Content and activity of the testis-specific isoform of angiotensin-converting enzyme are reduced in frozen–thawed bull spermatozoa
Mina Ojaghi A , Chinju Johnson A , Guilherme Rizzoto A , John Kastelic A and Jacob C. Thundathil A B
+ Author Affiliations
- Author Affiliations
A Faculty of Veterinary Medicine, Department of Production Animal Health, University of Calgary, TRW 2D13, 3280 Hospital Dr, NW T2N 4Z6, Canada.
B Corresponding author. Email: jthundat@ucalgary.ca
Reproduction, Fertility and Development 30(11) 1575-1583 https://doi.org/10.1071/RD17219
Submitted: 14 June 2017 Accepted: 27 April 2018 Published: 14 June 2018
Abstract
Sperm cryopreservation and thawing reduces fertility and alters the content and function of various sperm proteins. Previously, we reported that a testes-specific isoform of angiotensin-converting enzyme (tACE) was required for capacitation of bovine spermatozoa. The aim of the present study was to determine effects of sperm cryopreservation and thawing on the content, activity and localisation of tACE in bovine spermatozoa. Relative median fluorescence intensity (flow cytometry) was greater (P < 0.01), tACE content (110 kDa protein) in sperm proteins was higher (P < 0.01) and there was greater tACE enzyme activity (mean (±s.e.m.) 0.16 ± 0.01 vs 0.06 ± 0.02 U mL−1; P < 0.01) in fresh versus frozen–thawed spermatozoa (n = 6 bulls). In fresh spermatozoa, tACE was immunolocalised in the acrosomal and principal piece regions of the sperm head and tail respectively. However, in frozen–thawed spermatozoa, there were four patterns of localisation: most frozen–thawed spermatozoa (64%) had fluorescence in the acrosomal ridge, whereas in 17% and 9% of spermatozoa the signal was limited to the post-acrosomal region and the equatorial segment respectively; in the remainder (10%), there was no signal. We conclude that cryopreservation and thawing decrease the content and activity of tACE and cause it to be translocated to other parts of the sperm head.
Additional keywords: cryopreservation, fertility, protein.
References
Auger, J., and Dadoune, J. P. (1988). Computerized sperm motility and application of sperm cryopreservation. Arch. Androl. 20, 103–112.| Computerized sperm motility and application of sperm cryopreservation.Crossref | GoogleScholarGoogle Scholar |
Bailey, J. L., Bilodeau, J. F., and Cormier, N. (2000). Semen cryopreservation in domestic animals: a damaging and capacitating phenomenon. J. Androl. 21, 1–7.
Ball, B. A., Gravance, C. G., Wessel, M. T., and Sabeur, K. (2003). Activity of angiotensin-converting enzyme (ACE) in reproductive tissues of the stallion and effects of angiotensin II on sperm motility. Theriogenology 59, 901–914.
Blok, M. C., van der Neut-Kok, E. C., van Deenen, L. L., and de Gier, J. (1975). The effect of chain length and lipid phase transitions on the selective permeability properties of liposomes. Biochim. Biophys. Acta 406, 187–196.
| The effect of chain length and lipid phase transitions on the selective permeability properties of liposomes.Crossref | GoogleScholarGoogle Scholar |
Bredderman, P. J., and Foote, R. H. (1969). Volume of stressed bull spermatozoa and protoplasmic droplets, and the relationship of cell size to motility and fertility. J. Anim. Sci. 28, 496–501.
| Volume of stressed bull spermatozoa and protoplasmic droplets, and the relationship of cell size to motility and fertility.Crossref | GoogleScholarGoogle Scholar |
Chapman, D., Peel, W. E., Kingston, B., and Lilley, T. H. (1977). Lipid phase transitions in model biomembranes: the effect of ions on phosphatidylcholine bilayers. Biochim. Biophys. Acta 464, 260–275.
| Lipid phase transitions in model biomembranes: the effect of ions on phosphatidylcholine bilayers.Crossref | GoogleScholarGoogle Scholar |
Cormier, N., and Bailey, J. L. (2003). A differential mechanism is involved during heparin-and cryopreservation-induced capacitation of bovine spermatozoa. Biol. Reprod. 69, 177–185.
