Morphological and Biochemical Changes of Isolated Chicken Egg-Envelope During Sperm Penetration: Degradation of the 97-Kilodalton Glycoprotein Is Involved in Sperm-Driven Hole Formation on the Egg-Envelope1

Takeuchi, Yukinari; Cho, Ritsuko; Iwata, Yuji; Nishimura, Keiji; Kato, Takeshi; Aoki, Naohito; Kitajima, Ken; Matsuda, Tsukasa

doi:10.1095/biolreprod64.3.822

Cited by 30 publications

(31 citation statements)

References 43 publications

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“…From these observations, the acrosomal contents including protease are not that important for achieving fertilization in mice. In birds, the holes that form in the pvm due to sperm during fertilization are huge compared with those in the mammalian ZP, the fibers in the holes disappear, and the edges of the holes appear to be smooth (Takeuchi et al 2001). The holes do not develop only by the mechanical force generated by sperm motility but also by other means, namely, a protease.…”

Section: Discussionmentioning

confidence: 99%

Sperm proteasome degrades egg envelope glycoprotein ZP1 during fertilization of Japanese quail (Coturnix japonica)

Sasanami¹,

Sugiura²,

Tokumoto³

et al. 2012

Reproduction

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At the time of fertilization, the extracellular matrix surrounding avian oocytes, termed the perivitelline membrane (pvm), is hydrolyzed by a sperm-borne protease, although the actual protease that is responsible for the digestion of the pvm remains to be identified. Here, we show evidence that the ubiquitin-proteasome system is functional in the fertilization of Japanese quail. The activities for the induction of the acrosome reaction and binding to ZP3 as revealed by ligand blotting of purified serum ZP1 are similar to those of pvm ZP1. Western blot analysis of purified ZP1 and ZP3 by the use of the anti-ubiquitin antibody showed that only pvm ZP1 was reactive to the antibody. In vitro penetration assay of the sperm on the pvm indicated that fragments of ZP1 and intact ZP3 were released from the pvm. Western blot analysis using the anti-20S proteasome antibody and ultrastructural analysis showed that immunoreactive proteasome was localized in the acrosomal region of the sperm. Inclusion of specific proteasome inhibitor MG132 in the incubation mixture, or depletion of extracellular ATP by the addition of apyrase, efficiently suppressed the sperm perforation of the pvm. These results demonstrate for the first time that the sperm proteasome is important for fertilization in birds and that the extracellular ubiquitination of ZP1 might occur during its transport via blood circulation.

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Section: Discussionmentioning

confidence: 99%

Sperm proteasome degrades egg envelope glycoprotein ZP1 during fertilization of Japanese quail (Coturnix japonica)

Sasanami¹,

Sugiura²,

Tokumoto³

et al. 2012

Reproduction

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“…At the state of the F1 follicle, the PL is composed of the IPVL in construction (Elis et al 2008), very closely surrounded (tide junctions) by granulosa cells. At the ovulation state, the PL is composed of IPVL mainly comprising ZP proteins (Waclawek et al 1998, Takeuchi et al 2001, Bausek et al 2004, Okumura et al 2004. At the oviposition state, a mean of 24 h after ovulation and possible in vivo fertilization, the PL is composed of two layers, the IPVL and the OPVL.…”

Section: Discussionmentioning

confidence: 99%

“…PLs were isolated at different states of the daily reproductive cycle of hens. IPVLs were isolated from pre-ovulatory mature follicles (F1) as described previously by Takeuchi et al (2001) or from just ovulated eggs (Batellier et al 2003). They were homogenized in 150 mM NaCl with 20 mM TES (N-Tris-[hydroxymethyl]-methyl-2-aminoethanesulfonic acid) at pH 7.4 (NaCl-TES) as described previously by Horrocks et al (2000).…”

Section: Incubation Of Spermatozoamentioning

confidence: 99%

“…The IPVL can be considered to a certain extent as analogous to the mammalian zona pellucida (ZP; Waclawek et al 1998). It consists of ZP glycoproteins that are homologous to the mammalian ZP proteins known to have a key role in sperm binding to the ZP and in the induction of acrosomal exocytosis (Waclawek et al 1998, Takeuchi et al 2001, Bausek et al 2004, Okumura et al 2004.…”

Section: Introductionmentioning

confidence: 99%

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A reappraisal of the factors involved in in vitro initiation of the acrosome reaction in chicken spermatozoa

