Spermatozoa of the old endemic rodents of Australia – the possible functional significance of their ventral processes
Simon Drew A , Chris Leigh A and William G. Breed A B
+ Author Affiliations
- Author Affiliations
A Discipline of Anatomy and Pathology, School of Medical Sciences, Faculty of Heath Sciences, The University of Adelaide, SA 5005, Australia.
B Corresponding author. Email: bill.breed@adelaide.edu.au
Reproduction, Fertility and Development 26(8) 1183-1187 https://doi.org/10.1071/RD13162
Submitted: 26 May 2013 Accepted: 13 September 2013 Published: 21 October 2013
Abstract
Spermatozoa of the plains mouse (Pseudomys australis), like those of most Australian old endemic rodents, contain, in addition to an apical hook, two further processes that extend from the upper concave surface of the head, the ventral processes. This study shows that these processes contain thiol-rich cytoskeletal proteins, which presumably help to maintain their rigidity during sperm transport, together with the overlying cell membrane having abundant intramembranous proteins. To determine the possible functional significance of these processes, an in vitro study of spermatozoon–zona binding was undertaken. The findings suggest that initial sperm binding occurs by way of the cell membrane over the acrosome of the apical hook and that, subsequently, the lateral surfaces of the ventral processes also become tightly bound to the zona matrix. These ventral processes may therefore have evolved to increase sperm adhesion to the outer zona surface and/or to enhance stabilisation of the spermatozoon at the time of zona binding and initial penetration of the egg coat.
Additional keywords: egg coats, hydromyine rodents.
References
Bedford, J. M. (1991). The co-evolution of mammalian gametes. In ‘A Comparative Overview of Mammalian Fertilization’. (Eds B. S. Dunbar and M. G. O’Rand.) pp. 3–30. (Plenum Press: New York.)Bedford, J. M. (2004). Enigmas of mammalian gamete form and function. Biol. Rev. Camb. Philos. Soc. 79, 429–460.
| Enigmas of mammalian gamete form and function.Crossref | GoogleScholarGoogle Scholar | 15191231PubMed |
Bedford, J. M., and Hoskins, D. D. (1990). The spermatozoon: morphology, physiology and biochemistry. In ‘Marshall’s Physiology of Reproduction: Reproduction in the Male. Vol. 2.’. 4th edn. (Ed. G. E. Lamming.) pp. 279–568. (Churchill Livingstone: London.)
Bleil, J. D., and Wasserman, P. M. (1983). Sperm–egg interactions in the mouse: sequence of events and induction of the acrosome reaction. Dev. Biol. 95, 317–324.
| Sperm–egg interactions in the mouse: sequence of events and induction of the acrosome reaction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXhtVGitL4%3D&md5=d4d83bdfa6d6bf650d22caa256983ac5CAS | 6402397PubMed |
Breed, W. G. (1984). Sperm head structure in the Hydromyinae (Rodentia: Muridae): a further evolutionary development of the subacrosomal space in mammals. Gamete Res. 10, 31–44.
| Sperm head structure in the Hydromyinae (Rodentia: Muridae): a further evolutionary development of the subacrosomal space in mammals.Crossref | GoogleScholarGoogle Scholar |
Breed, W. G. (2004). The spermatozoon of Eurasian murine rodents: its morphological diversity and evolution. J. Morphol. 261, 52–69.
| The spermatozoon of Eurasian murine rodents: its morphological diversity and evolution.Crossref | GoogleScholarGoogle Scholar | 15164367PubMed |
Breed, W. G., and Leigh, C. M. (1991). Distribution of filamentous actin in and around spermatids and in spermatozoa of Australian conilurine rodents. Mol. Reprod. Dev. 30, 369–384.
| Distribution of filamentous actin in and around spermatids and in spermatozoa of Australian conilurine rodents.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK38%2FovVGnsg%3D%3D&md5=011d42c5a9fea6421a8962bc0e231377CAS | 1751042PubMed |
Breed, W. G., Swift, J. G., and Mukherjee, T. M. (1988). Variation in intramembranous particle distribution in the cell membrane of the sperm head of the plains rat and western chestnut mouse (Pseudomys spp). J. Submicrosc. Cytol. Pathol. 20, 341–348.
| 1:STN:280:DyaL1c3ot1egsA%3D%3D&md5=00945fb7e1ad443c49d937769b3879f1CAS | 3395973PubMed |
Breed, W. G., Idriss, D., and Oko, R. (2000). Protein composition of the ventral processes on the sperm head of Australian hydromyine rodents. Biol. Reprod. 63, 629–634.
| Protein composition of the ventral processes on the sperm head of Australian hydromyine rodents.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXltl2gurY%3D&md5=a3ccc05bbbb56fc4685ea52c8f8ded54CAS | 10906074PubMed |
Breed, W. G., Idriss, D., Leigh, C. M., and Oko, R. (2009). Temporal deposition and spatial distribution of cytoskeletal proteins in the sperm head of an Australian rodent. Reprod. Fertil. Dev. 21, 428–439.
| Temporal deposition and spatial distribution of cytoskeletal proteins in the sperm head of an Australian rodent.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXisFemsLg%3D&md5=9cfb2cdeceab56e601753fee0fcba936CAS | 19261220PubMed |
Cummins, J. M., and Woodall, P. F. (1985). On mammalian sperm dimensions. J. Reprod. Fertil. 75, 153–175.
