Sperm motility activation, sperm heterogeneity and sperm–female tract interactions in Bennett’s wallaby (Macropus rufogriseus rufogriseus)
Janneke Boere A B , Daniela Esteban Díaz C and William V. Holt A D
+ Author Affiliations
- Author Affiliations
A Institute of Zoology, Regent’s Park, London, NW1 4RY, UK.
B Royal Veterinary College, University of London, London, NW1 0UT, UK.
C Departamento de Fisiología Animal, Facultad de Veterinaria, Universidad de Murcia, Murcia 30071, Spain.
D Corresponding author. Email: bill.holt@ioz.ac.uk
Reproduction, Fertility and Development 23(4) 603-617 https://doi.org/10.1071/RD10257
Submitted: 6 October 2010 Accepted: 17 December 2011 Published: 3 May 2011
Abstract
Sperm–oviduct interactions in Bennett’s wallaby (Macropus rufogriseus rufogriseus) were investigated using in vitro cocultures of cauda epididymal spermatozoa and oviducal epithelial cells. Kidney epithelial cells were used as non-reproductive control tissues. Spermatozoa attached to epithelial cells of both origins, but sperm survival and activity was higher when cocultured with oviducal cells. New findings during live sperm–epithelial interactions included: (1) a high frequency of reversible head movements, from linear (streamlined configuration) to T shape (thumbtack configuration) in swimming spermatozoa immediately after the start of coculture; (2) the loss of sperm tails (tail shedding) increasing with time; and (3) interrupted swimming patterns, where periods of fast movement were interspersed with slower swimming while the spermatozoa interacted with the epithelial cell surface. Sperm motility activation responses were characterised after diluting the epididymal samples in phosphate-buffered saline, medium M199 and Tyrode’s medium. The results confirmed that the marsupial oviduct is able to support the viability and motility of a sperm subpopulation for at least 20 h in vitro and suggest that some spermatozoa shed their tails after binding, possibly as a result of a selective process.
Additional keywords: fertilisation, marsupial, maturation, sperm morphology.
References
Abaigar, T., Holt, W. V., Harrison, R. A. P., and del Barrio, G. (1999). Sperm subpopulations in boar (Sus scrofa) and gazelle (Gazella dama mhorr) semen as revealed by pattern analysis of computer-assisted motility assessments. Biol. Reprod. 60, 32–41.| Sperm subpopulations in boar (Sus scrofa) and gazelle (Gazella dama mhorr) semen as revealed by pattern analysis of computer-assisted motility assessments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhvFymtA%3D%3D&md5=e5d9639628b855a15be854e09d43a428CAS | 9858483PubMed |
Barth, A. D., and Oko, R. I. (1989). ‘Abnormal Morphology of Bovine Spermatozoa.’ (Iowa State University Press: Ames.)
Bedford, J. M., and Breed, W. G. (1994). Regulated storage and subsequent transformation of spermatozoa in the fallopian tubes of an Australian marsupial, Sminthopsis crassicaudata. Biol. Reprod. 50, 845–854.
| Regulated storage and subsequent transformation of spermatozoa in the fallopian tubes of an Australian marsupial, Sminthopsis crassicaudata.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2c3lslOmug%3D%3D&md5=7af068837232a80d7561cd9b8a442f7cCAS | 8199265PubMed |
Bennetts, L., Lin, M., and Aitken, R. J. (2004). Cyclic AMP-dependent tyrosine phosphorylation in tammar wallaby (Macropus eugenii) spermatozoa. J. Exp. Zoolog. A Comp. Exp. Biol. 301, 118–130.
Boyers, S. P., Davis, R., and Katz, D. F. (1989). Automated semen analysis. Curr. Probl. Obstet. Gynecol. 12, 172–200.
