Sturgeon hatching enzyme and the mechanism of egg envelope digestion: Insight into changes in the mechanism of egg envelope digestion during the evolution of ray‐finned fish

Abstract

We investigated the evolution of the hatching enzyme gene using bester sturgeon (hybrid of Acipencer ruthenus and Huso huso), a basal member of ray-finned fishes. We purified the bester hatching enzyme from hatching liquid, yielding a single band on SDS-PAGE, then isolated its cDNA from embryos by PCR. The sturgeon hatching enzyme consists of an astacin family protease domain and a CUB domain. The CUB domains are present in frog and bird hatching enzymes, but not in teleostei, suggesting that the domain structure of sturgeon hatching enzyme is the tetrapod type. The purified hatching enzyme swelled the egg envelope, and selectively cleaved one of five egg envelope proteins, ZPAX. Xenopus hatching enzyme preferentially digests ZPAX, thus, the egg envelope digestion process is conserved between amphibians and basal ray-finned fish. Teleostei hatching enzymes cleave the repeat sequences at the N-terminal region of ZPB and ZPC, suggesting that the targets of the teleostei hatching enzymes differ from those of amphibians and sturgeons. Such repeat sequences were not found in the N-terminal region of ZPB and ZPC of amphibians and sturgeons. Our results suggest that the change in substrates of the hatching enzymes was accompanied by the mutation of the amino acid sequence of N-terminal regions of ZPB and ZPC. We conclude that the changes in the mechanism of egg envelope digestion, including the change in the domain structure of the hatching enzymes and the switch in substrate, occurred during the evolution of teleostei, likely triggered by the teleost-specific third whole genome duplication. J. Exp. Zool. (Mol. Dev. Evol.) 324B: 720-732, 2015. © 2015 Wiley Periodicals, Inc.

Soya isoflavones, genistein and daidzein, induce differential transcriptional modulation in the ovary and testis of zebrafish Danio rerio

“…AcHEs), which are considered to be ovastacin homologs, predominated both in the ovary and testis, and these isoforms showed no expression biased by sex, suggesting a conserved role in other areas unrelated to sex. In addition, some of these metalloproteases play the role of proteolytic agents by digesting the egg-envelope to facilitate penetration of spermatozoa and by promoting interaction between both gametes; other metalloproteases which are within the ovary, such as the alveolin peptidase, do not break the egg-envelope, but are instead involved in its hardening upon fertilisation (Yamagami 1996, Sano et al 2008, Kawaguchi et al 2012, Shibata et al 2012, Nagasawa et al 2015. Interestingly, in zebra fish, HE1 expression levels were up-regulated by exposure to genistein (at 10 mg l −1 ) in both male and female gonads, while daidzein only increased HE1 expression levels in skeletal musculature.…”

“…choriolysins) digest the egg's protein envelope to facilitate hatching, alveoline, which is a metalloprotease released from cortical alveoli of early vitellogenic oocytes, induces reassembly of choriogenins to harden the egg envelope at the time of fecundation. Some metalloproteases that are present in gametes are essential to ensure reproductive success, by facilitating the passage and penetration of sperm during fertilisation (Yamagami, 1996, Sano et al 2008, Kawaguchi et al 2012, Shibata et al 2012, Nagasawa et al 2015, Chakraborty et al 2017.…”

Genomic and phylogenetic analysis of choriolysins, and biological activity of hatching liquid in the flatfish Senegalese sole

“…While the SseLCE is widely detected in Euteleostei, the SseHE was detected in Otocephala and a reduced number of euteleosteans. Moreover, these two genes were structured in 8 exons and 7 introns in different scaffolds indicating that they were derived from the ancestral copies in basal actinopterygians [37]. Previous studies that evaluated functional characteristics of enzymes belonging to these two subclades indicated that they could have followed a neofunctionalization acquiring different cleavage activities [6].…”

Effects of incubation temperature on the embryonic viability and hatching time in Russian sturgeon (Acipenser gueldenstaedtii)

“…Hatching enzyme is a protease with a choriolytic activity which can degrade the membrane of egg to let the larvae be free. Hatching enzymes have been isolated and characterized from various teleosts (Kawaguchi et al 2010;Nagasawa et al 2016) and also from the Bester sturgeon (hybrid of Acipenser ruthenus and Huso huso) (Nagasawa et al 2015). However, in contrast to the relative richness of information on in vitro activity of hatching enzyme at different temperature ranges (Shi et al 2006;Pype et al 2015), the in vivo expression (12, 16, or 20°C).…”