| A differential mechanism is involved during heparin-and cryopreservation-induced capacitation of bovine spermatozoa.Crossref | GoogleScholarGoogle Scholar |
De Leeuw, F. E., Chen, H.-C., Colenbrander, B., and Verkleij, A. J. (1990). Cold-induced ultrastructural changes in bull and boar sperm plasma membranes. Cryobiology 27, 171–183.
| Cold-induced ultrastructural changes in bull and boar sperm plasma membranes.Crossref | GoogleScholarGoogle Scholar |
De Leeuw, F. E., De Leeuw, A. M., Den Daas, J. H. G., Colenbrander, B., and Verkleij, A. J. (1993). Effects of various cryoprotective agents and membrane-stabilizing compounds on bull sperm membrane integrity after cooling and freezing. Cryobiology 30, 32–44.
| Effects of various cryoprotective agents and membrane-stabilizing compounds on bull sperm membrane integrity after cooling and freezing.Crossref | GoogleScholarGoogle Scholar |
Drevius, L.-O. (1972). Bull spermatozoa as osmometers. J. Reprod. Fertil. 28, 29–39.
| Bull spermatozoa as osmometers.Crossref | GoogleScholarGoogle Scholar |
Dubé, C., Leclerc, P., Baba, T., Reyes-Moreno, C., and Bailey, J. L. (2005). The proacrosin binding protein, sp32, is tyrosine phosphorylated during capacitation of pig sperm. J. Androl. 26, 519–528.
| The proacrosin binding protein, sp32, is tyrosine phosphorylated during capacitation of pig sperm.Crossref | GoogleScholarGoogle Scholar |
Esfahani, M., Limbrick, A. R., Knutton, S., Oka, T., and Wakil, S. J. (1971). The molecular organization of lipid in the membrane of Escherchia coli: phase transitions. Proc. Natl Acad. Sci. USA 68, 3180–3184.
| The molecular organization of lipid in the membrane of Escherchia coli: phase transitions.Crossref | GoogleScholarGoogle Scholar |
Esther, C. R., Howard, T. E., Marino, E. M., Goddard, J. M., Capecchi, M. R., and Bernstein, K. E. (1996). Mice lacking angiotensin-converting enzyme have low blood pressure, renal pathology, and reduced male fertility. Lab. Invest. 74, 953–965.
Eze, M. O. (1991). Phase transitions in phospholipid bilayer: lateral phase separations play vital roles in biomembranes. Biochem. Educ. 19, 204–208.
| Phase transitions in phospholipid bilayer: lateral phase separations play vital roles in biomembranes.Crossref | GoogleScholarGoogle Scholar |
Foresta, C., Indino, M., Manoni, F., and Scandellari, C. (1987). Angiotensin-converting enzyme content of human spermatozoa and its release during capacitation. Fertil. Steril. 47, 1000–1003.
| Angiotensin-converting enzyme content of human spermatozoa and its release during capacitation.Crossref | GoogleScholarGoogle Scholar |
Foresta, C., Mioni, R., Rossato, M., and Varotto, A. (1991). Evidence for the involvement of sperm angiotensin converting enzyme in fertilization. Int. J. Androl. 14, 333–339.
| Evidence for the involvement of sperm angiotensin converting enzyme in fertilization.Crossref | GoogleScholarGoogle Scholar |
Fuchs, S., Frenzel, K., Hubert, C., Lyng, R., Muller, L., Michaud, A., Xiao, H., Adams, J., Capecchi, M., Corvol, P., Shur, B., and Bernstein, K. (2005). Male fertility is dependent on dipeptidase activity of testes ACE. Nat. Med. 11, 1140–1142.
| Male fertility is dependent on dipeptidase activity of testes ACE.Crossref | GoogleScholarGoogle Scholar |
Galantino-Homer, H. L., Visconti, P. E., and Kopf, G. S. (1997). Regulation of protein tyrosine phosphorylation during bovine sperm capacitation by a cyclic adenosine 3′5′-monophosphate-dependent pathway. Biol. Reprod. 56, 707–719.