Breed, W. G., Leigh, C. M., and Bennett, J. H. (1989). Sperm morphology and storage in the female reproductive tract of the fat-tailed dunnart, Sminthopsis crassicaudata (Marsupialia: Dasyuridae). Gamete Res. 23, 61–75.
| Sperm morphology and storage in the female reproductive tract of the fat-tailed dunnart, Sminthopsis crassicaudata (Marsupialia: Dasyuridae).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1MzgslWiuw%3D%3D&md5=5b7f04fb3c53975d1869036262a87116CAS | 2744705PubMed |
Brewis, I. A., and Gadella, B. M. (2010). Sperm surface proteomics: from protein lists to biological function. Mol. Hum. Reprod. 16, 68–79.
| Sperm surface proteomics: from protein lists to biological function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXktlCitw%3D%3D&md5=8d127dab8d32803c4fadad9b05c3c6eaCAS | 19717474PubMed |
Brüssow, K. P., Ratky, J., and Rodriguez-Martinez, H. (2008). Fertilization and early embryonic development in the porcine fallopian tube. Reprod. Domest. Anim. 43, 245–251.
| Fertilization and early embryonic development in the porcine fallopian tube.Crossref | GoogleScholarGoogle Scholar | 18638131PubMed |
Clulow, J., Jones, R. C., and Murdoch, R. N. (1992). Maturation and regulation of the motility of spermatozoa in the epididymis of the tammar wallaby (Macropus eugenii). J. Reprod. Fertil. 94, 295–303.
| Maturation and regulation of the motility of spermatozoa in the epididymis of the tammar wallaby (Macropus eugenii).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK383nslGjtw%3D%3D&md5=a09cad91575ac24d0eb10d5fc7016270CAS | 1593531PubMed |
Coy, P., Lloyd, R., Romar, R., Satake, N., Matas, C., Gadea, J., and Holt, W. V. (2010). Effects of porcine pre-ovulatory oviductal fluid on boar sperm function. Theriogenology 74, 632–642.
| Effects of porcine pre-ovulatory oviductal fluid on boar sperm function.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cjms1GntA%3D%3D&md5=bca88ea93cfbcb607297a44d585e63d9CAS | 20363019PubMed |
Dawson, L., and Flannery, T. (1985). Taxonomic and phylogenetic status of living and fossil kangaroos and wallabies of the genus Macropus Shaw (Macropodidae, Marsupialia), with a new subgeneric name for the larger wallabies. Aust. J. Zool. 33, 473–498.
| Taxonomic and phylogenetic status of living and fossil kangaroos and wallabies of the genus Macropus Shaw (Macropodidae, Marsupialia), with a new subgeneric name for the larger wallabies.Crossref | GoogleScholarGoogle Scholar |
Elliott, R. M., Lloyd, R. E., Fazeli, A., Sostaric, E., Georgiou, A. S., Satake, N., Watson, P. F., and Holt, W. V. (2009). Effects of HSPA8, an evolutionarily conserved oviductal protein, on boar and bull spermatozoa. Reproduction 137, 191–203.
| Effects of HSPA8, an evolutionarily conserved oviductal protein, on boar and bull spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXovV2ks7g%3D&md5=c61ce8f1e8b398c6683b6c82944c0100CAS | 18996976PubMed |
Fazeli, A., Duncan, A. E., Watson, P. F., and Holt, W. V. (1999). Sperm–oviduct interaction: induction of capacitation and preferential binding of uncapacitated spermatozoa to oviductal epithelial cells in porcine species. Biol. Reprod. 60, 879–886.
| Sperm–oviduct interaction: induction of capacitation and preferential binding of uncapacitated spermatozoa to oviductal epithelial cells in porcine species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXitVGru7k%3D&md5=37c2a569a4ac0bd926faf69d89179cabCAS | 10084961PubMed |
Fleming, D., Cinderey, R. N., and Hearn, J. P. (1983). The reproductive biology of Bennett’s wallaby (Macropus rufogriseus rufogriseus) ranging free at Whipsnade park. J. Zool. 201, 283–291.
| The reproductive biology of Bennett’s wallaby (Macropus rufogriseus rufogriseus) ranging free at Whipsnade park.Crossref | GoogleScholarGoogle Scholar |
Gualtieri, R., and Talevi, R. (2003). Selection of highly fertilization-competent bovine spermatozoa through adhesion to the fallopian tube epithelium in vitro. Reproduction 125, 251–258.
