Oligomycin A-induced inhibition of mitochondrial ATP-synthase activity suppresses boar sperm motility and in vitro capacitation achievement without modifying overall sperm energy levels
Laura Ramió-Lluch A , Marc Yeste A , Josep M. Fernández-Novell B , Efrén Estrada A , Luiz Rocha A , José A. Cebrián-Pérez C , Teresa Muiño-Blanco C , Ilona I. Concha D , Alfredo Ramírez D and Joan E. Rodríguez-Gil A E
+ Author Affiliations
- Author Affiliations
A Department of Animal Medicine and Surgery, School of Veterinary Medicine, Autonomous University of Barcelona, E-08193 Bellaterra, Barcelona, Spain.
B Department of Biochemistry and Molecular Biology, University of Barcelona, E-08028 Barcelona, Spain.
C Department of Biochemistry and Molecular and Cell Biology, I. U. C. A., School of Veterinary Medicine, University of Zaragoza, E-50013 Zaragoza, Spain.
D Institute of Biochemistry and Microbiology and Institute of Animal Science, Universidad Austral de Chile, Independencia 641, Valdivia, Chile.
E Corresponding author. Email: juanenrique.rodriguez@uab.cat
Reproduction, Fertility and Development 26(6) 883-897 https://doi.org/10.1071/RD13145
Submitted: 27 February 2013 Accepted: 8 June 2013 Published: 16 July 2013
Abstract
Incubation of boar spermatozoa in a capacitation medium with oligomycin A, a specific inhibitor of the F0 component of the mitochondrial ATP synthase, induced an immediate and almost complete immobilisation of cells. Oligomycin A also inhibited the ability of spermatozoa to achieve feasible in vitro capacitation (IVC), as measured through IVC-compatible changes in motility patterns, tyrosine phosphorylation levels of the acrosomal p32 protein, membrane fluidity and the ability of spermatozoa to achieve subsequent, progesterone-induced in vitro acrosome exocytosis (IVAE). Both inhibitory effects were caused without changes in the rhythm of O2 consumption, intracellular ATP levels or mitochondrial membrane potential (MMP). IVAE was accompanied by a fast and intense peak in O2 consumption and ATP levels in control spermatozoa. Oligomycin A also inhibited progesterone-induced IVAE as well as the concomitant peaks of O2 consumption and ATP levels. The effect of oligomycin on IVAE was also accompanied by concomitant alterations in the IVAE-induced changes on intracellular Ca2+ levels and MMP. Our results suggest that the oligomycin A-sensitive mitochondrial ATP-synthase activity is instrumental in the achievement of an adequate boar sperm motion pattern, IVC and IVAE. However, this effect seems not to be linked to changes in the overall maintenance of adequate energy levels in stages other than IVAE.
Additional keywords: acrosome exocytosis, ATP, chemiosmosis, O2 consumption.
References
Aitken, R. J., Gibb, Z., Mitchell, L. A., Lambourne, S. R., Connaughton, H. S., and De Iuliis, G. N. (2012). Sperm motility is lost in vitro as a consequence of mitochondrial free-radical production and the generation of electrophylic aldehydes but can be significantly rescued by the presence of nucleophylic thiols. Biol. Reprod. 87, 110.| Sperm motility is lost in vitro as a consequence of mitochondrial free-radical production and the generation of electrophylic aldehydes but can be significantly rescued by the presence of nucleophylic thiols.Crossref | GoogleScholarGoogle Scholar | 22933515PubMed |
Alberts, B., Bray, D., Lewis, J., Raff, M., Roberts, K., and Watson, J. D. (1983). Membrane transport of small molecules. In: ‘Molecular Biology of the Cell’. (Eds B. Alberts, D. Bray, J. Lewis, M. Raff, K. Roberts and J. D. Watson) pp. 286–302. (Garland Publishing Inc.: New York, USA)
Arato-Oshima, T., Matsui, H., Wakizaka, A., and Homareda, H. (1996). Mechanism responsible for oligomycin-induced occlusion of Na+ within Na/K-ATPase. J. Biol. Chem. 271, 25 604–25 610.
| Mechanism responsible for oligomycin-induced occlusion of Na+ within Na/K-ATPase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xmt1eltrw%3D&md5=094d7e0157e66afcec5c2934dc010904CAS |
Austin, C. R. (1951). Observations on the penetration of the sperm into the mammalian egg. Aust. J. Sci. Res. B. 4, 581–596.
| 1:STN:280:DyaG38%2FisFGqsw%3D%3D&md5=d1e1d04000b1582dde6b472a2bf69bf4CAS | 14895481PubMed |
Austin, C. R. (1952). The capacitation of the mammalian sperm. Nature 170, 326.
