Sperm‐egg interaction in the painted frog (Discoglossus pictus): An ultrastructural study

Campanella, Chiara; Carotenuto, R.; Infante, Vincenzo; Maturi, G.; Atripaldi, U.

doi:10.1002/(sici)1098-2795(199707)47:3<323::aid-mrd11>3.3.co;2-b

Cited by 10 publications

(13 citation statements)

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“…Our recent data suggest that molecules homologous to SMIS in egg-jelly may initiate or activate sperm motility in the external fertilization of a primitive species of anuran amphibian, Discoglossus pictus (Watanabe et al, unpublished data) and of an urodele amphibian, Hynobius lichenatus (Ohta and Watanabe, unpublished data). Furthermore, acrosome reaction-inducing activity is localized in the outermost layer of Discoglossus egg-jelly (Campanella et al, 1997), suggesting that a similar mechanism of sperm motility initiation mediated by the acrosome reaction may exist in other amphibian species regardless of their modes of fertilization. On the other hand, this mechanism does not operate in fertilization in X. laevis or B. japonicus, in which the acrosome reaction is induced on the vitelline envelope after their sperm pass through the jelly layer (Yoshizaki and Katagiri, 1982;Ueda et al, 2002).…”

Section: A B C Dmentioning

confidence: 99%

Identification of the sperm motility-initiating substance in the newt, Cynops pyrrhogaster, and its possible relationship with the acrosome reaction during internal fertilization

Watanabe¹,

Kubo²,

Takeshima³

et al. 2010

Int. J. Dev. Biol.

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Motility initiation is a key event during internal fertilization of female-stored sperm, although the underlying mechanisms remain unclear. In internally fertilizing urodeles, quiescent sperm initiate motility on the surface of the egg-jelly, a thick extracellular matrix that accumulates around the egg in oviduct. By immunizing mice with egg-jelly extracts, we successfully generated an α34 monoclonal antibody (mAb) which neutralized sperm motility-initiating activity in the eggjelly of the newt, Cynops pyrrhogaster, in a dose-dependent manner. The α34 mAb recognized an unglycosylated 34 kDa protein in the outermost of the six layers that comprise egg-jelly. Under nonreducing conditions, immunoblotting with α34 mAb produced many bands in addition to the 34 kDa protein, suggesting that the 34 kDa protein associates not only with the jelly matrix itself, but also with additional substances present in the matrix. Our current results are compatible with the supposed features of sperm motility-initiating substance (SMIS), indicating that the 34 kDa protein itself, or a complex consisting of the 34 kDa protein and some other molecules, is the SMIS in C. pyrrhogaster. Immunofluorescence staining further indicated that SMIS was distributed in a dot-like pattern in the outermost jelly layer and was fully covered with acrosome reactioninducing substance (ARIS). Immunocytochemical and scanning electron microscopic examinations of the outermost jelly layer strongly suggests that the 34 kDa protein localized in granules (2 μm) and that ARIS was distributed covering the granules and in the sheet-like structure above the granules. These data suggest that the initiation of sperm motility is mediated by the acrosome reaction.

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Section: A B C Dmentioning

confidence: 99%

Identification of the sperm motility-initiating substance in the newt, Cynops pyrrhogaster, and its possible relationship with the acrosome reaction during internal fertilization

Watanabe¹,

Kubo²,

Takeshima³

et al. 2010

Int. J. Dev. Biol.

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“…Figure 1(d) depicts a spermatozoon in the VE. The plasma membrane and the outer acrosome membrane are in the process of vesiculation and only the outermost acrosome component is present in the acrosome cap (see Campanella et al, 1997).…”

Section: Resultsmentioning

confidence: 99%

Sulphated glycoconjugates are powerful inhibitors of spermatozoa binding to the vitelline envelope in amphibian eggs

