Sperm motility activation in the critically endangered booroolong frog: the effect of medium osmolality and phosphodiesterase inhibitors
Aimee J. Silla A B , Leesa M. Keogh A and Phillip G. Byrne AA Centre for Sustainable Ecosystem Solutions, School of Biological Sciences, University of Wollongong, Northfields Ave, Wollongong, NSW 2522, Australia.
B Corresponding author. Email: aimee.silla@gmx.com
Reproduction, Fertility and Development 29(11) 2277-2283 https://doi.org/10.1071/RD17012
Submitted: 3 November 2016 Accepted: 4 March 2017 Published: 31 March 2017
Abstract
Effective activation of sperm motility is fundamental to successful artificial fertilisation; however, studies investigating optimal procedures in amphibians are lacking. This study found the optimal osmolality of activation media for sperm motility activation and evaluated the effect of phosphodiesterase (PDE) inhibitors on sperm activation and longevity in the critically endangered booroolong frog, Litoria booroolongensis. To assess the effect of medium osmolality (10, 25, 50, 75, 100 and 200 mOsmol kg−1) and PDE inhibitors (control, 2.5 mM caffeine, 5 mM caffeine, 2.5 mM pentoxifylline, 5 mM pentoxifylline, 2.5 mM theophylline and 5 mM theophylline) on initial activation, percentage sperm motility and sperm velocity were quantified using computer-assisted sperm analysis. To assess the effect of PDE inhibitors (control, 2.5 mM caffeine and 2.5 mM theophylline) on sperm longevity, percentage motility and velocity were assessed hourly until 10 h after activation. High (>60%) percentage motility was achieved in a broad range of activation-medium osmolalities (10–75 mOsmol kg−1). PDE inhibitors did not have an effect on initial sperm motility or velocity, but caffeine and theophylline improved sperm longevity, significantly increasing motility and velocity at 8, 9 and 10 h after activation. Data also show that sperm longevity in L. booroolongensis is extreme, with spermatozoa remaining motile more than twice as long as those of any other anuran amphibian.
Additional keywords: amphibian, antioxidant, artificial fertilisation, assisted reproduction, IVF, reproduction technologies, spermatozoa.
References
Benau, D., and Terner, C. (1980). Initiation, prolongation, and reactivation of the motility of salmonid spermatozoa. Gamete Res. 3, 247–257.| Initiation, prolongation, and reactivation of the motility of salmonid spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXmtlGlt70%3D&md5=3db8e07f88243617ccfc81395ef8f537CAS |
Boswell-Smith, V., Spina, D., and Page, C. P. (2006). Phosphodiesterase inhibitors. Br. J. Pharmacol. 147, S252–S257.
| Phosphodiesterase inhibitors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XisVCksw%3D%3D&md5=c4a53183b282fc69f6a30923309ba387CAS |
Browne, R. K., Clulow, J., and Mahony, M. (2001). Short-term storage of cane toad (Bufo marinus) gametes. Reproduction 121, 167–173.
| Short-term storage of cane toad (Bufo marinus) gametes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnslaqsg%3D%3D&md5=c41cb3a1d0ab64c708328ce95c71fa94CAS |
Browne, R. K., Kaurova, S. A., Uteshev, V. K., Shishova, N. V., McGinnity, D., Figiel, C. R., Mansour, N., Agney, D., Wu, M., Gakhova, E. N., Dzuba, B., and Cosson, J. (2015). Sperm motility of externally fertilizing fish and amphibians. Theriogenology 83, 1–13.e8.
| Sperm motility of externally fertilizing fish and amphibians.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2MzitV2kug%3D%3D&md5=1c11f7bdba1f032a6ff86e0430612ecaCAS |
Byrne, P. G., and Silla, A. J. (2010). Hormonal induction of gamete release, and in vitro fertilisation, in the critically endangered southern corroboree frog, Pseudophryne corroboree. Reprod. Biol. Endocrinol. 8, 144.
| Hormonal induction of gamete release, and in vitro fertilisation, in the critically endangered southern corroboree frog, Pseudophryne corroboree.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFelu7rE&md5=4ad3cc1d14ecaba07dcfcca61025857dCAS |
Byrne, P. G., Dunne, C., Munn, A. J., and Silla, A. J. (2015). Environmental osmolality influences sperm motility activation in an anuran amphibian. J. Evol. Biol. 28, 521–534.