| The capacitation of the mammalian sperm.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaG3s%2FhslChsw%3D%3D&md5=bb5d22d22895618819078be232d3ed8aCAS | 12993150PubMed |
Bannur, S. V., Kulgod, S. V., Metkar, S. S., Mahajan, S. K., and Sainis, J. K. (1999). Protein determination by Ponceau S using digital colour image analysis of protein spots on nitrocellulose membranes. Anal. Biochem. 267, 382–389.
| Protein determination by Ponceau S using digital colour image analysis of protein spots on nitrocellulose membranes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXht1Oru7g%3D&md5=09ad1c26c832e1ccbb060147f0fd3b48CAS | 10036145PubMed |
Belles-Isles, M., Chapeau, C., White, D., and Gagnon, C. (1986). Isolation and characterization of dynein ATPase from bull spermatozoa. Biochem. J. 240, 863–869.
| 1:CAS:528:DyaL28Xmt1Wnurg%3D&md5=6ca2f103bb2df85a4eb8a09ef61c6d72CAS | 2950853PubMed |
Bhattacharyya, A., and Pakrashi, A. (1993). Specificity of ATP for the initiation of flagellar motility of hamster sperm. Arch. Androl. 31, 159–165.
| Specificity of ATP for the initiation of flagellar motility of hamster sperm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXhsF2qtLo%3D&md5=48bfcebe0be183497e327a276fc70a6cCAS | 8274042PubMed |
Blackmore, P. F., Beebe, S. J., Danforth, D. R., and Alexander, N. (1990). Progesterone and 17 +alpha-hydroxyprogesterone. Novel stimulators of calcium influx in human sperm. J. Biol. Chem. 265, 1376–1380.
| 1:CAS:528:DyaK3cXpt1SitA%3D%3D&md5=1e426d8d072e54ac9011d54c1a08e5c2CAS | 2104840PubMed |
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, 248–254.
| A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XksVehtrY%3D&md5=2bd99067c12b7e4a32c7d228e1466eabCAS | 942051PubMed |
Brown, G. C. (1992). Control of respiration and ATP synthesis in mammalian mitochondria and cells. Biochem. J. 284, 1–13.
| 1:CAS:528:DyaK38XisFaks7c%3D&md5=27b7d11649f9eeb84d561a798f138fb9CAS | 1599389PubMed |
Burnette, W. N. (1981). “Western blotting”: electrophoretic transfer of proteins from sodium dodecyl sulfate-polyacrylamide gels to unmodified nitrocellulose and radiographic detection with antibody and radioiodinated protein A. Anal. Biochem. 112, 195–203.
| “Western blotting”: electrophoretic transfer of proteins from sodium dodecyl sulfate-polyacrylamide gels to unmodified nitrocellulose and radiographic detection with antibody and radioiodinated protein A.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXhvVOqtbs%3D&md5=02732218b34b3b7a663962b66ade1290CAS | 6266278PubMed |
Bussalleu, E., Pinart, E., Yeste, M., Briz, M., Sancho, S., Garcia-Gil, N., Badia, E., Bassols, J., Pruneda, A., Casas, I., and Bonet, S. (2005). Development of a protocol for multiple staining with fluorochromes to assess the functional status of boar spermatozoa. Microsc. Res. Tech. 68, 277–283.
| Development of a protocol for multiple staining with fluorochromes to assess the functional status of boar spermatozoa.Crossref | GoogleScholarGoogle Scholar | 16315232PubMed |
Caiza de la Cueva, F. I., Pujol, M. R., Rigau, T., Bonet, S., Miró, J., Briz, M., and Rodríguez-Gil, J. E. (1997). Resistance to osmotic stress of horse spermatozoa: the role of ionic pumps and their relationship to cryopreservation success. Theriogenology 48, 947–968.
| Resistance to osmotic stress of horse spermatozoa: the role of ionic pumps and their relationship to cryopreservation success.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28zgtV2gtA%3D%3D&md5=9cdfc761ec1725682d50f9b521476616CAS | 16728185PubMed |
Chance, B., and Williams, G. R. (1955). Respiratory enzymes in oxidative phosphorylation: I. kinetics of oxygen utilization. J. Biol. Chem. 217, 383–393.
| 1:CAS:528:DyaG28XitVGhsA%3D%3D&md5=7ec392b3400844c39dfb3603d59968ceCAS | 13271402PubMed |
Chang, M. C. (1951). Fertilizing capacity of spermatozoa deposited into fallopian tubes. Nature 168, 697–698.
| Fertilizing capacity of spermatozoa deposited into fallopian tubes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaG38%2Fht1Cgtw%3D%3D&md5=5a08cf7b86081b289170289afb38ae40CAS | 14882325PubMed |
Chang, M. C. (1984). The meaning of sperm capacitation. A historical perspective. J. Androl. 5, 45–50.