| Regulation of protein tyrosine phosphorylation during bovine sperm capacitation by a cyclic adenosine 3′5′-monophosphate-dependent pathway.Crossref | GoogleScholarGoogle Scholar |
Gao, D. Y., Liu, J., Liu, C., McGann, L. E., Watson, P. F., Kleinhans, F. W., Mazur, P., Critser, E. S., and Critser, J. K. (1995). Andrology: prevention of osmotic injury to human spermatozoa during addition and removal of glycerol. Hum. Reprod. 10, 1109–1122.
| Andrology: prevention of osmotic injury to human spermatozoa during addition and removal of glycerol.Crossref | GoogleScholarGoogle Scholar |
Grasa, P., Colas, C., Gallego, M., Monteagudo, L., Muiño-Blanco, T., and Cebrián-Pérez, J. Á. (2009). Changes in content and localization of proteins phosphorylated at tyrosine, serine and threonine residues during ram sperm capacitation and acrosome reaction. Reproduction 137, 655–667.
| Changes in content and localization of proteins phosphorylated at tyrosine, serine and threonine residues during ram sperm capacitation and acrosome reaction.Crossref | GoogleScholarGoogle Scholar |
Gravance, C. G., Vishwanath, R., Pitt, C., Garner, D. L., and Casey, P. J. (1998). Effects of cryopreservation on bull sperm head morphometry. J. Androl. 19, 704–709.
Haest, C. W. M., De Gier, J., Van Es, G. A., Verkleij, A. J., and Van Deenen, L. L. M. (1972). Fragility of the permeability barrier of Escherichia coli. Biochim. Biophys. Acta 288, 43–53.
| Fragility of the permeability barrier of Escherichia coli.Crossref | GoogleScholarGoogle Scholar |
Hagaman, J. R., Moyer, J. S., Bachman, E. S., Sibony, M., Magyar, P. L., Welch, J. E., Smithies, O., Krege, J. H., and O’Brien, D. A. (1998). Angiotensin-converting enzyme and male fertility. Proc. Natl Acad. Sci. USA 95, 2552–2557.
| Angiotensin-converting enzyme and male fertility.Crossref | GoogleScholarGoogle Scholar |
Hamada, T., Kishimoto, Y., Nagasaki, T., and Takagi, M. (2011). Lateral phase separation in tense membranes Soft Matter 7, 9061–9068.
| Lateral phase separation in tense membranesCrossref | GoogleScholarGoogle Scholar |
Hammerstedt, R. H., Graham, J. K., and Nolan, J. P. (1990). Cryopreservation of mammalian sperm: what we ask them to survive. J. Androl. 11, 73–88.
Hazel, J. R. (1995). Thermal adaptation in biological-membranes – is homeoviscous adaptation the explanation. Annu. Rev. Physiol. 57, 19–42.
| Thermal adaptation in biological-membranes – is homeoviscous adaptation the explanation.Crossref | GoogleScholarGoogle Scholar |
Hinkovska-Galcheva, V., Petkova, D., and Koumanov, K. (1989). Changes in the phospholipid composition and phospholipid asymmetry of ram sperm plasma membranes after cryopreservation. Cryobiology 26, 70–75.
| Changes in the phospholipid composition and phospholipid asymmetry of ram sperm plasma membranes after cryopreservation.Crossref | GoogleScholarGoogle Scholar |
Holmquist, B., Bünning, P., and Riordan, J. F. (1979). A continuous spectrophotometric assay for angiotensin converting enzyme. Anal. Biochem. 95, 540–548.
Holt, W. V., and North, R. D. (1986). Thermotropic phase transitions in the plasma membrane of ram spermatozoa. J. Reprod. Fertil. 78, 447–457.
| Thermotropic phase transitions in the plasma membrane of ram spermatozoa.Crossref | GoogleScholarGoogle Scholar |
Hooper, N. M., and Turner, A. J. (2003). An ACE structure. Nat. Struct. Mol. Biol. 10, 155–157.
| An ACE structure.Crossref | GoogleScholarGoogle Scholar |
Inesi, G., Millman, M., and Eleter, S. (1973). Temperature-induced transitions of function and structure in sarcoplasmic reticulum membranes. J. Mol. Biol. 81, 483–504.
| Temperature-induced transitions of function and structure in sarcoplasmic reticulum membranes.Crossref | GoogleScholarGoogle Scholar |
Kamaruddin, M., Kroetsch, T., Basrur, P. K., Hansen, P. J., and King, W. A. (2004). Immunolocalization of heat shock protein 70 in bovine spermatozoa. 36, 327–334.
