Self-sterility of eggs induced by exogenous and endogenous protease in the solitary ascidian,Halocynthia roretzi

Fuke, Masako T.; Numakunai, Takaharu

doi:10.1002/(sici)1098-2795(199901)52:1<99::aid-mrd12>3.0.co;2-n

Cited by 16 publications

(20 citation statements)

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“…He also found that the eggs become self-fertile by treatment with mildly acidic seawater or proteases (1)(2)(3). Similar results were obtained in the solitary ascidian H. roretzi: treatment of the eggs with mildly acidic seawater (pH 2-3) or proteases is sufficient to allow self-fertilization (12,13). In addition, self-fertile immature oocytes become self-sterile during spontaneous oocyte maturation in this species (12,13).…”

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confidence: 66%

“…It is reported that self-sterility in the eggs of H. roretzi is acquired during oocyte maturation and that the self-sterile mature oocytes become self-fertile by acid treatment (12,13). From these results, it is inferred that a candidate allorecognition molecule may be attached to the vitelline coat during oocyte maturation and that this molecule may be easily detached from the vitelline coat by acid treatment.…”

Section: Resultsmentioning

confidence: 98%

“…Furthermore, it is reported that the acquisition of self-sterility during oocyte maturation is inhibited by proteinaceous and microbial trypsin inhibitors (13). These results led us to propose that a certain egg-or follicle-cell-derived protein with allorecognition activity, which is produced by means of limited proteolysis by a trypsin-like protease, may be attached to the vitelline coat during the oocyte maturation and that this protein may be removed from the vitelline coat by mildly acidic conditions.…”

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confidence: 99%

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Self/nonself recognition in ascidian fertilization: Vitelline coat protein HrVC70 is a candidate allorecognition molecule

Sawada

Tanaka

et al. 2004

Proc. Natl. Acad. Sci. U.S.A.

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Ascidians are hermaphrodites releasing sperm and eggs simultaneously, but many species are self-sterile because of a self͞nonself-recognition system in sperm-egg interaction. Here, we show that a 70-kDa vitelline coat protein, HrVC70, consisting of 12 epidermal growth factor-like repeats, plays a key role in self͞nonself recognition during ascidian fertilization. We discovered that the amount of HrVC70 of the self-sterile mature oocytes is markedly higher than that of the self-fertile immature oocytes and that the selfsterile mature oocytes become self-fertile by acid treatment, which is able to release the HrVC70 from isolated vitelline coats. In addition, fertilization is strongly inhibited by the pretreatment of sperm with HrVC70 from a different individual, but not from the same individual, and the number of nonself sperm bound to HrVC70-agarose was significantly higher than that of self-sperm. A sequence analysis of HrVC70 disclosed that several amino acid residues in a restricted region are substituted at an individual level, with no identical sequences among the 10 individuals tested. Furthermore, genomic DNA analysis revealed that the epidermal growth factor-like domains correspond to the exons, and each intron is highly conserved among even-and odd-numbered introns, suggesting that multiple gene duplications or amplification of this region might have taken place during evolution. It was also found that diversity in cDNA sequences is derived from genomic DNA polymorphism probably elicited by crossing over and specific nucleotide substitutions. These results indicate that HrVC70 is a candidate allogeneic recognition molecule in the gamete interaction of the ascidian Halocynthia roretzi.

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confidence: 66%

Section: Resultsmentioning

confidence: 98%

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confidence: 99%

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Self/nonself recognition in ascidian fertilization: Vitelline coat protein HrVC70 is a candidate allorecognition molecule

Sawada

Tanaka

et al. 2004

Proc. Natl. Acad. Sci. U.S.A.

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“…data). In the pyurid Halocynthia , GVBD occurs shortly after ovulation and is accompanied by expansion of the perivitelline space and release of the test cells (Sakairi & Shirai 1991; Fuke & Numakunai 1996; Fuke & Numakunai 1999). Sakairi & Shirai (1991) have suggested that a protease released by the follicle cells may be the trigger of GVBD in Halocynthia .…”

Section: Introductionmentioning

confidence: 99%

Signaling pathways in ascidian oocyte maturation: Effects of various inhibitors and activators on germinal vesicle breakdown