| 1:STN:280:DyaL2c7osFejtw%3D%3D&md5=b35fbbfa55a023e16724c92cadc4b11eCAS | 6370941PubMed |
Chappell, J. B., and Greville, G. D. (1961). Effects of atractylate and oligomycin A on respiration and swelling of isolated liver mitochondria. Nature 190, 502–504.
| Effects of atractylate and oligomycin A on respiration and swelling of isolated liver mitochondria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF3MXhtFans74%3D&md5=ede6a38e0d3e3e706a1c5a55979d47e4CAS | 13692427PubMed |
de Lamirande, E., Jiang, H., Zini, A., Kodama, H., and Gagnon, C. (1997). Reactive oxygen species and sperm physiology. Rev. Reprod. 2, 48–54.
| Reactive oxygen species and sperm physiology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhs1Kmsrk%3D&md5=03a7fe50ebecbc409e168971f7bdbfeeCAS | 9414465PubMed |
Donà, G., Fiore, C., Tibaldi, E., Frezzato, F., Andrisani, A., Ambrosini, G., Fiorentin, D., Armanini, D., Bordin, L., and Clari, G. (2011). Endogenous reactive oxygen species content and modulation of tyrosine phosphorylation during sperm capacitation. Int. J. Androl. 34, 411–419.
| Endogenous reactive oxygen species content and modulation of tyrosine phosphorylation during sperm capacitation.Crossref | GoogleScholarGoogle Scholar | 20738429PubMed |
Eisenbach, M., and Giojalas, L. C. (2006). Sperm guidance in mammals: an unpaved road to the egg. Nat. Rev. Mol. Cell Biol. 7, 276–285.
| Sperm guidance in mammals: an unpaved road to the egg.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xjt12qsLY%3D&md5=66b571e8fb235ddbc26bee66f8664ca2CAS | 16607290PubMed |
Espinoza, J. A., Schulz, M. A., Sánchez, R., and Villegas, J. V. (2009). Integrity of mitochondrial membrane potential reflects human sperm quality. Andrologia 41, 51–54.
| Integrity of mitochondrial membrane potential reflects human sperm quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXivVGrs7c%3D&md5=a1930f613d9615248300ff086dcbaa4cCAS | 19143731PubMed |
Ford, W. C. (2006). Glycolysis and sperm motility: does a spoonful of sugar help the flagellum go round? Hum. Reprod. Update 12, 269–274.
| Glycolysis and sperm motility: does a spoonful of sugar help the flagellum go round?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xjtlanurg%3D&md5=425327a975649ac8b34b63eaeaa02b07CAS | 16407453PubMed |
Ford, W. C., and Harrison, A. (1981). The role of oxidative phosphorylation in the generation of ATP in human spermatozoa. J. Reprod. Fertil. 63, 271–278.
| The role of oxidative phosphorylation in the generation of ATP in human spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXlsVOrs70%3D&md5=43a72f9a719c506944b57c6ddabe3b95CAS | 7277330PubMed |
Ford, W. C., and Harrison, A. (1985). The presence of glucose increases the lethal effect of alpha-chlorohydrin on ram and boar spermatozoa in vitro. J. Reprod. Fertil. 73, 197–206.
| The presence of glucose increases the lethal effect of alpha-chlorohydrin on ram and boar spermatozoa in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXht1Gkt74%3D&md5=f3dfc69d8f386ebbb7ce7a0e9ae72a24CAS | 3968653PubMed |
García, M. A., and Meizel, S. (1999). Progesterone-mediated calcium influx and acrosome reaction of human spermatozoa: pharmacological investigation of T-type calcium channels. Biol. Reprod. 60, 102–109.
| Progesterone-mediated calcium influx and acrosome reaction of human spermatozoa: pharmacological investigation of T-type calcium channels.Crossref | GoogleScholarGoogle Scholar | 9858492PubMed |
Garcıa Herreros, M., Aparicio, I. M., Núñez, I., García-Marín, L. J., Gil, M. C., and Peña Vega, F. J. (2005). Boar sperm velocity and motility patterns under capacitating and non-capacitating incubation conditions. Theriogenology 63, 795–805.
| Boar sperm velocity and motility patterns under capacitating and non-capacitating incubation conditions.Crossref | GoogleScholarGoogle Scholar | 15629798PubMed |
Garner, D. L., and Johnson, L. A. (1995). Viability assessment of mammalian sperm using SYBR-14 and propidium iodide. Biol. Reprod. 53, 276–284.
