Changes in the Cellular Distribution of Tyrosine Phosphorylation and Its Relationship with the Acrosomal Exocytosis and Plasma Membrane Integrity During In Vitro Capacitation of Frozen/Thawed Bull Spermatozoa

Overview

Journal Int J Mol Sci

Publisher MDPI

Specialties Biochemistry
Chemistry
Molecular Biology

Date 2020 Apr 25

PMID 32326382

Citations 10

Authors

Sara Ruiz-Diaz

Sergio Grande-Perez

Sol Arce-Lopez

Carolina Tamargo

Carlos Olegario Hidalgo

Serafin Perez-Cerezales

Affiliations

Soon will be listed here.

Abstract

During sperm capacitation, intracellular signaling leads to protein tyrosine phosphorylation (PTP) of multiple cellular structures. However, the connection of this molecular signaling to the physiology of capacitated spermatozoa is not completely understood. This is the case of the short lifespan of capacitated spermatozoa and their increased susceptibility to initiate acrosomal exocytosis (AE) during incubation. Herein, by employing frozen/thawed bull spermatozoa, we aimed to study the relationship between PTP with AE and with plasma membrane integrity (PMI) at the cellular level. For this, we employed double staining following immunofluorescence for PTP combined with fluorescence probes for the acrosome (PNA-FITC) and PMI (LIVE/DEAD Fixable Dead Cell Stain Kit). Our results revealed that the presence of PTP at sperm head was less abundant in the sperm fraction that triggered the AE after 3 h of incubation under capacitating conditions, or by its induction with calcium ionophore, compared to the unreacted fraction. Furthermore, PTP at the equatorial region of the head (PTP-EQ) was enriched in the fraction showing damaged membrane while induction of AE with calcium ionophore did not alter the PMI and its relation to PTP-EQ. These results suggest that spontaneous AE and induced AE trigger similar cellular events regarding PTP and the spermatozoa showing PTP-EQ are more prone to suffer plasma membrane damage.

Citing Articles

Integrating proteomics and metabolomics to evaluate impact of semen collection techniques on the quality and cryotolerance of goat semen.

Li C, Liang J, Allai L, Badaoui B, Shao Q, Ouyang Y Sci Rep. 2024; 14(1):29489.

PMID: 39604559 PMC: 11603158. DOI: 10.1038/s41598-024-80556-2.

Revisiting the Injury Mechanism of Goat Sperm Caused by the Cryopreservation Process from a Perspective of Sperm Metabolite Profiles.

Li C, Lv C, Larbi A, Liang J, Yang Q, Wu G Int J Mol Sci. 2024; 25(16).

PMID: 39201798 PMC: 11354876. DOI: 10.3390/ijms25169112.

The antioxidant effects of butylated hydroxytoluene on cryopreserved goat sperm from a proteomic perspective.

Li C, Allai L, Liang J, Lv C, Zhao X, Ni X PeerJ. 2024; 12:e17580.

PMID: 38978759 PMC: 11229688. DOI: 10.7717/peerj.17580.

Bull spermatozoa selected by thermotaxis exhibit high DNA integrity, specific head morphometry, and improve ICSI outcome.

Ruiz-Diaz S, Mazzarella R, Navarrete-Lopez P, Fernandez-Gonzalez R, de Frutos C, Maroto M J Anim Sci Biotechnol. 2023; 14(1):11.

PMID: 36627704 PMC: 9832681. DOI: 10.1186/s40104-022-00810-3.

Quantitative phosphoproteomics analyses reveal the regulatory mechanisms related to frozen-thawed sperm capacitation and acrosome reaction in yak ().

Zhang R, Liang C, Guo X, Bao P, Pei J, Wu F Front Physiol. 2022; 13:1013082.

PMID: 36277216 PMC: 9583833. DOI: 10.3389/fphys.2022.1013082.

References

Gadella B, Harrison R . The capacitating agent bicarbonate induces protein kinase A-dependent changes in phospholipid transbilayer behavior in the sperm plasma membrane. Development. 2000; 127(11):2407-20. DOI: 10.1242/dev.127.11.2407. View

Visconti P, Bailey J, Moore G, Pan D, Kopf G . Capacitation of mouse spermatozoa. I. Correlation between the capacitation state and protein tyrosine phosphorylation. Development. 1995; 121(4):1129-37. DOI: 10.1242/dev.121.4.1129. View

Herz Z, Northey D, Lawyer M, First N . Acrosome reaction of bovine spermatozoa in vivo: sites and effects of stages of the estrous cycle. Biol Reprod. 1985; 32(5):1163-8. DOI: 10.1095/biolreprod32.5.1163. View