Karunakaran, M., and Devanathan, T. G. (2017). Evaluation of bull semen for fertility-associated protein, in vitro characters and fertility. J. Appl. Anim. Res. 45, 136–144.
| Evaluation of bull semen for fertility-associated protein, in vitro characters and fertility.Crossref | GoogleScholarGoogle Scholar |
Kimelberg, H. K. (1975). Alternation in phospholipid-dependent (Na-K)-ATPase activity due to lipid fluidity. Biochim. Biophys. Acta 413, 143–156.
| Alternation in phospholipid-dependent (Na-K)-ATPase activity due to lipid fluidity.Crossref | GoogleScholarGoogle Scholar |
Kimelberg, H. K., and Mayhew, E. (1975). Increased ouabain-sensitive 86Rb+ uptake and sodium and potassium ion-activated adenosine triphosphatase activity in transformed cell lines. J. Biol. Chem. 250, 100–104.
Kimelberg, H. K., and Papahadjopoulos, D. (1974). Effects of phospholipid acyl chain fluidity, phase transitions, and cholesterol on (Na+ + K+)-stimulated adenosine triphosphatase. J. Biol. Chem. 249, 1071–1080.
Kohn, F. M., Miska, W., and Schill, W. B. (1995). Release of angiotensin-converting enzyme (ACE) from human spermatozoa during capacitation and acrosome reaction. J. Androl. 16, 259–265.
Kondoh, G., Tojo, H., Nakatani, Y., Komazawa, N., Murata, C., Yamagata, K., Maeda, Y., Kinoshita, T., Okabe, M., Taguchi, R., and Takeda, J. (2005). Angiotensin-converting enzyme is a GPI-anchored protein releasing factor crucial for fertilization. Nat. Med. 11, 160–166.
| Angiotensin-converting enzyme is a GPI-anchored protein releasing factor crucial for fertilization.Crossref | GoogleScholarGoogle Scholar |
Krege, J. H., John, S. W., Langenbach, L. L., Hodgin, J. B., Hagaman, J. R., Bachman, E. S., Jennette, J. C., O’Brien, D. A., and Smithies, O. (1995). Male-female differences in fertility and blood pressure in ACE-deficient mice. Nature 375, 146–148.
| Male-female differences in fertility and blood pressure in ACE-deficient mice.Crossref | GoogleScholarGoogle Scholar |
Lasso, J. L., Noiles, E. E., Alvarez, J. G., and Storey, B. T. (1994). Mechanism of superoxide dismutase loss from human sperm cells during cryopreservation J. Androl. 15, 255–265.
Lessard, C., Parent, S., Leclerc, P., Baileys, J. L., and Sullivan, R. (2000). Cryopreservation alters the levels of the bull sperm surface protein P25b. J. Androl. 21, 700–707.
McGann, L. E., Yang, H., and Walterson, M. (1988). Manifestations of cell damage after freezing and thawing. Cryobiology 25, 178–185.
| Manifestations of cell damage after freezing and thawing.Crossref | GoogleScholarGoogle Scholar |
Momchilova, A. B., Petkova, D. H., and Koumanov, K. S. (1986). Phospholipid composition modifications influence phospholipase A2 activity in rat liver plasma membranes. Int. J. Biochem. 18, 945–952.
| Phospholipid composition modifications influence phospholipase A2 activity in rat liver plasma membranes.Crossref | GoogleScholarGoogle Scholar |
Naz, R. K., Ahmad, K., and Kumar, R. (1991). Role of membrane phosphotyrosine proteins in human spermatozoal function. J. Cell Sci. 99, 157–165.
Newton, L. D., Krishnakumar, S., Menon, A. G., Kastelic, J. P., Van Der Hoorn, F. A., and Thundathil, J. C. (2010). Na+/K+ATPase regulates sperm capacitation through a mechanism involving kinases and redistribution of its testis-specific isoform. Mol. Reprod. Dev. 77, 136–148.