| Selection of highly fertilization-competent bovine spermatozoa through adhesion to the fallopian tube epithelium in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXisVKlt7g%3D&md5=088398e3998d9b0432151a1c98cb914cCAS | 12578539PubMed |
Holt, W. V. (2009). Is semen analysis useful to predict the odds that the sperm will meet the egg? Reprod. Domest. Anim. 44, 31–38.
| Is semen analysis useful to predict the odds that the sperm will meet the egg?Crossref | GoogleScholarGoogle Scholar | 19660078PubMed |
Holt, W. V., and Fazeli, A. (2010). The oviduct as a complex mediator of mammalian sperm function and selection. Mol. Reprod. Dev. 77, 934–943.
| The oviduct as a complex mediator of mammalian sperm function and selection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsVCktrnL&md5=41d2ac2d921a2c1528fdb462b219dfddCAS | 20886635PubMed |
Holt, W. V., and Harrison, R. A. (2002). Bicarbonate stimulation of boar sperm motility via a protein kinase A-dependent pathway: between-cell and between-ejaculate differences are not due to deficiencies in protein kinase A activation. J. Androl. 23, 557–565.
| 1:CAS:528:DC%2BD38Xlt1KhsLc%3D&md5=9664566914bfb7314ec4b463e641ef60CAS | 12065464PubMed |
Holt, W. V., and Lloyd, R. E. (2010). Sperm storage in the vertebrate female reproductive tract: how does it work so well? Theriogenology 73, 713–722.
| Sperm storage in the vertebrate female reproductive tract: how does it work so well?Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3c7ot1Wqsw%3D%3D&md5=9a02eb0a505862065c7ff5ef0a0cbd2aCAS | 19632711PubMed |
Holt, W. V., and Van Look, K. J. W. (2004). Concepts in sperm heterogeneity, sperm selection and sperm competition as biological foundations for laboratory tests of semen quality. Reproduction 127, 527–535.
| Concepts in sperm heterogeneity, sperm selection and sperm competition as biological foundations for laboratory tests of semen quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXkvFOqurk%3D&md5=4232b4ba93313db4c65bcf28659caa02CAS | 15129008PubMed |
Holt, C., Holt, W. V., and Moore, H. D. M. (1996). Choice of operating conditions to minimize sperm subpopulation sampling bias in the assessment of boar semen by computer-assisted semen analysis. J. Androl. 17, 587–596.
| 1:STN:280:DyaK2s7hs1Kitw%3D%3D&md5=4f8dc990ba3fcf9f487f3b6731e6558eCAS | 8957703PubMed |
Holt, C., Holt, W. V., Moore, H. D. M., Reed, H. C. B., and Curnock, R. M. (1997). Objectively measured boar sperm motility parameters correlate with the outcomes of on-farm inseminations. Results of two fertility trials. J. Androl. 18, 20–31.
Holt, W. V., Penfold, L. M., Johnston, S. D., Temple-Smith, P., McCallum, C., Shaw, J., Lindemans, W., and Blyde, D. (1999). Cryopreservation of macropodid spermatozoa: new insights from the cryomicroscope. Reprod. Fertil. Dev. 11, 345–353.
| Cryopreservation of macropodid spermatozoa: new insights from the cryomicroscope.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3cvktVehug%3D%3D&md5=9c70a9255207912c9d464c22e2482533CAS | 10972303PubMed |
Holt, W. V., O’Brien, J., and Abaigar, T. (2007). Applications and interpretation of computer-assisted sperm analyses and sperm sorting methods in assisted breeding and comparative research. Reprod. Fertil. Dev. 19, 709–718.
| Applications and interpretation of computer-assisted sperm analyses and sperm sorting methods in assisted breeding and comparative research.Crossref | GoogleScholarGoogle Scholar | 17714625PubMed |
Hunter, R. H. F. (1981). Sperm transport and reservoirs in the pig oviduct in relation to the time of ovulation. J. Reprod. Fertil. 63, 109–117.
