Mechanism of egg envelope digestion by hatching enzymes, HCE and LCE in medaka, Oryzias latipes

Yasumasu, Shigeki; Kawaguchi, Mari; Ouchi, Satoshi; Sano, Kôkichi; Murata, Kenji; Sugiyama, Hitoshi; Akema, Tatsuo; Iuchi, Ichiro

doi:10.1093/jb/mvq086

Cited by 35 publications

(71 citation statements)

References 30 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…In this regard, it is notable that the dimensions of the chicken ZP3 dimer approximately match those of the structural repeat found in ZP filaments [5]. Moreover, a recent analysis of the molecular basis of hatching in fish [52] suggests that the dimer interface of chicken ZP3, the structure of which represents a snapshot of the protein after CFCS cleavage but before EHP dissociation ( Fig. 2A), could be maintained in the egg coat.…”

Section: Potential Polymerization Interfacesmentioning

confidence: 59%

A Structural View of Egg Coat Architecture and Function in Fertilization1

Monné¹,

Jovine²

2011

Biology of Reproduction

View full text Add to dashboard Cite

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.

show abstract

Section: Potential Polymerization Interfacesmentioning

confidence: 59%

A Structural View of Egg Coat Architecture and Function in Fertilization1

Monné¹,

Jovine²

2011

Biology of Reproduction

View full text Add to dashboard Cite

show abstract

“…The ZP domains are polymerized to each other to form long filaments by inter-molecular non-covalent interactions between the subdomains [4-6]. The N-terminal regions loop out from the filaments [3], and tie or bunch the filamentous structures [7]. In fish, the ε-(γ-glutamyl) lysine isopeptide cross-links (Glu-Lys cross-links) are formed between the filamentous structures at fertilization.…”

Section: Introductionmentioning

confidence: 99%

“…Hatching enzyme, which belongs to the astacin metalloproteinase family [8,9], is found in fish, amphibians, birds, reptiles, and mammals [7,10-13]. In teleosts, we have cloned 67 hatching enzyme genes from 27 species, and elucidated their evolutionary pathway [14,15].…”

Section: Introductionmentioning

confidence: 99%

“…The clade I enzyme named MHCE (medaka high choriolytic enzyme) cleaves the N-terminal regions of ZPB, where many of the Glu-Lys cross-links are located [20], into short peptide fragments, thereby swelling the egg envelope in a manner similar to the Japanese eel single enzyme [7]. The clade II enzyme named MLCE (medaka low choriolytic enzyme) cleaves two specific sites on the swollen egg envelope, termed the mid-ZPd and N-ZPd sites.…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Neofunctionalization of a duplicate hatching enzyme gene during the evolution of teleost fishes

et al. 2014

View full text Add to dashboard Cite

BackgroundDuplication and subsequent neofunctionalization of the teleostean hatching enzyme gene occurred in the common ancestor of Euteleostei and Otocephala, producing two genes belonging to different phylogenetic clades (clade I and II). In euteleosts, the clade I enzyme inherited the activity of the ancestral enzyme of swelling the egg envelope by cleavage of the N-terminal region of egg envelope proteins. The clade II enzyme gained two specific cleavage sites, N-ZPd and mid-ZPd but lost the ancestral activity. Thus, euteleostean clade II enzymes assumed a new function; solubilization of the egg envelope by the cooperative action with clade I enzyme. However, in Otocephala, the clade II gene was lost during evolution. Consequently, in a late group of Otocephala, only the clade I enzyme is present to swell the egg envelope. We evaluated the egg envelope digestion properties of clade I and II enzymes in Gonorynchiformes, an early diverging group of Otocephala, using milkfish, and compared their digestion with those of other fishes. Finally, we propose a hypothesis of the neofunctionalization process.ResultsThe milkfish clade II enzyme cleaved N-ZPd but not mid-ZPd, and did not cause solubilization of the egg envelope. We conclude that neofunctionalization is incomplete in the otocephalan clade II enzymes. Comparison of clade I and clade II enzyme characteristics implies that the specificity of the clade II enzymes gradually changed during evolution after the duplication event, and that a change in substrate was required for the addition of the mid-ZPd site and loss of activity at the N-terminal region.ConclusionsWe infer the process of neofunctionalization of the clade II enzyme after duplication of the gene. The ancestral clade II gene gained N-ZPd cleavage activity in the common ancestral lineage of the Euteleostei and Otocephala. Subsequently, acquisition of cleavage activity at the mid-ZPd site and loss of cleavage activity in the N-terminal region occurred during the evolution of Euteleostei, but not of Otocephala. The clade II enzyme provides an example of the development of a neofunctional gene for which the substrate, the egg envelope protein, has adapted to a gradual change in the specificity of the corresponding enzyme.

show abstract

“…The mechanisms of the biochemical processes occurring during hatching are well described (Yamagami 1988(Yamagami , 1996(Yamagami , 1997Yasumasu et al 1988Yasumasu et al , 2010Kawaguchi et al 2008Kawaguchi et al , 2009Kawaguchi et al , 2010. Far less information is available regarding the distribution of the hatching gland cells and its relation with the location of egg envelope digestion, as well as embryonic movements prior to hatching, and strategies for larvae to escape from egg envelopes.…”

Section: Introductionmentioning

confidence: 99%

Fish hatching strategies: a review

Korwin-Kossakowski

2011

Rev Fish Biol Fisheries

View full text Add to dashboard Cite

The paper presents differences in the distribution of hatching gland cells, and the location of egg envelope digestion, the significance of hatching movements, and the ways larvae escape from egg envelopes. A review of the literature on the hatching orientation of 34 fish species is compared. No correlation was seen between hatching orientation and egg diameter or newly hatched larva length, nor newly hatched larvae length ratio to egg diameter. Photographs of twelve freshwater species present the moment of hatching either head first or tail first. Some differences were shown in swelling between eggs incubated in commercial hatchery and developed in natural conditions, as well as possible effect of these differences on hatching.

show abstract

Mechanism of egg envelope digestion by hatching enzymes, HCE and LCE in medaka, Oryzias latipes

Cited by 35 publications

References 30 publications

A Structural View of Egg Coat Architecture and Function in Fertilization1

A Structural View of Egg Coat Architecture and Function in Fertilization1

Neofunctionalization of a duplicate hatching enzyme gene during the evolution of teleost fishes

Fish hatching strategies: a review

Contact Info

Product

Resources

About