Lemoine¹,

Grasseau²,

Brillard³

et al. 2008

Reproduction

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Chicken spermatozoa may remain in the female oviduct for a prolonged period before induction of the acrosome reaction on contact with the inner perivitelline layer (IPVL). By contrast, the acrosome reaction may be induced very rapidly in vitro in the presence of IPVL and Ca 2C. In the present study, we examined the extent to which the chicken acrosome reaction can be induced in media of various compositions in the presence or absence of IPVL and/or Ca 2C and other factors known to be efficient in mammals. We also compared the efficacy of perivitelline layer (PL) taken at various states of oocyte maturation in initiating the reaction. The acrosome reaction was induced in less than 5 min in the presence of Ca 2C and IPVL. Incubation of spermatozoa in different saline media (Beltsville poultry semen extender (BPSE); Dulbecco's modified eagle medium; NaCl-TES buffer) without IPVL showed a significant induction of acrosome reaction in BPSE supplemented with 5 mM Ca 2C and in the three media after supplementation with Ca 2C and Ca 2C ionophore A23187.By contrast, the acrosome reaction was never induced without Ca 2C. BSA, NaHCO 3 , and progesterone did not stimulate the acrosome reaction. Ca 2C plus PL taken at various physiological states (follicle IPVL, ovulated IPVL, oviposited IPVL, and/or outer perivitelline layer) strongly stimulated the acrosome reaction, the latest states being the most efficient. Although PL induced the acrosome reaction in the presence of extracellular Ca 2C, it was not possible to induce hyperactivation in chicken spermatozoa. Taken together, these results emphasize the central role of Ca 2C in the in vitro initiation of the acrosome reaction in chickens and show specific features of this induction in birds.

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“…In the case of ZP1, this is spaced from the central trefoil domain and C-terminal ZP module by a Pro/Thr/Leu-rich region, which in chicken ZP1 is expanded into an approximately 450-residue linker containing a highly repetitive sequence pattern [60]. Moreover, in a subset of ZP1 homologues, the N-terminal ZP-N domain contains an additional unpaired Cys residue within the loop between b-strands C and D, which is presumably responsible for forming an intermolecular disulfide bond that underlies the observed homodimerization of chicken, mouse, and human ZP1 [2,61,62].…”

Section: Implications For the Overall Domain Architecture Of The Zpmentioning

confidence: 99%

A Structural View of Egg Coat Architecture and Function in Fertilization1

Monné¹,

Jovine²

2011

Biology of Reproduction

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Species-restricted interaction between gametes at the beginning of fertilization is mediated by the extracellular coat of the egg, a matrix of cross-linked glycoprotein filaments called the zona pellucida (ZP) in mammals and the vitelline envelope in nonmammals. All egg coat subunits contain a conserved protein-protein interaction module-the "ZP domain"-that allows them to polymerize upon dissociation of a C-terminal propeptide containing an external hydrophobic patch (EHP). Recently, the first crystal structures of a ZP domain protein, sperm receptor ZP subunit zona pellucida glycoprotein 3 (ZP3), have been reported, giving a glimpse of the structural organization of the ZP at the atomic level and the molecular basis of gamete recognition in vertebrates. The ZP module is divided in two related immunoglobulin-like domains, ZP-N and ZP-C, that contain characteristic disulfide bond patterns and, in the case of ZP-C, also incorporate the EHP. This segment lies at the interface between the two domains, which are connected by a long loop carrying a conserved O-glycan important for binding to sperm in vitro. The structures explain several apparently contradictory observations by reconciling the variable disulfide bond patterns found in different homologues of ZP3 as well as the multiple ZP3 determinants alternatively involved in gamete interaction. These findings have implications for our understanding of ZP subunit biogenesis; egg coat assembly, architecture, and interaction with sperm; structural rearrangements leading to postfertilization hardening of the ZP and the block to sperm binding; and the evolutionary origin of egg coats.

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Morphological and Biochemical Changes of Isolated Chicken Egg-Envelope During Sperm Penetration: Degradation of the 97-Kilodalton Glycoprotein Is Involved in Sperm-Driven Hole Formation on the Egg-Envelope1

Cited by 30 publications

References 43 publications

Sperm proteasome degrades egg envelope glycoprotein ZP1 during fertilization of Japanese quail (Coturnix japonica)

Sperm proteasome degrades egg envelope glycoprotein ZP1 during fertilization of Japanese quail (Coturnix japonica)

A reappraisal of the factors involved in in vitro initiation of the acrosome reaction in chicken spermatozoa

A Structural View of Egg Coat Architecture and Function in Fertilization1

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