Spermatozoa of the Shrew, Suncus murinus, Undergo the Acrosome Reaction and Then Selectively Kill Cells in Penetrating the Cumulus Oophorus1

Kaneko, Tadaaki; Iida, Hiroshi; Bedford, J. M.; Mōri, Takayuki

doi:10.1095/biolreprod65.2.544

Cited by 17 publications

(16 citation statements)

References 31 publications

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“…This interaction appears to initiate the acrosome reaction, following which such spermatozoa then lose the reacted acrosomal carapace well before reaching the zona pellucida. Even more striking, reacted S. murinus spermatozoa enter and kill cumulus cells along a radial line in moving toward the inner perizonal space (Kaneko et al, 2001). This unusual mode of cumulus penetration stands in sharp contrast to that in other Eutheria, in which spermatozoa -whether reacted or not -pass between the constituent cells of the cumulus.…”

Section: Sperm/egg Interactionsmentioning

confidence: 85%

Novelties of conception in insectivorous mammals (Lipotyphla), particularly shrews

Bedford

Mock

2004

Biological Reviews

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In the order Lipotyphla (Insectivora), certain reproductive features differ quite distinctly from the eutherian norms, and are of interest with regard to the evolution of mammalian gamete function and perhaps for questions of lipotyphlan phylogeny. As seen in one or more members of five lipotyphlan families (shrews, moles, hedgehogs, golden moles, tenrecs), these features can involve the configuration of the male tract including the penis, the morphology of the sperm head, the anatomy of the oviduct and the patterns of sperm transport within it, the character of the cumulus oophorus, and the way in which fertilising spermatozoa interact with the eggs. However, the picture is by no means uniform within the order. Reproductive idiosyncrasies occur variously in the different lipotyphlan families, and appear consistently and strikingly in shrews--the group studied most extensively. Compared to the patterns in most Eutheria, the most interesting anomalies in soricids include (a) the regulation of sperm transport to the site of fertilisation by oviduct crypts, whose arrangement can vary even according to species, (b) a circumscribed matrix-free cumulus oophorus that appears essential for fertilisation as the inducer of the acrosome reaction, (c) barbs on the acrosome-reacted sperm head by which it may attach to the zona pellucida. With regard to the bearing such reproductive traits might have on lipotyphlan systematics, the African mouse shrew (Myosorex varius) displays a mix of traits that characterize either crocidurine or soricine shrews, consistent with the proposal that it belongs in a more primitive tribe, Myosoricinae, or subfamily, the Crocidosoricinae, from which the crocidurine and soricine lines probably evolved. Moreover, although elephant shrews are assigned now to a separate order (Macroscelidea), they display several of the unusual reproductive features seen in lipotyphlans, particularly in chrysochlorids and tenrecs. On the other hand, if used as a phylogenetic yardstick, none of the reproductive features described serves to define the Lipotyphla as classically constituted within one order, nor necessarily all the relationships suggested by recent sequencing studies of nuclear and mitochondrial genes.

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Section: Sperm/egg Interactionsmentioning

confidence: 85%

Novelties of conception in insectivorous mammals (Lipotyphla), particularly shrews

Bedford

Mock

2004

Biological Reviews

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“…SEM observations also indicate that sperm heads initiate penetration parallel to the surface of the hamster ZP [58,59] and that the physical properties of the outer surface of the ZP may be important for human sperm adhesion [60]. An extreme case of physical interaction between mammalian gametes is given by a shrew, the sperm of which appears to bind to the ZP after the acrosomal reaction by barbs of the perforatorium [61]. Anyway, adhesion to-and onset of penetration of the ZP would probably be less easy if its surface was flat and smooth.…”

