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During capacitation in bull spermatozoa, actin and PLC-ζ undergo dynamic interactions

Published online by Cambridge University Press:  20 September 2017

Itzayana Mejía-Flores
Affiliation:
Departamento de Morfología, Facultad de Medicina Veterinaria y Zootecnia, UNAM
Natalia Chiquete-Félix
Affiliation:
Instituto de Fisiología Celular, UNAM, C.U., CDMX, 04510, México.
Icela Palma-Lara
Affiliation:
Escuela Superior de Medicina, IPN, Plan de San Luis y Díaz Mirón, Col. Santo Tomás, CDMX, 11340, México.
Salvador Uribe-Carvajal
Affiliation:
Instituto de Fisiología Celular, UNAM, C.U., CDMX, 04510, México.
María de Lourdes Juárez-Mosqueda*
Affiliation:
Departamento de Morfología, Facultad de Medicina Veterinaria y Zootecnia, UNAM, C.U., CDMX, 04510, México.
*
All correspondence to: María de Lourdes Juárez-Mosqueda. Departamento de Morfología, Facultad de Medicina Veterinaria y Zootecnia, UNAM, C.U., CDMX, 04510, México. Tel:/Fax: +52 55 56225910. E-mail: [email protected]

Summary

The migration pattern of sperm-specific phospholipase C-ζ (PLC-ζ) was followed and the role of this migration in actin cytoskeleton dynamics was determined. We investigated whether PLC-ζ exits sperm, opening the possibility that PLC-ζ is the ‘spermatozoidal activator factor’ (SOAF). As capacitation progresses, the highly dynamic actin cytoskeleton bound different proteins to regulate their location and activity. PLC-ζ participation at the start of fertilization was established. In non-capacitated spermatozoa, PLC-ζ is in the perinuclear theca (PT) and in the flagellum, therefore it was decided to determine whether bovine sperm actin interacts with PLC-ζ to direct its relocation as it progresses from non-capacitated (NC) to capacitated (C) and to acrosome-reacted (AR) spermatozoa. PLC-ζ interacted with actin in NC spermatozoa (100%), PLC-ζ levels decreased in C spermatozoa to 32% and in AR spermatozoa to 57% (P < 0.001). The level of actin/PLC-ζ interaction was twice as high in G-actin (P < 0.001) that reflected an increase in affinity. Upon reaching the AR spermatozoa, PLC-ζ was partially released from the cell. It was concluded that actin cytoskeleton dynamics control the migration of PLC-ζ during capacitation and leads to its partial release at AR spermatozoa. It is suggested that liberated PLC-ζ could reach the egg and favour fertilization.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2017 

