there were differences among bulls, viability, motility, and mitochondrial membrane potential of spermatozoa thawed at 70 °C for 8 seconds and stabilized at 39 °C for 52 seconds were significantly higher than those of controls (thawed at 39 °C for 60 seconds) at 0 and 3 h after thawing. Just after thawing, however, there were no differences in acrosome integrity and distribution of phospholipase C zeta1, whereas mitochondrial reactive oxygen species production was significantly lower in spermatozoa thawed at 70 °C. From these results, we conclude that rapid thawing at 70 °C and then stabilization at 39 °C significantly improves viability, motility and mitochondrial health of bull spermatozoa rather than conventional thawing at 39 °C. The beneficial effect of rapid transient thawing could be due to shorter exposure to temperatures outside the physiological range, consequently maintaining mitochondrial health.

Keywords

bull semen, cryopreservation process, phospholipase C zeta1 (PLCZ1), temperature of thawing

References

Akaki Y, Yoshioka K, Noguchi M, Hoshi H, Funahashi H. Successful piglet production in a chemically defined system for in-vitro production of porcine embryos: dibutyryl cyclic amp and epidermal growth factor-family peptides support in-vitro maturation of oocytes in the absence of gonadotropins. J Reprod Dev. 2009;55(4):446-53. http://dx.doi.org/10.1262/jrd.20219. PMid:19444007.

Al-Badry KI. Effect of various thawing times and temperatures on frozen semen quality of Friesian bulls in Iraq. Int J Anim Vet Adv. 2012;4(6):384-8.

Amdani SN, Yeste M, Jones C, Coward K. Sperm factors and oocyte activation: current controversies and considerations. Biol Reprod. 2015;93(2):50. http://dx.doi.org/10.1095/biolreprod.115.130609. PMid:26157070.

Athurupana R, Ioki S, Funahashi H. Rapid thawing and stabilizing procedure improve postthaw survival and in vitro penetrability of boar spermatozoa cryopreserved with a glycerol-free trehalose-based extender. Theriogenology. 2015;84(6):940-7. http://dx.doi.org/10.1016/j.theriogenology.2015.05.033. PMid:26130006.

Bahmyari R, Zare M, Sharma R, Agarwal A, Halvaei I. The efficacy of antioxidants in sperm parameters and production of reactive oxygen species levels during the freeze-thaw process: A systematic review and meta-analysis. Andrologia. 2020;52(3):e13514. http://dx.doi.org/10.1111/and.13514. PMid:31967363.

Bulkeley EA, Foutouhi A, Wigney K, Santistevan AC, Collins C, McNabb B, Meyers S. Effects from disruption of mitochondrial electron transport chain function on bull sperm motility. Theriogenology. 2021;176:63-72. http://dx.doi.org/10.1016/j.theriogenology.2021.09.015. PMid:34571399.

Cerolini S, Maldjian A, Pizzi F, Gliozzi TM. Changes in sperm quality and lipid composition during cryopreservation of boar semen. Reproduction. 2001;121(3):395-401. http://dx.doi.org/10.1530/rep.0.1210395. PMid:11226065.

Correa JR, Rodriguez MC, Patterson DJ, Zavos PM. Thawing and processing of cryopreserved bovine spermatozoa at various temperatures and their effects on sperm viability, osmotic shock and sperm membrane functional integrity. Theriogenology. 1996;46(3):413-20. http://dx.doi.org/10.1016/0093-691X(96)00163-X. PMid:16727909.[REMOVED IF= FIELD]

Gonzalez-Castro RA, Amoroso-Sanches F, Stokes JE, Graham JK, Carnevale EM. Localisation of phospholipase Czeta1 (PLCZ1) and postacrosomal WW-binding protein (WBP2 N-terminal like) on equine spermatozoa and flow cytometry quantification of PLCZ1 and association with cleavage in vitro. Reprod Fertil Dev. 2019;31(12):1778-92. http://dx.doi.org/10.1071/RD19217. PMid:31597592.

Gürler H, Malama E, Heppelmann M, Calisici O, Leiding C, Kastelic JP, Bollwein H. Effects of cryopreservation on sperm viability, synthesis of reactive oxygen species, and DNA damage of bovine sperm. Theriogenology. 2016;86(2):562-71. http://dx.doi.org/10.1016/j.theriogenology.2016.02.007. PMid:27039074.