| Viability assessment of mammalian sperm using SYBR-14 and propidium iodide.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXntVSmtbc%3D&md5=af36deeacac0bdb0d10f544ea4c0b039CAS | 7492679PubMed |
Garner, D. L., and Thomas, C. A. (1999). Organelle-specific probe JC-1 identifies membrane potential differences in the mitochondrial function of bovine sperm. Mol. Reprod. Dev. 53, 222–229.
| Organelle-specific probe JC-1 identifies membrane potential differences in the mitochondrial function of bovine sperm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXivFKmtLo%3D&md5=6b925f72b10928346569a9fec60d312eCAS | 10331460PubMed |
Garrahan, P. J., and Glynn, I. M. (1967). Factors affecting the relative magnitudes of the sodium:potassium and sodium:sodium exchanges catalysed by the sodium pump. J. Physiol. 192, 189–216.
| 1:CAS:528:DyaF2sXkvFygtLw%3D&md5=bd0dca81398066c3123ddee4ceb5781eCAS | 6051803PubMed |
Gravance, C. G., Garner, D. L., Baumber, J., and Ball, B. A. (2000a). Assessment of equine sperm mitochondrial function using JC-1. Theriogenology 53, 1691–1703.
| Assessment of equine sperm mitochondrial function using JC-1.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3cvpsFensg%3D%3D&md5=c19394b3c1446a4a16b5912a98ddc263CAS | 10968415PubMed |
Gravance, C. G., Garner, D. L., Miller, M. G., and Berger, T. (2000b). Fluorescent probes and flow cytometry to assess rat sperm integrity and mitochondrial function. Reprod. Toxicol. 15, 5–10.
| Fluorescent probes and flow cytometry to assess rat sperm integrity and mitochondrial function.Crossref | GoogleScholarGoogle Scholar |
Grüber, G., Godovac-Zimmermann, J., and Nawroth, T. (1994). ATP synthesis and hydrolysis of the ATP synthase from Microccocus luteus regulated by an inhibitor subunit and membrane energisation. Biochem. Biophys. Acta – Bioenergetics 1186, 43–51.
| ATP synthesis and hydrolysis of the ATP synthase from Microccocus luteus regulated by an inhibitor subunit and membrane energisation.Crossref | GoogleScholarGoogle Scholar |
Guthrie, H. D., Welch, G. R., and Long, J. A. (2008). Mitochondrial function and reactive oxygen species action in relation to boar motility. Theriogenology 70, 1209–1215.
| Mitochondrial function and reactive oxygen species action in relation to boar motility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlKqsL7I&md5=d3d4aff2c3d172783a1a623a9917546cCAS | 18667230PubMed |
Harrison, R. A. P., Ashworth, P. J., and Miller, N. G. A. (1996). Bicarbonate/CO2, an effector of capacitation, induces a rapid and reversible change in the lipid architecture of boar sperm plasma membranes. Mol. Reprod. Dev. 45, 378–391.
| Bicarbonate/CO2, an effector of capacitation, induces a rapid and reversible change in the lipid architecture of boar sperm plasma membranes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XmslWlu7g%3D&md5=5592c0847734da5a17d761ef15699f2aCAS |
Idziorek, T., Estaquier, J., De Bels, F., and Ameisen, J. C. (1995). YOPRO-1 permits cytofluorometric analysis of programmed cell death (apoptosis) without interfering with cell viability. J. Immunol. Methods 185, 249–258.
| YOPRO-1 permits cytofluorometric analysis of programmed cell death (apoptosis) without interfering with cell viability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXotFCkt7Y%3D&md5=47ff5bfe6da941b580495e52e7f29810CAS | 7561136PubMed |
Jiménez, I., Gónzalez-Márquez, H., Ortiz, R., Herrera, J. A., García, A., Betancourt, M., and Fierro, R. (2003). Changes in the distribution of lectin receptors during capacitation and acrosome reaction in boar spermatozoa. Theriogenology 59, 1171–1180.
| Changes in the distribution of lectin receptors during capacitation and acrosome reaction in boar spermatozoa.Crossref | GoogleScholarGoogle Scholar | 12527065PubMed |
Kamp, G., Büsselmann, G., Jones, N., Wiesner, B., and Lauterwein, J. (2003). Energy metabolism and intracellular pH in boar spermatozoa. Reproduction 126, 517–525.
| Energy metabolism and intracellular pH in boar spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpt1Cksr8%3D&md5=28d8690293fd34f080cd70b9c5830088CAS | 14525534PubMed |
Kasai, T., Ogawa, K., Mizuno, K., Nagai, S., Uchida, Y., Ohta, S., Fujie, M., Suzuki, K., Hirata, S., and Hoshi, K. (2002). Relationship between sperm mitochondrial membrane potential, sperm motility and fertility potential. Asian J. Androl. 4, 97–103.