| Sperm transport and reservoirs in the pig oviduct in relation to the time of ovulation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL38%2FhtVeqtA%3D%3D&md5=37ce7d5f85e8660ea84c618213ed8442CAS | 6895091PubMed |
Johnston, S. D., McGowan, M. R., Carrick, F. N., Cameron, R. D., and Tribe, A. (1994). Seminal characteristics and spermatozoal morphology of captive Queensland koalas (Phascolarctos cinereus adustus). Theriogenology 42, 501–511.
| Seminal characteristics and spermatozoal morphology of captive Queensland koalas (Phascolarctos cinereus adustus).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1MfhsVOjsw%3D%3D&md5=58cecdcc5ffce533fc6ffb7926d122b7CAS | 16727557PubMed |
Jones, R. C., and Clulow, J. (1994). Interactions of sperm and the reproductive ducts of the male tammar wallaby, Macropus eugenii (Macropodidae: Marsupialia). Reprod. Fertil. Dev. 6, 437–444.
| Interactions of sperm and the reproductive ducts of the male tammar wallaby, Macropus eugenii (Macropodidae: Marsupialia).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2M7otlOgtw%3D%3D&md5=971114d05b4a7dd4e9d81ca2de8d3c09CAS | 7878219PubMed |
Jones, R. C., and Murdoch, R. N. (1996). Regulation of the motility and metabolism of spermatozoa for storage in the epididymis of eutherian and marsupial mammals. Reprod. Fertil. Dev. 8, 553–568.
| Regulation of the motility and metabolism of spermatozoa for storage in the epididymis of eutherian and marsupial mammals.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2s%2FitlOnsw%3D%3D&md5=cc6bae09871b451a547916481e9ab0bdCAS | 8870080PubMed |
Khalil, A. A., Petrunkina, A. M., Sahin, E., Waberski, D., and Topfer-Petersen, E. (2006). Enhanced binding of sperm with superior volume regulation to oviductal epithelium. J. Androl. 27, 754–765.
| Enhanced binding of sperm with superior volume regulation to oviductal epithelium.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28nksF2jsA%3D%3D&md5=33e8001d98aca7e67c53dc9310476286CAS | 16809276PubMed |
Lin, M., and Rodger, J. C. (1999). Acrosome formation during sperm transit through the epididymis in two marsupials, the tammar wallaby (Macropus eugenii) and the brushtail possum (Trichosurus vulpecula). J. Anat. 194, 223–232.
| Acrosome formation during sperm transit through the epididymis in two marsupials, the tammar wallaby (Macropus eugenii) and the brushtail possum (Trichosurus vulpecula).Crossref | GoogleScholarGoogle Scholar | 10337954PubMed |
Lloyd, R. E., Badia, E., Fazeli, A., Watson, P. F., and Holt, W. V. (2008). Temporal dynamics of ram sperm binding and survival during 48-h coculture with oviducal epithelial cells. Reprod. Fertil. Dev. 20, 835–845.
| Temporal dynamics of ram sperm binding and survival during 48-h coculture with oviducal epithelial cells.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1cnkvF2gsA%3D%3D&md5=fdb0e64cf4c05be0cc2dfb6255633365CAS | 18842186PubMed |
Mack, S. O., Tash, J. S., and Wolf, D. P. (1989). Effect of measurement conditions on quantification of hyperactivated human-sperm subpopulations by digital image-analysis. Biol. Reprod. 40, 1162–1169.
| Effect of measurement conditions on quantification of hyperactivated human-sperm subpopulations by digital image-analysis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1MznsFGmsQ%3D%3D&md5=91b0cbef04c4757d0fd4055c51fa2335CAS | 2775811PubMed |
Mate, K. E., and Rodger, J. C. (1996). Capacitation and the acrosome reaction in marsupial spermatozoa. Reprod. Fertil. Dev. 8, 595–603.
| Capacitation and the acrosome reaction in marsupial spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2s%2FitlOntg%3D%3D&md5=9e246e9ab9377a91e705aac515b0c6faCAS | 8870083PubMed |
Mate, K. E., Sidhu, K. S., Molinia, F. C., Glazier, A. M., and Rodger, J. C. (2000). Sperm binding and penetration of the zona pellucida in vitro but not sperm–egg fusion in an Australian marsupial, the brushtail possum (Trichosurus vulpecula). Zygote 8, 189–196.