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References

Aarabi, M., Qin, Z., Xu, W., Mewburn, J. & Oko, R. (2010). Sperm-borne protein, PAWP, initiates zygotic development in Xenopus laevis by eliciting intracellular calcium release. Mol. Reprod. Dev. 77, 249–56.CrossRefGoogle ScholarPubMed
Aarabi, M., Blakier, M., Bashar, S., Moskovtsev, S.I., Sutovsky, P., Librach, C.L. & Oko, R. (2014). Sperm-derived WW domain-binding protein, PAWP, elicits calcium oscillations and oocyte activation in humans and mice. FASEB J. 28, 4434–40.Google Scholar
Azamar, Y., Uribe, S. & Mujica, A. (2007). F-actin involvement in guinea pig sperm motility. Mol. Reprod. Dev. 74, 312– 20.CrossRefGoogle ScholarPubMed
Bernabó, N., Berardinelli, P., Mauro, A., Russo, V., Lucidi, P., Mattioli, M. & Barboni, B. (2011). The role of actin in capacitation-related signaling: an in silico and in vitro study. BMC Systems Biol. 5, 113.CrossRefGoogle ScholarPubMed
Bradford, M.M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248–54.Google Scholar
Breitbart, H., Cohen, G. & Rubinstein, S. (2005). Role of actin cytoskeleton in mammalian sperm capacitation and the acrosome reaction. Reproduction 129, 263–8.Google Scholar
Breitbart, H. & Finkelstein, M. (2015). Regulation of sperm capacitation and the acrosome reaction by PIP2 and actin modulation. Asian J. Androl. 17, 597600.Google Scholar
Brener, E., Rubinstein, S., Cohen, G., Shternall, K., Rivlin, J. & Breitbart, H. (2003). Remodeling of the actin cytoskeleton during mammalian sperm capacitation and acrosome reaction. Biol. Reprod. 68, 837–45.Google Scholar
Chiquete-Felix, N., Hernández, J.M., Mendez, J.A., Zepeda-Bastida, A., Chagolla-López, A. & Mujica, A. (2009). In guinea pig sperm, aldolase A forms a complex with actin, WAS, and Arp2/3 that plays a role in actin polymerization. Reproduction 137, 669–78.Google Scholar
de Lourdes Juárez-Mosqueda, M. & Mujica, A. (1999). A perinuclear theca substructure is formed during epididymal guinea pig sperm maturation and disappears in acrosome reacted cells. J. Struct. Biol. 128, 225–36.Google Scholar
Felipe-Perez, Y.E., Valencia, J., Juárez-Mosqueda, Mde.L., Pescador, N., Roa-Espitia, A.L. & Hernández-Gonzalez, E.O. (2012). Cytoskeletal proteins F-actin and β-dystrobrevin are altered by the cryopreservation process in bull sperm. Cryobiology 64, 103–9.CrossRefGoogle ScholarPubMed
Flaherty, S.P., Winfrey, V.P. & Olso, G.E. (1988). Localization of actin in human, bull, rabbit, and hamster sperm by immunoelectron microscopy. Anat. Rec. 221, 599610.Google Scholar
Fraser, L.R., Abeydeera, L.R. & Niwa, K. (1995). Ca2+-regulating mechanisms that modulate bull sperm capacitation and acrosomal exocytosis as determined by chlortetracycline analysis. Mol. Reprod. Dev. 40, 233–41.CrossRefGoogle Scholar
Fujimoto, S., Yoshida, N., Fukui, T., Amanai, M., Isobe, T., Itagaki, C., Izumi, T. & Perry, A.C. (2004). Mammalian phospholipase Cζ induces oocyte activation from the sperm perinuclear matrix. Dev. Biol. 274, 370–83.Google Scholar
Howes, E.A., Hurst, S.M. & Jones, R. (2001). Actin and actin-binding proteins in bovine spermatozoa: potential role in membrane remodeling and intracellular signaling during epididymal maturation and the acrosome reaction. J. Androl. 22, 6272.Google Scholar
Jagan Mohanarao, G. & Atreja, S.K. (2011). Identification of capacitation associated tyrosine phosphoproteins in buffalo (Bubalus bubalis) and cattle spermatozoa. Anim. Reprod. Sci. 123, 40–7.Google Scholar
Kashir, J., Nomikos, M., Lai, F.A. & Swann, K. (2014). Sperm-induced Ca2+ release during egg activation in mammals. Biochem. Biophys. Res. Commun. 450, 1204–11.CrossRefGoogle ScholarPubMed
Katan, M. & Parker, P.J. (1987). Purification of phosphoinositide-specific phospholipase C from a particulate fraction of bovine brain. Eur. J. Biochem. 168, 413–8.Google Scholar