Hamano S. Practice: Cyropreservation of bull semen. In: Takahashi Y, editor. Artificial insemination manual for cattle and pig. Tokyo, Japan: Japan Artificial Insemination Association; 2016. p. 310-1.

Hammerstedt RH, Graham JK, Nolan JP. Cryopreservation of mammalian sperm: what we ask them to survive. J Androl. 1990;11(1):73-88. PMid:2179184.

Hezavehei M, Sharafi M, Fathi R, Shahverdi A, Gilani MAS. Membrane lipid replacement with nano-micelles in human sperm cryopreservation improves post-thaw function and acrosome protein integrity. Reprod Biomed Online. 2021;43(2):257-68. http://dx.doi.org/10.1016/j.rbmo.2021.05.005. PMid:34256996.

Ioki S, Wu QS, Takayama O, Motohashi HH, Wakai T, Funahashi H. A phosphodiesterase type-5 inhibitor, sildenafil, induces sperm capacitation and penetration into porcine oocytes in a chemically defined medium. Theriogenology. 2016;85(3):428-33. http://dx.doi.org/10.1016/j.theriogenology.2015.09.013. PMid:26443234.

Kashir J, Heynen A, Jones C, Durrans C, Craig J, Gadea J, Turner K, Parrington J, Coward K. Effects of cryopreservation and density-gradient washing on phospholipase C zeta concentrations in human spermatozoa. Reprod Biomed Online. 2011;23(2):263-7. http://dx.doi.org/10.1016/j.rbmo.2011.04.006. PMid:21665540.

Kasimanickam V, Kasimanickam R, Arangasamy A, Saberivand A, Stevenson JS, Kastelic JP. Association between mRNA abundance of functional sperm function proteins and fertility of Holstein bulls. Theriogenology. 2012;78(9):2007-2019.e2. http://dx.doi.org/10.1016/j.theriogenology.2012.07.016. PMid:23040061.

Lessard C, Parent S, Leclerc P, Bailey JL, Sullivan R. Cryopreservation alters the levels of the bull sperm surface protein P25b. J Androl. 2000;21(5):700-7. PMid:10975417.

Lyashenko A. Effect of different thawing procedures on the quality and fertility of the bull spermatozoa. Asian Pac J Reprod. 2015;4(1):17-21. http://dx.doi.org/10.1016/S2305-0500(14)60051-8.

Macías-García B, Gonzalez-Fernandez L, Gallardo-Bolanos JM, Pena FJ, Johannisson A, Morrell JM. Androcoll-E large selects a subset of live stallion spermatozoa capable of producing ROS. Anim Reprod Sci. 2012;132(1-2):74-82. http://dx.doi.org/10.1016/j.anireprosci.2012.03.017. PMid:22534021.

Marchetti P, Ballot C, Jouy N, Thomas P, Marchetti C. Influence of mitochondrial membrane potential of spermatozoa on in vitro fertilisation outcome. Andrologia. 2012;44(2):136-41. http://dx.doi.org/10.1111/j.1439-0272.2010.01117.x. PMid:21714802.

Mehmood S, Ahmed H, Shah SAH, Wattoo FH, Akhtar S, Andrabi SMH. Determination of an optimal membrane-permeable cryoprotectant addition and dilution protocol for water buffalo spermatozoa. Cryo Letters. 2017;38(3):239-49. PMid:28767747.

Moreau J, Fargeon S, Gatimel N, Parinaud J, Léandri RD. Expression of phospholipase PLC Zeta in human spermatozoa: impact of cryopreservation. Andrology. 2019;7(3):315-8. http://dx.doi.org/10.1111/andr.12593. PMid:30779311.

Nomikos M, Kashir J, Swann K, Lai FA. Sperm PLCζ: from structure to Ca2+ oscillations, egg activation and therapeutic potential. FEBS Lett. 2013;587(22):3609-16. http://dx.doi.org/10.1016/j.febslet.2013.10.008. PMid:24157362.

Ogata K, Imai A, Sato S, Nishino K, Watanabe S, Somfai T, Kobayashi E, Takeda K. Effects of reduced glutathione supplementation in semen freezing extender on frozen-thawed bull semen and in vitro fertilization. J Reprod Dev. 2022;68(1):53-61. http://dx.doi.org/10.1262/jrd.2021-079. PMid:34866119.