| Sperm binding and penetration of the zona pellucida in vitro but not sperm–egg fusion in an Australian marsupial, the brushtail possum (Trichosurus vulpecula).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3cvmt1CntA%3D%3D&md5=a3575b9e297c34b4db2157aa1da03056CAS | 11014497PubMed |
McClean, R., MacCallum, C., Blyde, D., Holt, W. V., and Johnston, S. D. (2006). Ultrastructure, osmotic tolerance, glycerol toxicity and cryopreservation of caput and cauda epididymidal kangaroo spermatozoa. Reprod. Fertil. Dev. 18, 469–476.
| Ultrastructure, osmotic tolerance, glycerol toxicity and cryopreservation of caput and cauda epididymidal kangaroo spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjtV2hu7w%3D&md5=61c00103a4008aa51977c74ad1f9257cCAS | 16737640PubMed |
McClean, R. V., Holt, W. V., and Johnston, S. D. (2007). Ultrastructural observations of cryoinjury in kangaroo spermatozoa. Cryobiology 54, 271–280.
| Ultrastructural observations of cryoinjury in kangaroo spermatozoa.Crossref | GoogleScholarGoogle Scholar | 17462621PubMed |
Murdoch, R. N., Jones, R. C., Wade, M., and Lin, M. (1999). The ultrastructure and metabolism of ejaculated tammar wallaby sperm are impaired by swim-up procedures when compared with sperm from the cauda epididymidis. Reprod. Fertil. Dev. 11, 263–271.
| The ultrastructure and metabolism of ejaculated tammar wallaby sperm are impaired by swim-up procedures when compared with sperm from the cauda epididymidis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3czovFentg%3D%3D&md5=4f9ff260ab5e53ca227ad98f19dc72e6CAS | 10898291PubMed |
Paris, D. B., Taggart, D. A., Paris, M. C., Temple-Smith, P. D., and Renfree, M. B. (2004). Sperm transport, size of the seminal plug and the timing of ovulation after natural mating in the female tammar wallaby Macropus eugenii. Reprod. Fertil. Dev. 16, 811–822.
| Sperm transport, size of the seminal plug and the timing of ovulation after natural mating in the female tammar wallaby Macropus eugenii.Crossref | GoogleScholarGoogle Scholar | 15740705PubMed |
Pena, F. J., Saravia, F., Garcia-Herreros, M., Nunez-Martinez, I., Tapia, J. A., Johannisson, A., Wallgren, M., and Rodriguez-Martinez, H. (2005). Identification of sperm morphometric subpopulations in two different portions of the boar ejaculate and its relation to postthaw quality. J. Androl. 26, 716–723.
| Identification of sperm morphometric subpopulations in two different portions of the boar ejaculate and its relation to postthaw quality.Crossref | GoogleScholarGoogle Scholar | 16291966PubMed |
Petrunkina, A. M., and Topfer-Petersen, E. (2000). Heterogeneous osmotic behaviour in boar sperm populations and its relevance for detection of changes in plasma membrane. Reprod. Fertil. Dev. 12, 297–305.
| Heterogeneous osmotic behaviour in boar sperm populations and its relevance for detection of changes in plasma membrane.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MzpvF2jsw%3D%3D&md5=7aab2255e6ec595499e9dda3d950c92cCAS | 11451021PubMed |
Quintero-Moreno, A., Miro, J., Rigau, T. A., and Rodriguez-Gil, J. E. (2003). Identification of sperm subpopulations with specific motility characteristics in stallion ejaculates. Theriogenology 59, 1973–1990.
| Identification of sperm subpopulations with specific motility characteristics in stallion ejaculates.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3s7mslWquw%3D%3D&md5=4545a1e6cae9a1af5772da21f160cc55CAS | 12600734PubMed |
Ramio, L., Rivera, M. M., Ramirez, A., Concha, I. I., Pena, A., Rigau, T., and Rodriguez-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 | 1:STN:280:DC%2BD1c%2FovFSgug%3D%3D&md5=e740ab3a88d000fa75d55592308fc063CAS | 18068222PubMed |
Rigau, T., Farre, M., Ballester, J., Mogas, T., Pena, A., and Rodriguez-Gil, J. E. (2001). Effects of glucose and fructose on motility patterns of dog spermatozoa from fresh ejaculates. Theriogenology 56, 801–815.