Caputo

Riccio

Paglierucci

et al. 2005

Biology of the Cell

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Background information. In amphibians, the role of sulphated glycans has not been determined in spermatozoa-egg interaction, although they are known to be involved in other systems. In previous studies, it was found that, in Discoglossus pictus, a VE (vitelline envelope) glycoprotein of 63 kDa exhibits high homology to Xenopus laevis gp69/gp64 and to ZP2 of mammals. gp63 and a glycoprotein of 75 kDa are both capable of binding the spermatozoa in in vitro assays and, having similar peptide maps and different glycosylation, are probably two glycoforms of the same protein.Results. In the present study, binding assays performed by treating dejellied eggs with metaperiodate suggest that hydroxy groups of sugars are not directly involved in spermatozoa-vitelline envelope binding. Competition assays between dejellied eggs and spermatozoa preincubated with dextran, dextran sulphate or fucoidan indicated that sulphated oligosaccharides have an inhibitory effect on spermatozoa binding. In similar competition assays, Le x (Lewis x ) trisaccharide 3 -sulphate inhibited spermatozoa binding to VE in contrast with 3 -sialyl-Le x tetrasaccharide. Assays performed with gp75-or gp63-coated beads and spermatozoa treated with fucoidan or dextran sulphate indicated that sulphated oligosaccharides competitively inhibit spermatozoa binding to gp75-coated beads, yet not to gp63-coated beads. Finally, solubilized VE digested with N-glycosidase F retains the inhibitory activity in spermatozoa-VE binding assays in contrast with VE treated with α-N-acetylgalactosaminidase. Conclusion.It was concluded that VE sulphate groups are involved in spermatozoa binding. These groups are present in gp75 glycoconjugates and are probably located in O-linked glycoconjugates.

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“…SMIS activity is present in the jelly layers of the externally fertilizing urodele Hynobius lichenatus and the anuran Discoglossus pictus , indicating that SMIS activity is widely conserved among urodeles and anurans. In the primitive anuran D. pictus , the acrosome reaction (AR) is induced in the outermost jelly sublayer (Campanella et al 1997 ), although a thick layer of jelly matrix covers the outer surface without locating granules (Takayama-Watanabe et al 2012 ;Fig. 8.2b ).…”

Section: Smis Activity In the Amphibian Jelly Layermentioning

confidence: 99%

Acrosome Reaction-Mediated Motility Initiation That Is Critical for the Internal Fertilization of Urodele Amphibians

Takayama‐Watanabe

Takahashi

Watanabe

2014

Sexual Reproduction in Animals and Plants

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The reproductive modes of extant amphibians are highly diversifi ed in their adaptation to species-specifi c reproductive environments. In the external fertilization of most amphibians, fertilization begins from motility initiation of the sperm by the hyposmolality of freshwater at spawning, whereas in internal fertilization, the sperm initiate motility without any change in osmolality. Acrosome reaction (AR)-mediated motility initiation is an initial event of the internal fertilization of the urodele amphibian Cynops pyrrhogaster , also known as the Japanese fi re belly newt. It initiates motility of female-stored sperm on the surface of the jelly layer in the cloaca. This unique mechanism of motility initiation is based on the fi ne structure of the jelly matrix, in which AR-inducing substance (ARIS) and sperm motilityinitiating substance (SMIS) are localized in the sheet-like structure covering the outer surface and in the granules beneath it. The ARIS and the SMIS repeatedly increase the sperm intracellular Ca 2+ level and result in the sporadic initiation of motility within 4 min. The SMIS activity is also present in the jelly layer of the externally fertilizing anuran amphibian Discoglossus pictus (the Mediterranean painted frog), but a thick layer of matrix simply covers the outer surface of the jelly layer. The AR-mediated mechanism may be established in the reproductive strategies for the internal fertilization of urodeles.

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Sperm‐egg interaction in the painted frog (Discoglossus pictus): An ultrastructural study

Cited by 10 publications

References 0 publications

Identification of the sperm motility-initiating substance in the newt, Cynops pyrrhogaster, and its possible relationship with the acrosome reaction during internal fertilization

Identification of the sperm motility-initiating substance in the newt, Cynops pyrrhogaster, and its possible relationship with the acrosome reaction during internal fertilization

Sulphated glycoconjugates are powerful inhibitors of spermatozoa binding to the vitelline envelope in amphibian eggs

Acrosome Reaction-Mediated Motility Initiation That Is Critical for the Internal Fertilization of Urodele Amphibians

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