| Environmental osmolality influences sperm motility activation in an anuran amphibian.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2Mvmt1answ%3D%3D&md5=ea453b14cbe4831a3762f2de3f3cd97eCAS |
Calogero, A. E., Fishel, S., Hall, J., Ferrara, E., Vicari, E., Green, S., Hunter, A., Burrello, N., Thornton, S., and D’Agata, R. (1998). Correlation between intracellular cAMP content, kinematic parameters and hyperactivation of human spermatozoa after incubation with pentoxifylline. Hum. Reprod. 13, 911–915.
| Correlation between intracellular cAMP content, kinematic parameters and hyperactivation of human spermatozoa after incubation with pentoxifylline.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjs12gtbg%3D&md5=9e48cfeaf27723dcd32ac85877981fc1CAS |
Christensen, J. R. (2002). The effects of environmental contaminants on metamorphosis in Rana catesbeiana and sperm motility in Xenopus laevis. Retrospective Theses and Dissertations, 1919–2007 , .
| The effects of environmental contaminants on metamorphosis in Rana catesbeiana and sperm motility in Xenopus laevis.Crossref | GoogleScholarGoogle Scholar |
Cosson, J. (2004). The ionic and osmotic factors controlling motility of fish spermatozoa. Aquaculture Int. 12, 69–85.
| The ionic and osmotic factors controlling motility of fish spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhsFSjsro%3D&md5=722bb14caea264a734d2cea3387054efCAS |
Costanzo, J. P., Mugnano, J. A., Wehrheim, H. M., and Lee, R. E. (1998). Osmotic and freezing tolerance in spermatozoa of freeze-tolerant and -intolerant frogs. Am. J. Physiol. 275, R713–R719.
| 1:CAS:528:DyaK1cXmtFWjtbo%3D&md5=05fbf9c36f32354d6fe9e36253e00b58CAS |
Devasagayam, T. P. A., Kamat, J. P., Mohan, H., and Kesavan, P. C. (1996). Caffeine as an antioxidant: inhibition of lipid peroxidation induced by reactive oxygen species. Biochim. Biophys. Acta 1282, 63–70.
| Caffeine as an antioxidant: inhibition of lipid peroxidation induced by reactive oxygen species.Crossref | GoogleScholarGoogle Scholar |
Dias, T. R., Alves, M. G., Tomás, G. D., Socorro, S., Silva, B. M., and Oliveira, P. F. (2014). White tea as a promising antioxidant medium additive for sperm storage at room temperature: a comparative study with green tea. J. Agric. Food Chem. 62, 608–617.
| White tea as a promising antioxidant medium additive for sperm storage at room temperature: a comparative study with green tea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXitVWnsLvF&md5=08a8837bbb366669132a97c229290ab5CAS |
Durrant, B. S. (2009). The importance and potential of artificial insemination in CANDES (companion animals, non-domestic, endangered species). Theriogenology 71, 113–122.
| The importance and potential of artificial insemination in CANDES (companion animals, non-domestic, endangered species).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1cjnt1Snsg%3D%3D&md5=b546a83e751818ff039e22a9ebda280dCAS |
Edwards, D. L., Mahony, M. J., and Clulow, J. (2004). Effect of sperm concentration, medium osmolality and oocyte storage on artificial fertilisation success in a myobatrachid frog (Limnodynastes tasmaniensis). Reprod. Fertil. Dev. 16, 347–354.
| Effect of sperm concentration, medium osmolality and oocyte storage on artificial fertilisation success in a myobatrachid frog (Limnodynastes tasmaniensis).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2cvgtF2gsw%3D%3D&md5=d3fe7e6c40cf194ac395d3905df9b2abCAS |
Fitzsimmons, C., McLaughlin, E., Mahony, M., and Clulow, J. (2007). Optimisation of handling, activation and assessment procedures for Bufo marinus spermatozoa. Reprod. Fertil. Dev. 19, 594–601.
| Optimisation of handling, activation and assessment procedures for Bufo marinus spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXltFyisbc%3D&md5=274f40fce795458e3b329060d22b1897CAS |
Guthrie, H. D., and Welch, G. R. (2012). Effects of reactive oxygen species on sperm function. Theriogenology 78, 1700–1708.
| Effects of reactive oxygen species on sperm function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XosFCgsLw%3D&md5=d5ddc98ad5448b1528cfad6856e8ec15CAS |
Kashou, A. H., Sharma, R., and Agarwal, A. (2013). Assessment of oxidative stress in sperm and semen. In ‘Spermatogenesis: Methods and Protocols’. (Eds T. D. Carrell and I. K. Aston.) pp. 351–361. (Humana Press: Totowa, NJ, USA.)