| 12085099PubMed |
Krzyzosiak, J., Molan, P., and Vishwanath, R. (1999). Measurements of bovine sperm velocities under true anaerobic and aerobic conditions. Anim. Reprod. Sci. 55, 163–173.
| Measurements of bovine sperm velocities under true anaerobic and aerobic conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXivFelt7w%3D&md5=8947065b77855fe7ef41d174abac5d7fCAS | 10379669PubMed |
Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685.
| Cleavage of structural proteins during the assembly of the head of bacteriophage T4.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlsFags7s%3D&md5=6f0c22623faf3f19401c15a9d52476bdCAS | 5432063PubMed |
Lambrecht, M., and Transtschold, D. (1974). ATP determination with hexokinase and glucose 6-phosphate dehydrogenase. In ‘Methods of enzymatic analysis’. (Ed. H. U. Bergmeyer.) pp. 543–551. (Verlag Chemie: Weinheim, Germany.)
Lee, J. A., Spidlen, J., Boyce, K., Cai, J., Crosbie, N., Dalphin, M., Furlong, J., Gasparetto, M., Goldberg, M., Goralczykm, E. M., Hyun, B., Jansen, K., Kollmann, T., Kong, M., Leif, R., McWeeney, S., Moloshok, T. D., Moore, W., Nolan, G., Nolan, J., Nikolich-Zugich, J., Parrish, D., Pursel, B., Qian, Y., Selvaraj, B., Smith, C., Tchuvatkina, O., Wertheimer, A., Wilkinson, P., Wilson, C., Wood, J., Zigon, R., International Society for Advancement of Cytometry Data Standards Task Force Scheuermann, R. H., and Brinkman, R. R. (2008). MIFlowCyt: the minimum information about a flow cytometry experiment. Cytometry A 73A, 926–930.
| MIFlowCyt: the minimum information about a flow cytometry experiment.Crossref | GoogleScholarGoogle Scholar |
Marín, S., Chiang, K., Bassilian, S., Lee, W. N., Boros, L. G., Fernandez-Novell, J. M., Centelles, J. J., Medrano, A., Rodriguez-Gil, J. E., and Cascante, M. (2003). Metabolic strategy of boar spermatozoa revealed by metabolomic characterisation. FEBS Lett. 554, 342–346.
| Metabolic strategy of boar spermatozoa revealed by metabolomic characterisation.Crossref | GoogleScholarGoogle Scholar | 14623091PubMed |
Martínez-Pastor, F., Johannisson, A., Gil, J., Kaabi, M., Anel, L., Paz, P., and Rodríguez-Martínez, H. (2004). Use of chromatin stability assay, mitochondrial stain JC-1 and fluorometric assessment of plasma membrane to evaluate frozen–thawed ram semen. Anim. Reprod. Sci. 84, 121–133.
| Use of chromatin stability assay, mitochondrial stain JC-1 and fluorometric assessment of plasma membrane to evaluate frozen–thawed ram semen.Crossref | GoogleScholarGoogle Scholar | 15302392PubMed |
Medrano, A., Fernández-Novell, J. M., Ramió, L., Álvarez, J., Goldberg, E., Rivera, M. M., Guinovart, J. J., Rigau, T., and Rodríguez-Gil, J. E. (2006). Utilisation of citrate and lactate through a lactate dehydrogenase and ATP-regulated pathway in boar spermatozoa. Mol. Reprod. Dev. 73, 369–378.
| Utilisation of citrate and lactate through a lactate dehydrogenase and ATP-regulated pathway in boar spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhsVKhtL0%3D&md5=50bc9e758aa13bb958c6f2cd79fb0c3dCAS | 16362974PubMed |
Miki, K., Qu, W., Goulding, E. H., Willis, W. D., Bunch, D. O., Strader, L. F., Perreault, S. D., Eddy, E. M., and O’Brien, D. A. (2004). Glyceraldehyde 3-phosphate dehydrogenase-S, a sperm-specific glycolytic enzyme, is required for sperm motility and male fertility. Proc. Natl. Acad. Sci. USA 101, 16 501–16 506.
| Glyceraldehyde 3-phosphate dehydrogenase-S, a sperm-specific glycolytic enzyme, is required for sperm motility and male fertility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVOisbvJ&md5=11114ab9a05a1d5fc6b320bebc2c9409CAS |
Mukai, C., and Okuno, M. (2004). Glycolysis plays a major role for adenosine triphosphate supplementation in mouse sperm flagellar movement. Biol. Reprod. 71, 540–547.