Nicholls, P., and Miller, N. (1974). Chloride diffusion from liposomes. Biochim Biophys. Acta 356, 184–198.
| Chloride diffusion from liposomes.Crossref | GoogleScholarGoogle Scholar |
Ojaghi, M., Kastelic, J., and Thundathil, J. (2017). Testis-specific isoform of angiotensin-converting enzyme (tACE) is involved in the regulation of bovine sperm capacitation. Mol. Reprod. Dev. 84, 376–388.
Ollero, M., Cebrian-Perez, J. A., and Muino-Blanco, T. (1997). Improvement of cryopreserved ram sperm heterogeneity and viability by addition of seminal plasma. J. Androl. 18, 732–739.
Quinn, P. J. (1981). The fluidity of cell membranes and its regulation. Prog. Biophys. Mol. Biol. 38, 1–104.
| The fluidity of cell membranes and its regulation.Crossref | GoogleScholarGoogle Scholar |
Rajamanickam, G. D., Kastelic, J., and Thundathil, J. (2017). Content of testis-specific isoform of Na/K-ATPase (ATP1A4) is increased during bovine sperm capacitation through translation in mitochondrial ribosomes. Cell Tissue Res. 368, 187–200.
Royere, D., Hamamah, S., Nicolle, J. C., and Lansac, J. (1991). Chromatin alterations induced by freeze–thawing influence the fertilizing ability of human sperm. Int. J. Androl. 14, 328–332.
| Chromatin alterations induced by freeze–thawing influence the fertilizing ability of human sperm.Crossref | GoogleScholarGoogle Scholar |
Sancho, S., Casas, I., Ekwall, H., Saravia, F., Rodriguez-Martinez, H., Rodriguez-Gil, J. E., Flores, E., Pinart, E., Briz, M., Garcia-Gil, N., Bassols, J., Pruneda, A., Bussalleu, E., Yeste, M., and Bonet, S. (2007). Effects of cryopreservation on semen quality and the expression of sperm membrane hexose transporters in the spermatozoa of Iberian pigs. Reproduction 134, 111–121.
| Effects of cryopreservation on semen quality and the expression of sperm membrane hexose transporters in the spermatozoa of Iberian pigs.Crossref | GoogleScholarGoogle Scholar |
Tardif, S., Dubé, C., Chevalier, S., and Bailey, J. L. (2001). Capacitation is associated with tyrosine phosphorylation and tyrosine kinase-like activity of pig sperm proteins. Biol. Reprod. 65, 784–792.
| Capacitation is associated with tyrosine phosphorylation and tyrosine kinase-like activity of pig sperm proteins.Crossref | GoogleScholarGoogle Scholar |
Thundathil, J., Gil, J., Januskauskas, A., Larsson, B., Soderquist, L., Mapletoft, R., and Rodriguez-Martinez, H. (1999). Relationship between the proportion of capacitated spermatozoa present in frozen–thawed bull semen and fertility with artificial insemination. Int. J. Androl. 22, 366–373.
| Relationship between the proportion of capacitated spermatozoa present in frozen–thawed bull semen and fertility with artificial insemination.Crossref | GoogleScholarGoogle Scholar |
Tocanne, J.-F., Dupou-Cézanne, L., Lopez, A., and Tournier, J.-F. (1989). Lipid lateral diffusion and membrane organization. FEBS Lett. 257, 10–16.
| Lipid lateral diffusion and membrane organization.Crossref | GoogleScholarGoogle Scholar |
van Wagtendonk-de Leeuw, A. M., Haring, R. M., Kaal-Lansbergen, L. M. T. E., and Den Daas, J. H. G. (2000). Fertility results using bovine semen cryopreserved with extenders based on egg yolk and soy bean extract. Theriogenology 54, 57–67.
| Fertility results using bovine semen cryopreserved with extenders based on egg yolk and soy bean extract.Crossref | GoogleScholarGoogle Scholar |
Watson, P. F. (1995). Recent developments and concepts in the cryopreservation of spermatozoa and the assessment of their post-thawing function. Reprod. Fertil. Dev. 7, 871–891.
| Recent developments and concepts in the cryopreservation of spermatozoa and the assessment of their post-thawing function.Crossref | GoogleScholarGoogle Scholar |