Keogh, L. M., Byrne, P. G., and Silla, A. J. (2017). The effect of gentamicin on sperm motility and bacterial abundance during chilled sperm storage in the Booroolong frog. Gen. Comp. Endocrinol. 243, 51–59.
| The effect of gentamicin on sperm motility and bacterial abundance during chilled sperm storage in the Booroolong frog.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhvVGqtL%2FE&md5=93859dd87bbea6f759c43958684371f5CAS |
Kopf, G. S., Lewis, C. A., and Vacquier, V. D. (1983). Regulation of abalone sperm cyclic AMP concentrations and the acrosome reaction by calcium and methylxanthines. Dev. Biol. 98, 28–36.
| Regulation of abalone sperm cyclic AMP concentrations and the acrosome reaction by calcium and methylxanthines.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXktF2qsL4%3D&md5=ab6c54e2dc4db79df698d3c59bf6ca07CAS |
Kouba, A. J., Vance, C. K., Frommeyer, M. A., and Roth, T. L. (2003). Structural and functional aspects of Bufo americanus spermatozoa: effects of inactivation and reactivation. J. Exp. Zoolog. Part A Comp. Exp. Biol. 295A, 172–182.
| Structural and functional aspects of Bufo americanus spermatozoa: effects of inactivation and reactivation.Crossref | GoogleScholarGoogle Scholar |
Kouba, A. J., Lloyd, R. E., Houck, M. L., Silla, A. J., Calatayud, N., Trudeau, V. L., Clulow, J., Molinia, F., Langhorne, C., Vance, C., and Arregui, L. (2013). Emerging trends for biobanking amphibian genetic resources: the hope, reality and challenges for the next decade. Biol. Conserv. 164, 10–21.
| Emerging trends for biobanking amphibian genetic resources: the hope, reality and challenges for the next decade.Crossref | GoogleScholarGoogle Scholar |
Lahnsteiner, F., Mansour, N., and Plaetzer, K. (2010). Antioxidant systems of brown trout (Salmo trutta f. fario) semen. Anim. Reprod. Sci. 119, 314–321.
| Antioxidant systems of brown trout (Salmo trutta f. fario) semen.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXktVait7g%3D&md5=75701216a7382acecee9d49c1aebfc72CAS |
Morisawa, M., and Ishida, K. (1987). Short‐term changes in levels of cyclic AMP, adenylate cyclase, and phosphodiesterase during the initiation of sperm motility in rainbow trout. J. Exp. Zool. 242, 199–204.
| Short‐term changes in levels of cyclic AMP, adenylate cyclase, and phosphodiesterase during the initiation of sperm motility in rainbow trout.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXksFKhsrg%3D&md5=cc1a2e9101d0b01e85bb4e18b2703c43CAS |
Mostafa, T. (2008). Oral phosphodiesterase-5 inhibitors and sperm functions. Int. J. Impot. Res. 20, 530–536.
| Oral phosphodiesterase-5 inhibitors and sperm functions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlCksrrE&md5=d0b40accffd66d169924ac012c21fcf1CAS |
O’Brien, E. D., Krapf, D., Cabada, M. O., Visconti, P. E., and Arranz, S. E. (2011). Transmembrane adenylyl cyclase regulates amphibian sperm motility through protein kinase A activation. Dev. Biol. 350, 80–88.
| Transmembrane adenylyl cyclase regulates amphibian sperm motility through protein kinase A activation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnsVSksA%3D%3D&md5=1fa97adf7d2741014dff6a81053a130eCAS |
Pankaj, P. K., Raina, V. J., Roy, B., Mohanty, T. K., and Mishra, A. (2009). Effect of antioxidant preservative on cold protection ability of low-grade riverine buffalo (Bubalus bubalis) bull spermatozoa. Asian-Australas. J. Anim. Sci. 22, 626–635.
| Effect of antioxidant preservative on cold protection ability of low-grade riverine buffalo (Bubalus bubalis) bull spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXot12rtL4%3D&md5=b6ce687e30a1df79c5ef75416ecd11ddCAS |
Roth, T. L., Howard, J. G., Donoghue, A. M., Swanson, W. F., and Wildt, D. E. (1994). Function and culture requirements of snow leopard (Panthera uncia) spermatozoa in vitro. J. Reprod. Fertil. 101, 563–569.