Kennedy, C.E., Krieger, K.B., Sutovsky, M., Xu, W., Vargovič, P., Didion, B.A., Ellersieck, M.R., Hennessy, M.E., Verstegen, J., Oko, R et al. (2014). Protein expression pattern of PAWP in bull spermatozoa is associated with sperm quality and fertility following artificial insemination. Mol. Reprod. Dev. 81, 436–49.Google Scholar
Kierszenbaum, A.L., Rivkin, E. & Tres, L.L. (2007). Molecular biology of sperm head shaping. Soc. Reprod. Fertil. Suppl. 65, 3343.Google Scholar
Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–5.Google Scholar
Moreno-Fierros, L., Hernández, E.O., Salgado, Z.O. & Mujica, A. (1992). F-actin in guinea pig spermatozoa: its role in calmodulin translocation during acrosome reaction. Mol. Reprod. Dev. 33, 172–81.Google Scholar
Nomikos, M., Blayney, L.M., Larman, M.G., Campbell, K., Rossbach, A., Saunders, C.M., Swann, K. & Lai, F.A. (2005). Role of phospholipase C-ζ domains in Ca2+-dependent phosphatidylinositol 4,5-bisphosphate hydrolysis and cytoplasmic Ca2+ oscillations. J. Biol. Chem. 280, 31011–8.CrossRefGoogle ScholarPubMed
Nomikos, M., Elgmati, K., Theodoridou, M., Calver, B.L., Cumbes, B., Nounesis, G., Swann, K. & Lai, F.A. (2011). Male infertility-linked point mutation disrupts the Ca2+ oscillation-inducing and PIP2 hydrolysis activity of sperm PLCζ. Biochem. J. 434, 211–7.Google Scholar
Oko, R. & Maravei, D. (1994). Protein composition of the perinuclear theca of bull spermatozoa. Biol. Reprod. 50, 1000–14.CrossRefGoogle ScholarPubMed
Pardee, J.D. & Spudich, J.A. (1982). Purification of muscle actin. Methods Enzymol. 85 Pt B, 164–81.Google Scholar
Sato, Y., Kameya, M., Arai, H., Ishii, M. & Igarashi, Y. (2011). Detecting weak protein–protein interactions by modified far-western blotting. J. Biosci. Bioeng. 112, 304–7.CrossRefGoogle ScholarPubMed
Saunders, C.M., Larman, M.G., Parrington, J., Cox, L.J., Royse, J., Blayney, L.M., Swann, K. & Lai, F.A. (2002). PLCζ: a sperm-specific trigger of Ca2+ oscillations in eggs and embryo development. Development 129, 3533–44.Google Scholar
Swann, K., Larman, M.G., Saunders, C.M. & Lai, F.A. (2004). The cytosolic sperm factor that triggers Ca2+ oscillations and egg activation in mammals is a novel phospholipase C: PLCζ. Reproduction 127, 431–9.Google Scholar
Swann, K., Windsor, S., Campbell, K., Elgmati, K., Nomikos, M., Zernicka-Goetz, M., Amso, N., Lai, F.A., Thomas, A. & Graham, C. (2012). Phospholipase Cζ -induced Ca2+ oscillations cause coincident cytoplasmic movements in human oocytes that failed to fertilize after intracytoplasmic sperm injection. Fertil. Steril. 97, 742–7.Google Scholar
Takiguchi, H., Murayama, E., Kaneko, T., Kurio, H., Toshimori, K. & Iida, H. (2011). Characterization and subcellular localization of Tektin 3 in rat spermatozoa. Mol. Reprod. Dev. 78, 611–20.Google Scholar
UniProtKB-Q1RML2 (PLCZ1_BOVIN). (2016). http://www.uniprot.org/uniprot/Q1RML2.Google Scholar
Yeste, M., Jones, C., Amdani, S.N., Patel, S. & Coward, K. (2016). Oocyte activation deficiency: a role for an oocyte contribution? Hum. Reprod. Update 22, 2347.Google Scholar
Yoneda, A., Kashima, M., Yoshida, S., Terada, K., Nakagawa, S., Sakamoto, A., Hayakawa, K., Suzuki, K., Ueda, J. & Watanabe, T. (2006). Molecular cloning, testicular postnatal expression, and oocyte-activating potential of porcine phospholipase Cζ. Reproduction 132, 393401.Google Scholar
Yoon, S.Y., Jellerette, T., Salicioni, A.M., Lee, H.C., Yoo, M.S., Coward, K., Parrington, J., Grow, D., Cibelli, J.B., Visconti, P.E., Mager, J. & Fissore, R.A. (2008). Human sperm devoid of PLCζ 1 fail to induce Ca2+ release and are unable to initiate the first step of embryo development. J. Clin. Invest. 118, 3671–81.CrossRefGoogle Scholar
Young, C., Grasa, P., Coward, K., Davis, L.C. & Parrington, J. (2009). Phospholipase Cζ undergoes dynamic changes in its pattern of localization in sperm during capacitation and the acrosome reaction. Fertil. Steril. 91, 2230–42.CrossRefGoogle Scholar