Jankovicova J, Michalkova K, Secova P, Horovska L, Manaskova-Postlerova P, Antalikova J . Evaluation of protein phosphorylation in bull sperm during their maturation in the epididymis. Cell Tissue Res. 2017; 371(2):365-373. DOI: 10.1007/s00441-017-2705-x. View

Watson P . Recent developments and concepts in the cryopreservation of spermatozoa and the assessment of their post-thawing function. Reprod Fertil Dev. 1995; 7(4):871-91. DOI: 10.1071/rd9950871. View

Aitken R, Baker M, Nixon B . Are sperm capacitation and apoptosis the opposite ends of a continuum driven by oxidative stress?. Asian J Androl. 2015; 17(4):633-9. PMC: 4492056. DOI: 10.4103/1008-682X.153850. View

Lybaert P, Danguy A, Leleux F, Meuris S, Lebrun P . Improved methodology for the detection and quantification of the acrosome reaction in mouse spermatozoa. Histol Histopathol. 2009; 24(8):999-1007. DOI: 10.14670/HH-24.999. View

Deppe M, Morales P, Sanchez R . Effect of protease inhibitors on the acrosome reaction and sperm-zona pellucida binding in bovine sperm. Reprod Domest Anim. 2008; 43(6):713-9. DOI: 10.1111/j.1439-0531.2007.00977.x. View

Giaretta E, Munerato M, Yeste M, Galeati G, Spinaci M, Tamanini C . Implementing an open-access CASA software for the assessment of stallion sperm motility: Relationship with other sperm quality parameters. Anim Reprod Sci. 2016; 176:11-19. DOI: 10.1016/j.anireprosci.2016.11.003. View

10.

Pons-Rejraji H, Bailey J, Leclerc P . Cryopreservation affects bovine sperm intracellular parameters associated with capacitation and acrosome exocytosis. Reprod Fertil Dev. 2009; 21(4):525-37. DOI: 10.1071/RD07170. View

11.

Bajpai M, Doncel G . Involvement of tyrosine kinase and cAMP-dependent kinase cross-talk in the regulation of human sperm motility. Reproduction. 2003; 126(2):183-95. DOI: 10.1530/rep.0.1260183. View

12.

Lishko P, Botchkina I, Kirichok Y . Progesterone activates the principal Ca2+ channel of human sperm. Nature. 2011; 471(7338):387-91. DOI: 10.1038/nature09767. View

13.

Botta D, Arruda R, Watanabe Y, Balieiro J, Romanello N, Barreto A . Influence of post-thawing thermal environment on bovine sperm characteristics and in vitro fertility. Andrologia. 2019; 51(6):e13266. DOI: 10.1111/and.13266. View

14.

Chamberland A, Fournier V, Tardif S, Sirard M, Sullivan R, Bailey J . The effect of heparin on motility parameters and protein phosphorylation during bovine sperm capacitation. Theriogenology. 2001; 55(3):823-35. DOI: 10.1016/s0093-691x(01)00446-0. View

15.

Grasa P, Cebrian-Perez J, Muino-Blanco T . Signal transduction mechanisms involved in in vitro ram sperm capacitation. Reproduction. 2006; 132(5):721-32. DOI: 10.1530/rep.1.00770. View

16.

Urner F, Leppens-Luisier G, Sakkas D . Protein tyrosine phosphorylation in sperm during gamete interaction in the mouse: the influence of glucose. Biol Reprod. 2001; 64(5):1350-7. DOI: 10.1095/biolreprod64.5.1350. View

17.

Neild D, Gadella B, Aguero A, Stout T, Colenbrander B . Capacitation, acrosome function and chromatin structure in stallion sperm. Anim Reprod Sci. 2005; 89(1-4):47-56. DOI: 10.1016/j.anireprosci.2005.06.017. View

18.

Naresh S, Atreja S . The protein tyrosine phosphorylation during in vitro capacitation and cryopreservation of mammalian spermatozoa. Cryobiology. 2015; 70(3):211-6. DOI: 10.1016/j.cryobiol.2015.03.008. View

19.

Gangwar D, Atreja S . Signalling Events and Associated Pathways Related to the Mammalian Sperm Capacitation. Reprod Domest Anim. 2015; 50(5):705-11. DOI: 10.1111/rda.12541. View

20.

Yanagimachi R . Mammalian sperm acrosome reaction: where does it begin before fertilization?. Biol Reprod. 2011; 85(1):4-5. DOI: 10.1095/biolreprod.111.092601. View