| Function and culture requirements of snow leopard (Panthera uncia) spermatozoa in vitro.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2M%2FlsFCjsQ%3D%3D&md5=81f6907e6991ee24f1f5ecf70a832152CAS |
Safarinejad, M. R. (2011). Effect of pentoxifylline on semen parameters, reproductive hormones, and seminal plasma antioxidant capacity in men with idiopathic infertility: a randomized double-blind placebo-controlled study. Int. Urol. Nephrol. 43, 315–328.
| Effect of pentoxifylline on semen parameters, reproductive hormones, and seminal plasma antioxidant capacity in men with idiopathic infertility: a randomized double-blind placebo-controlled study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmtVyls7s%3D&md5=e935afe263aebeaf6124034649c96c7cCAS |
Silla, A. J. (2011). Effect of priming injections of luteinizing hormone-releasing hormone on spermiation and ovulation in Günther’s toadlet, Pseudophryne guentheri. Reprod. Biol. Endocrinol. 9, 68.
| Effect of priming injections of luteinizing hormone-releasing hormone on spermiation and ovulation in Günther’s toadlet, Pseudophryne guentheri.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmvVKrt7k%3D&md5=df96fdea642af8f3d47bc5f9bb824724CAS |
Silla, A. J. (2013). Artificial fertilisation in a terrestrial toadlet (Pseudophryne guentheri): effect of medium osmolality, sperm concentration and gamete storage. Reprod. Fertil. Dev. 25, 1134–1141.
| Artificial fertilisation in a terrestrial toadlet (Pseudophryne guentheri): effect of medium osmolality, sperm concentration and gamete storage.Crossref | GoogleScholarGoogle Scholar |
Silla, A. J., Keogh, L. M., and Byrne, P. G. (2015). Antibiotics and oxygen availability affect the short-term storage of spermatozoa from the critically endangered booroolong frog, Litoria booroolongensis. Reprod. Fertil. Dev. 27, 1147–1153.
| Antibiotics and oxygen availability affect the short-term storage of spermatozoa from the critically endangered booroolong frog, Litoria booroolongensis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhs1Glu7jO&md5=00ccd3dbce850ed37b0fdaa3adbca589CAS |
Snook, R. R. (2005). Sperm in competition: not playing by the numbers. Trends Ecol. Evol. 20, 46–53.
| Sperm in competition: not playing by the numbers.Crossref | GoogleScholarGoogle Scholar |
Stephens, T. D., Brooks, R. M., Carrington, J. L., Cheng, L., Carrington, A. C., Porr, C. A., and Splan, R. K. (2013). Effects of pentoxifylline, caffeine, and taurine on post-thaw motility and longevity of equine frozen semen. J. Equine Vet. Sci. 33, 615–621.
| Effects of pentoxifylline, caffeine, and taurine on post-thaw motility and longevity of equine frozen semen.Crossref | GoogleScholarGoogle Scholar |
Stockley, P., Gage, M. J. G., Parker, G. A., and Moller, A. P. (1996). Female reproductive biology and the coevolution of ejaculate characteristics in fish. Proc. R. Soc. Lond. B Biol. Sci. 263, 451–458.
| Female reproductive biology and the coevolution of ejaculate characteristics in fish.Crossref | GoogleScholarGoogle Scholar |
Wolf, D. P., and Hedrick, J. L. (1971). A molecular approach to fertilization 11. Viability and artificial fertilization of Xenopus laevis gametes. Dev. Biol. 25, 360–376.
| A molecular approach to fertilization 11. Viability and artificial fertilization of Xenopus laevis gametes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3MXkslejt70%3D&md5=55fb163881e56cfb68555d495a17f383CAS |
Yovich, J. L. (1993). Pentoxifylline: actions and applications in assisted reproduction. Hum. Reprod. 8, 1786–1791.
| Pentoxifylline: actions and applications in assisted reproduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXitlKhs7w%3D&md5=5f85cc66dbb400d42e87c6dde0a6c628CAS |
Yunes, R., Fernández, P., Doncel, G. F., and Acosta, A. A. (2005). Cyclic nucleotide phosphodiesterase inhibition increases tyrosine phosphorylation and hyper motility in normal and pathological human spermatozoa. Biocell 29, 287–293.
| 1:CAS:528:DC%2BD28Xjt1GiurY%3D&md5=671ea4f1320c3574503a1d42a23cd9b3CAS |