Ömür AD. Evaluation of the effects of photostimulation on freeze-thawed bull sperm cells in terms of reproductive potential. Pol J Vet Sci. 2022;25(2):249-59. PMid:35861955.

Petrunkina AM, Waberski D, Bollwein H, Sieme H. Identifying non-sperm particles during flow cytometric physiological assessment: a simple approach. Theriogenology. 2010;73(7):995-1000. http://dx.doi.org/10.1016/j.theriogenology.2009.12.006. PMid:20171719.

Rastegarnia A, Shahverdi A, Topraggaleh TR, Ebrahimi B, Shafipour V. Effect of different thawing rates on post-thaw viability, kinematic parameters and chromatin structure of buffalo (Bubalus bubalis) spermatozoa. Cell J. 2013;14(4):306-13. PMid:23577311.

Rezaie FS, Hezavehei M, Sharafi M, Shahverdi A. Improving the post-thaw quality of rooster semen using the extender supplemented with resveratrol. Poult Sci. 2021;100(9):101290. http://dx.doi.org/10.1016/j.psj.2021.101290. PMid:34311322.

Rodriguez AM, Silva CB, Macías-García B, Bolaños JMG, Tapia JA, Aparicio IM, Ortega-Ferrusola C, Peña FJ. Dimethylformamide improves the in vitro characteristics of thawed stallion spermatozoa reducing sublethal damage. Reprod Domest Anim. 2012;47(6):995-1002. http://dx.doi.org/10.1111/j.1439-0531.2012.02005.x. PMid:22384798.

Royere D, Barthelemy C, Hamamah S, Lansac J. Cryopreservation of spermatozoa: a 1996 review. Hum Reprod Update. 1996;2(6):553-9. http://dx.doi.org/10.1093/humupd/2.6.553. PMid:9111188.

Samper JC, Hellander JC, Crabo BG. Relationship between the fertility of fresh and frozen stallion semen and semen quality. J Reprod Fertil Suppl. 1991;44:107-14. PMid:1795253.

Sapanidou V, Lavrentiadou SN, Errico M, Panagiotidis I, Fletouris D, Efraimidis I, Zervos I, Taitzoglou I, Gasparrini B, Tsantarliotou M. The addition of crocin in the freezing medium extender improves post-thaw semen quality. Reprod Domest Anim. 2022;57(3):269-76. http://dx.doi.org/10.1111/rda.14049. PMid:34825745.

Sharafi M, Borghei-Rad SM, Hezavehei M, Shahverdi A, Benson JD. Cryopreservation of semen in domestic animals: A review of current challenges, applications, and prospective strategies. Animals (Basel). 2022;12(23):3271. http://dx.doi.org/10.3390/ani12233271. PMid:36496792.

Thanassoulas A, Swann K, Lai FA, Nomikos M. Sperm factors and egg activation: the structure and function relationship of sperm PLCZ1. Reproduction. 2022;164(1):F1-8. http://dx.doi.org/10.1530/REP-21-0477. PMid:35521907.

Upadhyay VR, Ramesh V, Dewry RK, Kumar G, Raval K, Patoliya P. Implications of cryopreservation on structural and functional attributes of bovine spermatozoa: an overview. Andrologia. 2021;53(8):e14154. http://dx.doi.org/10.1111/and.14154. PMid:34143907.

World Health Organization. WHO laboratory manual for the examination of human semen and sperm-cervical mucus interaction [Internet]. 4th ed. Cambridge: Cambridge University Press; 1999 [cited 2022 Dec 16]. Available from: https://www.aab.org/images/WHO 4th manual.pdf.

World Health Organization. WHO laboratory manual for the examination and processing of human semen [Internet]. 5th ed. Cambridge: Cambridge University Press; 2010 [cited 2022 Dec 16]. Available from: https://apps.who.int/iris/handle/10665/44261.

Yilmaz E, Ak K, Baran A. Effect of different thawing time and high temperature on frozen thawed bull semen traits. J Anim Vet Adv. 2019;18(7):239-45.
 


Submitted date:
12/16/2022

Accepted date:
07/13/2023

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