| Effects of glucose and fructose on motility patterns of dog spermatozoa from fresh ejaculates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnvF2mtL4%3D&md5=50de3de89fd819e23d581052bf3f5bb9CAS | 11665883PubMed |
Rodriguez-Martinez, H., Saravia, F., Wallgren, M., Tienthai, P., Johannisson, A., Vazquez, J. M., Martinez, E., Roca, J., Sanz, L., and Calvete, J. J. (2005). Boar spermatozoa in the oviduct. Theriogenology 63, 514–535.
| Boar spermatozoa in the oviduct.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjsVSr&md5=0d0e658847d7638a3103691ef931e4abCAS | 15626414PubMed |
Setiadi, D., Lin, M., and Rodger, J. C. (1997). Posttesticular development of spermatozoa of the tammar wallaby (Macropus eugenii). J. Anat. 190, 275–288.
| Posttesticular development of spermatozoa of the tammar wallaby (Macropus eugenii).Crossref | GoogleScholarGoogle Scholar | 9061449PubMed |
Sidhu, K. S., Mate, K. E., and Rodger, J. C. (1998). Sperm–oviduct epithelial cell monolayer co-culture: an in vitro model of sperm–female tract interactions in a marsupial, the tammar wallaby (Macropus eugenii). J. Reprod. Fertil. 114, 55–61.
| Sperm–oviduct epithelial cell monolayer co-culture: an in vitro model of sperm–female tract interactions in a marsupial, the tammar wallaby (Macropus eugenii).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXotFektrw%3D&md5=0b86ee152a8b88a649efb5243120cb44CAS | 9875155PubMed |
Sidhu, K. S., Mate, K. E., Molinia, F. C., Glazier, A. M., and Rodger, J. C. (1999a). Secretory proteins from the female reproductive tract of the brushtail possum (Trichosurus vulpecula): binding to sperm and effects on sperm survival in vitro. Reprod. Fertil. Dev. 11, 329–336.
| Secretory proteins from the female reproductive tract of the brushtail possum (Trichosurus vulpecula): binding to sperm and effects on sperm survival in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlvVSltrc%3D&md5=9468e4ee7fda3eeb021435b874794affCAS | 10972301PubMed |
Sidhu, K. S., Mate, K. E., Molinia, F. C., and Rodger, J. C. (1999b). Induction of thumbtack sperm during coculture with oviduct epithelial cell monolayers in a marsupial, the brushtail possum (Trichosurus vulpecula). Biol. Reprod. 61, 1356–1361.
| Induction of thumbtack sperm during coculture with oviduct epithelial cell monolayers in a marsupial, the brushtail possum (Trichosurus vulpecula).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmvFertL8%3D&md5=e2ad3d220b6bcc55500b34c837bb3967CAS | 10529285PubMed |
Sistina, Y., Lin, M., Mate, K. E., and Rodger, J. C. (1993). Induction of the marsupial sperm acrosome reaction in-vitro by treatment with diacylglycerols. J. Reprod. Fertil. 99, 335–341.
| Induction of the marsupial sperm acrosome reaction in-vitro by treatment with diacylglycerols.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXivFGhsrg%3D&md5=d25a240bc2abe9de10adc31c4a9470b9CAS | 8107014PubMed |
Suarez, S. S. (2008). Regulation of sperm storage and movement in the mammalian oviduct. Int. J. Dev. Biol. 52, 455–462.
| Regulation of sperm storage and movement in the mammalian oviduct.Crossref | GoogleScholarGoogle Scholar | 18649258PubMed |
Talevi, R., and Gualtieri, R. (2010). Molecules involved in sperm–oviduct adhesion and release. Theriogenology 73, 796–801.
| Molecules involved in sperm–oviduct adhesion and release.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXivFGltrw%3D&md5=715743a45fe897bde19cde1fe2d7bc22CAS | 19682733PubMed |