Section: Surfacementioning

confidence: 99%

Texture of the zona pellucida of the mature pig oocyte. The mammalian egg envelope revisited

et al. 2004

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-The zona pellucida (ZP) of mature pig oocytes is believed to consist of a dense filamentous meshwork, less compact on the inner and outer faces. The uneven surface of the ZP is made of unordered and stretched fibrils surrounding deep funnels which are the openings of the radial canaliculi. The topography of the ZP surface may contribute to the initial interplay between male and female gametes. Using cytochemical techniques for transmission electron microscopy (TEM), such as tannic acid and ruthenium red treatments, we found that the ZP of pig oocytes was essentially made of bundles of fibrils distributed in concentric layers (except in the innermost and outer parts). A correlation appears between the dense structure of the core layer of the ZP and its texture: it is constituted of superposed layers of fibril bundles, whereas only a random meshwork is found in a very thin innermost and in the outer layer. The fascicular configuration may control the permeability of the ZP, giving its semi-rigidity and elasticity, and may facilitate sperm penetration. The liquid crystal-like design of the core layer of the ZP is similar to textures found in the the vitelline envelope (zona radiata) of other vertebrates and possibly of all the deuterostomes. Such texture is probably related to the unique ZP protein composition and to a coordinated synthesis. vitelline envelope / ultrastructural cytochemistry / glycoproteins / liquid crystal-like texture / Sus scrofa Abbreviations PVS: perivitelline space; SEM: scanning electron microscopy; TEM: transmission electron microscopy; ZP: zona pellucida.

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“…This model has received much support from light microscopic analyses of in vitro sperm-egg interaction in the mouse. However, the membrane fusion process of the acrosome reaction is beyond the resolving power of the light microscope and studies of in vivo sperm-egg interaction in some mammalian species indicate that the acrosome reaction is initiated as spermatozoa traverse the cumulus cell layer of the egg (Bedford, 1998;Kaneko et al, 2001). Thus, although the time of the initiation of the acrosome reaction in vivo remains debatable, in most mammalian species it appears to be completed on the zona surface (Bedford, 1998;Cherr et al, 1986;Yanagimachi and Phillips, 1984).…”

Section: Introductionmentioning

confidence: 99%

Structural modification of the hamster sperm acrosome during posttesticular development in the epididymis

Olson

Winfrey

NagDas

2003

Microscopy Res & Technique

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The acrosome of the mature spermatozoon functions as a regulated secretory vesicle which performs several critical functions in mammalian fertilization. Acrosome assembly occurs throughout spermiogenesis and continues during posttesticular sperm maturation in the epididymis, resulting in a structurally polarized membrane-bounded organelle that contains an assortment of hydrolases and a stable infrastructure termed the acrosomal matrix. The role of stable acrosomal matrix assemblies in acrosomal biogenesis and function are poorly understood. This article presents ultrastructural, immunocytochemical, and biochemical data on the remodeling of the hamster acrosomal matrix during spermiogenesis and posttesticular sperm maturation in the epididymis. Specific posttranslational modifications of the major acrosomal matrix protein are evident in late, step 16, spermatids and matrix protein processing continues within specific acrosomal subdomains of caput epididymal spermatozoa. At the completion of sperm maturation, the acrosomal matrix consists of two structurally distinct domains which are adherent to the outer acrosomal membrane and exhibit a localized distribution pattern. Coincident with acrosomal matrix differentiation, a paracrystalline cytoskeletal complex is assembled onto the outer acrosomal membrane of epididymal spermatozoa. This cytoskeletal network appears to establish transmembrane structural interactions with the acrosomal matrix and may maintain attachment of the acrosomal cap to the sperm head during the early steps of the acrosome reaction.

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Spermatozoa of the Shrew, Suncus murinus, Undergo the Acrosome Reaction and Then Selectively Kill Cells in Penetrating the Cumulus Oophorus1

Cited by 17 publications

References 31 publications

Novelties of conception in insectivorous mammals (Lipotyphla), particularly shrews

Novelties of conception in insectivorous mammals (Lipotyphla), particularly shrews

Texture of the zona pellucida of the mature pig oocyte. The mammalian egg envelope revisited

Structural modification of the hamster sperm acrosome during posttesticular development in the epididymis

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