| Glycolysis plays a major role for adenosine triphosphate supplementation in mouse sperm flagellar movement.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmtFWgur4%3D&md5=5caa61aa5496eaefc013d23f95ac4bf1CAS | 15084484PubMed |
Nascimento, J. M., Shi, L. Z., Tam, J., Chandsawangbhuwana, C., Durrant, B., Botvinick, E. L., and Berns, M. W. (2008). Comparison of glycolysis and oxidative phosphorylation as energy sources for mammalian sperm motility, using the combination of fluorescence imaging, laser tweezers and real-time automated tracking and trapping. J. Cell. Physiol. 217, 745–751.
| Comparison of glycolysis and oxidative phosphorylation as energy sources for mammalian sperm motility, using the combination of fluorescence imaging, laser tweezers and real-time automated tracking and trapping.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlOqt7rJ&md5=ad0f91964fab36686f41b8aed6bec1faCAS | 18683212PubMed |
Nohl, H., Kozlov, A. V., Gille, L., and Staniek, K. (2003). Cell respiration and formation of reactive oxygen species: facts and artefacts. Biochem. Soc. Trans. 31, 1308–1311.
| Cell respiration and formation of reactive oxygen species: facts and artefacts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXps12jsbw%3D&md5=dbd02a8fe7d94265c3805bdb3674c000CAS | 14641050PubMed |
O’Flaherty, C., de Lamirande, E., and Gagnon, C. (2006). Positive role of reactive oxygen species in mammalian sperm capacitation: triggering and modulation of phosphorylation events. Free Radic. Biol. Med. 41, 528–540.
| Positive role of reactive oxygen species in mammalian sperm capacitation: triggering and modulation of phosphorylation events.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XntlCqtrk%3D&md5=28899d27cbfe16f57ba0dc525c22f611CAS | 16863985PubMed |
Odet, F., Gabel, S., London, R. E., Goldberg, E., and Eddy, M. (2013). Glycolysis and mitochondrial respiration in mouse LDHC null sperm. Biol. Reprod. 88, 95.
| Glycolysis and mitochondrial respiration in mouse LDHC null sperm.Crossref | GoogleScholarGoogle Scholar | 23486916PubMed |
Pasupuleti, V. (2007). Role of glycolysis and respiration in sperm metabolism and motility. M.Sc. Thesis. Kent State University, Kent, OH, USA.
Peris, S., Solanes, D., Peña, A., Rodríguez-Gil, J. E., and Rigau, T. (2000). Ion-mediated resistance to osmotic changes of ram spermatozoa: the role of amiloride and ouabain. Theriogenology 54, 1453–1467.
| Ion-mediated resistance to osmotic changes of ram spermatozoa: the role of amiloride and ouabain.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXltFOntQ%3D%3D&md5=233ed3e3f3371da46b3a74ed18c96e21CAS | 11191869PubMed |
Petrunkina, A. M., and Harrison, R. A. P. (2010). Systematic mis-estimation of cell subpopulations by flow cytometry: a mathematical analysis. Theriogenology 73, 839–847.
| Systematic mis-estimation of cell subpopulations by flow cytometry: a mathematical analysis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3c3gtlKlsw%3D%3D&md5=cf81c2da390a2afc9fe4c77a2d35ce7cCAS | 19896183PubMed |
Petrunkina, A. M., Waberski, D., Bollwein, H., and Sieme, H. (2010). Identifying non-sperm particles during flow cytometric physiological assessment: a simple approach. Theriogenology 73, 995–1000.
| Identifying non-sperm particles during flow cytometric physiological assessment: a simple approach.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3c3gsVejtQ%3D%3D&md5=a83726cf4e3be80153906064e2fa578eCAS | 20171719PubMed |
Piomboni, P., Focarelli, R., Stendardi, A., Ferramosca, A., and Zara, V. (2012). The role of mitochondria in energy production for human sperm motility. Int. J. Androl. 35, 109–124.
| The role of mitochondria in energy production for human sperm motility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XnsVCgtL4%3D&md5=0d72fcb23a7d2cba12fd563b3a266097CAS | 21950496PubMed |
Publicover, S., Harper, C. V., and Barratt, C. (2007). [Ca2+] signalling in sperm: making the most of what you’ve got. Nat. Cell Biol. 9, 235–242.
| [Ca2+] signalling in sperm: making the most of what you’ve got.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXit12kurg%3D&md5=8a5bcc0d7e0a20a52f13e23ea8d90789CAS | 17330112PubMed |
Ramió, L., Rivera, M. M., Ramírez, A., Concha, I. I., Peña, A., Rigau, T., and Rodríguez-Gil, J. E. (2008). Dynamics of motile-sperm subpopulation structure in boar ejaculates subjected to in vitro capacitation and further in vitro acrosome reaction. Theriogenology 69, 501–512.