| On mammalian sperm dimensions.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2M3pt1yntA%3D%3D&md5=b5ec56d3f0da932d447ec8347235182aCAS | 4032369PubMed |
Fawcett, D. W. (1970). A comparative view of sperm ultrastructure. Biol. Reprod. 2, 90–127.
| A comparative view of sperm ultrastructure.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38rgsFSqug%3D%3D&md5=36353696784c1289ce8983eeb0e34b8dCAS | 5521054PubMed |
Fawcett, D. W. (1975). The mammalian spermatozoon. Dev. Biol. 44, 394–436.
| The mammalian spermatozoon.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE2M7mvVGmug%3D%3D&md5=ed0b5b02f5cebd3bbf641e713ce19fd8CAS | 805734PubMed |
Flaherty, S. P., and Breed, W. G. (1983). The sperm head of the plains mouse Pseudomys australis: ultrastructure and effects of chemical treatments. Gamete Res. 8, 231–244.
| The sperm head of the plains mouse Pseudomys australis: ultrastructure and effects of chemical treatments.Crossref | GoogleScholarGoogle Scholar |
Flaherty, S. P., Breed, W. G., and Sarafis, V. (1983). Localisation of actin in the sperm head of the plains mouse, Pseudomys australis. J. Exp. Zool. 225, 497–500.
| Localisation of actin in the sperm head of the plains mouse, Pseudomys australis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXhsFyhtL8%3D&md5=e46dba9d1a1457bab9ebe7f71ee0216eCAS | 6842163PubMed |
Florman, H. M., and Ducibella, T. (2006). Fertilization in mammals. In ‘Knobil and Neill’s Physiology of Reproduction’. 3rd edn. (Ed. J. D. Neill.) pp. 55–112. (Elsevier Academic Press: St Louis.)
Gage, M. J. G. (1998). Mammalian sperm morphometry. Proc. Biol. Sci. 265, 97–103.
| Mammalian sperm morphometry.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c7jsFWgtw%3D%3D&md5=e65597310a207784bbbacf700699115fCAS |
Gerton, G. L. (2002). Function of the sperm acrosome. In ‘Fertilization’. (Ed. D. M. Hardy.) pp. 266–302. (Academic Press: San Diego.)
Lalli, M., and Clermont, Y. (1981). Structural changes of the head components of the rat spermatid during spermiogenesis. Am. J. Anat. 160, 419–434.
| Structural changes of the head components of the rat spermatid during spermiogenesis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL38%2FitV2htg%3D%3D&md5=4000fb8a0b703df8ca6a99ca1c48d02eCAS | 7282567PubMed |
Oko, R., and Clermont, Y. (1988). Isolation, structure and protein composition of the perforatorium of rat spermatozoa. Biol. Reprod. 39, 673–687.
| Isolation, structure and protein composition of the perforatorium of rat spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXmt1Omsrg%3D&md5=ca12f0015bbcc4c2b07c607b9b7a2c31CAS | 3196798PubMed |
Oko, R., Moussakova, L., and Clermont, Y. (1990). Regional differences in composition of the perforatorium and outer periacrosomal layer of the rat spermatozoon as revealed by immunocytochemistry. Am. J. Anat. 188, 64–73.
| Regional differences in composition of the perforatorium and outer periacrosomal layer of the rat spermatozoon as revealed by immunocytochemistry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXktlyjsrw%3D&md5=945fad09311ac576a90b0e7836551edfCAS | 2346120PubMed |
Saling, P. M., Sowinski, J., and Storey, B. T. (1979). An ultrastructure study of epididymal mouse spermatozoa binding to the zonae pellucidae in vitro: sequential relationship to the acrosome reaction J. Exp. Zool. 209, 229–238.
| An ultrastructure study of epididymal mouse spermatozoa binding to the zonae pellucidae in vitro: sequential relationship to the acrosome reactionCrossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3c%2FntlyrtQ%3D%3D&md5=87047bfcd1fa4c95b1503120493cb252CAS | 512592PubMed |
Shalgi, R., Seligma, J., and Kosower, N. S. (1989). Dynamics of thiol status of rat sperm during maturation: analysis with labelling agent monobromobimane. Biol. Reprod. 40, 1037–1045.
| Dynamics of thiol status of rat sperm during maturation: analysis with labelling agent monobromobimane.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXltFakurY%3D&md5=ec42dc99a1978cd9c5529f35d88902f2CAS | 2765609PubMed |
Talbot, P. (1985). Sperm penetration through oocyte investments in mammals. Am. J. Anat. 174, 331–346.
| Sperm penetration through oocyte investments in mammals.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL28%2Fntl2quw%3D%3D&md5=724a5037de03b712fd0f5b933d53573bCAS | 4072945PubMed |
Talbot, P., Shur, B. D., and Myles, D. G. (2003). Cell adhesion and fertilisation: steps in oocyte transport, sperm–zona pellucida interactions and sperm–egg fusion. Biol. Reprod. 68, 1–9.
| Cell adhesion and fertilisation: steps in oocyte transport, sperm–zona pellucida interactions and sperm–egg fusion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjtVOq&md5=98019fff2a9df8a969fc1ed4c7de9f6dCAS | 12493688PubMed |
Yanagimachi, R. (1988). Mammalian fertilization. In ‘The Physiology of Reproduction Vol. 1’. 2nd edn. (Eds E. Knobil and J. D. Neill.) pp. 136–185. (Raven Press: New York.)