| Dynamics of motile-sperm subpopulation structure in boar ejaculates subjected to in vitro capacitation and further in vitro acrosome reaction.Crossref | GoogleScholarGoogle Scholar | 18068222PubMed |
Ramió-Lluch, L., Fernández-Novell, J. M., Peña, A., Colás, C., Cebrián-Pérez, J. A., Muiño-Blanco, T., Ramírez, A., Concha, I. I., Rigau, T., and Rodríguez-Gil, J. E. (2011). In vitro capacitation and acrosome reaction are concomitant with specific changes in mitochondrial activity in boar sperm: evidence for a nucleated mitochondrial activation and for the existence of a capacitation-sensitive subpopulational structure. Reprod. Domest. Anim. 46, 664–673.
| In vitro capacitation and acrosome reaction are concomitant with specific changes in mitochondrial activity in boar sperm: evidence for a nucleated mitochondrial activation and for the existence of a capacitation-sensitive subpopulational structure.Crossref | GoogleScholarGoogle Scholar | 21121968PubMed |
Ramió-Lluch, L., Fernández-Novell, J. M., Peña, A., Bucci, D., Rigau, T., and Rodríguez-Gil, J. E. (2012a). In vitro capacitation and subsequent acrosome reaction are related to changes in the expression and location of midpiece actin and mitofusin-2 in boar spermatozoa. Theriogenology 77, 979–988.
| In vitro capacitation and subsequent acrosome reaction are related to changes in the expression and location of midpiece actin and mitofusin-2 in boar spermatozoa.Crossref | GoogleScholarGoogle Scholar | 22192394PubMed |
Ramió-Lluch, L., Fernández-Novell, J. M., Peña, A., Ramírez, A., Concha, I. I., and Rodríguez-Gil, J. E. (2012b). In vitro capacitation and further in vitro progesterone-induced acrosome exocytosis are linked to specific changes in the expression and acrosome location of protein phosphprylation in serine residues of boar spermatozoa. Reprod. Domest. Anim. 47, 766–776.
| In vitro capacitation and further in vitro progesterone-induced acrosome exocytosis are linked to specific changes in the expression and acrosome location of protein phosphprylation in serine residues of boar spermatozoa.Crossref | GoogleScholarGoogle Scholar | 22188209PubMed |
Rich, P. R. (2003). The molecular machinery of Keilin’s respiratory chain. Biochem. Soc. Trans. 31, 1095–1105.
| The molecular machinery of Keilin’s respiratory chain.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXps1yqurk%3D&md5=9127ea556cb746606d4e9795d8e3c0deCAS | 14641005PubMed |
Rodríguez-Gil, J. E., and Rigau, T. (1996). Effects of ouabain on the response to osmotic changes in dog and boar spermatozoa. Theriogenology 45, 873–888.
| Effects of ouabain on the response to osmotic changes in dog and boar spermatozoa.Crossref | GoogleScholarGoogle Scholar | 16727849PubMed |
Rodríguez-Martínez, H. (2007). Role of the oviduct in sperm capacitation. Theriogenology 68, S138–S146.
| Role of the oviduct in sperm capacitation.Crossref | GoogleScholarGoogle Scholar | 17452049PubMed |
Ruíz-Pesini, E., Díez, C., López-Pérez, M. J., and Enríquez, J. A. (2007). The role of the mitochondrion in sperm function: is there a place for oxidative phosphorylation or is it a purely glycolytic process? Curr. Top. Dev. Biol. 77, 3–19.
| The role of the mitochondrion in sperm function: is there a place for oxidative phosphorylation or is it a purely glycolytic process?Crossref | GoogleScholarGoogle Scholar | 17222698PubMed |
Sachs, J. R. (1980). The order of release of sodium and addition of potassium in the sodium–potassium pump reaction mechanism. J. Physiol. 302, 219–240.
| 1:CAS:528:DyaL3cXkt1ehurY%3D&md5=db3e96f36f77cd212c29fc3a1578b4f2CAS | 6447780PubMed |
Shchepina, L. A., Pletjushkina, O. Y., Avetisyan, A. V., Bakkeva, L. E., Fetisova, E. K., Izyumov, D. S., Sprunova, V. B., Vyssokikh, M. Y., Chernyak, B. V., and Skulachev, V. P. (2002). Oligomycin, inhibitor of the F0 part of H+-ATP-synthase, suppresses the TNF-induced apoptosis. Oncogene 21, 8149–8157.
| Oligomycin, inhibitor of the F0 part of H+-ATP-synthase, suppresses the TNF-induced apoptosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XovVWhsrk%3D&md5=82807041038ac957c41179b42c7f1216CAS | 12444550PubMed |
Shinoda, T., Ogawa, H., Cornelius, F., and Toyoshima, C. (2009). Crystal structure of the sodium–potassium pump at 2.4A° resolution. Nature 459, 446–450.
| Crystal structure of the sodium–potassium pump at 2.4A° resolution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtFKmtbo%3D&md5=486e4fcc723004485445d7d75afd804eCAS | 19458722PubMed |
Storey, B. T. (2008). Mammalian sperm metabolism: oxygen and sugar, friend and foe. Int. J. Dev. Biol. 52, 427–437.
| Mammalian sperm metabolism: oxygen and sugar, friend and foe.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht12qs7bK&md5=50b0fdf521cd27afdabd76659bdbd026CAS | 18649255PubMed |
Suárez, S. S. (1996). Hyperactivated motility in sperm. J. Androl. 17, 331–335.
| 8889694PubMed |
Teves, M. E., Barbano, F., Guidobaldi, H. A., Sanchez, R., Miska, W., and Giojalas, L. C. (2006). Progesterone at the picomolar range is a chemoattractant for mammalian spermatozoa. Fertil. Steril. 86, 745–749.
| Progesterone at the picomolar range is a chemoattractant for mammalian spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFCqsLzJ&md5=355f9b1966bca42811d915cedca58991CAS | 16784744PubMed |
Travis, A. J., Jorges, C. J., Merduishev, T., Jones, B. H., Dess, D. M., Díaz-Cueto, L., Storey, B. T., Kopf, G. S., and Moss, S. B. (2001). Functional relationships between capacitation-dependent cell signalling and compartmentalised metabolic pathways in murine spermatozoa. J. Biol. Chem. 276, 7630–7636.
| Functional relationships between capacitation-dependent cell signalling and compartmentalised metabolic pathways in murine spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXisl2qsL8%3D&md5=9a1746bf66fe67c198d56b26e7f70f4cCAS | 11115497PubMed |
Tulsiani, D. R., Zeng, H. T., and Abou-Haila, A. (2007). Biology of sperm capacitation: evidence for multiple signalling pathways. Soc. Reprod. Fertil. Suppl. 63, 257–272.
| 1:CAS:528:DC%2BD1cXpvVyktLw%3D&md5=65cc17020b7317f79fbb04ec15705c47CAS | 17566278PubMed |
Urner, F., and Sakkas, D. (2003). Protein phosphorylation in mammalian spermatozoa. Reproduction 125, 17–26.
| Protein phosphorylation in mammalian spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhvFGls78%3D&md5=4b7369c17dce587494144c99158750caCAS | 12622692PubMed |
Visconti, P. E., and Kopf, G. (1998). Regulation of protein phosphorylation during sperm capacitation. Biol. Reprod. 59, 1–6.
| Regulation of protein phosphorylation during sperm capacitation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXktFaksLw%3D&md5=dabded89a0bf24a8d6ecb8c520214529CAS | 9674985PubMed |
Vívenes, C. Y., Peralta-Arias, R. D., Camejo, M. I., Guerrero, K., Fernández, V. H., Piñero, S., Proverbio, T., Proverbio, F., and Marín, R. (2009). Biochemical identification of dynein-ATPase activity in human sperm. Z. Naturforsch. C 64, 747–753.
| 19957446PubMed |
Wu, J. T., Chiang, K. C., and Cheng, F. P. (2006). Expression of progesterone receptor(s) during capacitation and incidence of acrosome reaction induced by progesterone and zona proteins in boar spermatozoa. Anim. Reprod. Sci. 93, 34–45.
| Expression of progesterone receptor(s) during capacitation and incidence of acrosome reaction induced by progesterone and zona proteins in boar spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XktFSrsrs%3D&md5=700f984bfcf09464c6e1094f22f0c529CAS | 16139444PubMed |
Yanagimachi, R. (1989). Sperm capacitation and gamete interaction. J. Reprod. Fertil. Suppl. 38, 27–33.
| 1:STN:280:DyaK3c%2Fht1Shtg%3D%3D&md5=8a76a7000535c6950de6dd70534d4db6CAS | 2677347PubMed |
Yanagimachi, R. (1994). Mammalian fertilization. In ‘Physiology of Reproduction. Vol 1’. (Eds E. Knobil and J. D. Neill.) pp. 189–317. (Raven Press: New York.)
Yeste, M., Estrada, E., Casas, I., Bonet, S., and Rodríguez-Gil, J. E. (2013). Good and bad freezability boar ejaculates differ in the integrity of nucleoprotein structure after freeze–thawing but not in ROS levels. Theriogenology , .
| Good and bad freezability boar ejaculates differ in the integrity of nucleoprotein structure after freeze–thawing but not in ROS levels.Crossref | GoogleScholarGoogle Scholar | 23773688PubMed |