Lambert

2005

Dev Growth Differ

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The Ascidiacea, the invertebrate chordates, includes three orders; the Stolidobranchia is the most complex. Until the present study, the onset of oocyte maturation (germinal vesicle breakdown) had been investigated in only a single pyurid (Halocynthia roretzi), in which germinal vesicle breakdown (GVBD) begins when the oocyte contacts seawater (SW); nothing was known about internal events. This study strongly suggests the importance of protein phosphorylation in this process. Herdmania pallida (Pyuridae) functions like H. roretzi; GVBD occurs in SW. Oocytes of Cnemidocarpa irene (Styelidae) do not spontaneously undergo GVBD in SW but must be activated. Herdmania oocytes are inhibited from GVBD by pH 4 SW and subsequently activated by mastoparan (G-protein activator), A23187 (Ca 2+ ionophore) or dimethylbenzanthracene (tyrosine kinase activator). This requires maturation promoting factor (MPF) activity; cyclin-dependent kinase inhibitors roscovitine and olomoucine are inhibitory. It also entails dephosphorylation as demonstrated by the ability of the phosphatase inhibitor vitamin K3 to inhibit GVBD. GVBD is also inhibited by the tyrosine kinase inhibitors tyrphostin A23 and genistein, and LY-294002, a phosphatidylinositol-3-kinase inhibitor previously shown to inhibit starfish GVBD. LY-294002 inhibits strongly when activation is by mastoparan or ionophore but not when activated by dimethylbenzanthracene (DMBA). The DMBA is hypothesized to phosphorylate a phosphatase directly or indirectly causing secondary activation, bypassing inhibition.

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“…As in C. intestinalis, mature oocytes but not immature oocytes are self-sterile in H. roretzi, and the self-sterility is lost by treatment with acidic seawater (9). Furthermore, the acquisition of self-sterility during oocyte maturation was blocked by trypsin inhibitors, whereas exogenously added trypsin stimulates the acquisition of self-sterility (10,11). These results led us to propose that a putative allorecognition protein might be expressed in immature oocytes as a precursor and that the active form might be generated by a trypsin-like protease, resulting in its attachment to the VC during oocyte maturation.…”

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confidence: 99%

Ascidian Sperm Glycosylphosphatidylinositol-anchored CRISP-like Protein as a Binding Partner for an Allorecognizable Sperm Receptor on the Vitelline Coat

Urayama

Harada

Nakagawa

et al. 2008

Journal of Biological Chemistry

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Although ascidians are hermaphroditic, many species including Halocynthia roretzi are self-sterile. We previously reported that a vitelline coat polymorphic protein HrVC70, consisting of 12 EGF (epidermal growth factor)-like repeats, is a candidate allorecognition protein in H. roretzi, because the isolated HrVC70 shows higher affinity to nonself-sperm than to self-sperm. Here, we show that a sperm 35-kDa glycosylphosphatidylinositol-anchored CRISP (cysteine-rich secretory protein)-like protein HrUrabin in a low density detergentinsoluble membrane fraction is a physiological binding partner for HrVC70. We found that HrVC70 specifically interacts with HrUrabin, which had been separated by SDS-PAGE and transferred onto a nitrocellulose membrane. HrUrabin has an N-linked sugar chain, essential for binding to HrVC70. HrUrabin mRNA is expressed in the testis but not in the ovary, and the protein appears to be localized on the surface of sperm head and tail. Anti-HrUrabin antibody, which neutralizes the interaction between HrUrabin and HrVC70, potently inhibited fertilization and allorecognizable sperm-binding to HrVC70-agarose. However, no significant difference in the binding ability of HrUrabin to HrVC70 was observed in autologous and allogeneic combinations by Far Western analyses. These results indicate that sperm-egg binding in H. roretzi is mediated by the molecular interaction between HrUrabin on the sperm surface and HrVC70 on the vitelline coat, but that HrUrabin per se is unlikely to be a direct allorecognition protein.Ascidians, the invertebrate chordates, are hermaphroditic animals releasing gametes nearly simultaneously during the spawning season. Most ascidians show self-sterility or preference for "non-autologous" (allogeneic) fertilization (1, 2), which appears to be beneficial for the achievement of genetic diversity in the next generation. However, the mechanism of self-sterility during ascidian fertilization is a long-standing enigma. In the early part of the 20th century, Morgan (3-6) studied this problem using the solitary ascidian Ciona intestinalis, and found that a barrier against self-fertilization is abolished by the treatment of eggs with weak acid (citrus juice) or protease (pancreatic extract) (3). Because the vitelline coat (VC) 3 -free naked eggs are self-fertile, he proposed that a self/nonself-recognition molecule must reside on the VC or test cells. Later, it was found that only nonself-sperm tightly and specifically bound to the VC of glycerinated eggs in C. intestinalis (7). From these results, it is currently believed that a certain allorecognition molecule responsible for self-sterility must reside on the VC.We have been studying the mechanism of self-sterility using another solitary ascidian, Halocynthia roretzi, because a large quantity of readily fertilizable gametes can be easily obtained from this species, which is aqua-cultured in Japan for human consumption (8). Although H. roretzi exhibits much more strict self-sterility than C. intestinalis, the mode of self-sterility in...

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Self-sterility of eggs induced by exogenous and endogenous protease in the solitary ascidian,Halocynthia roretzi

Cited by 16 publications

References 14 publications

Self/nonself recognition in ascidian fertilization: Vitelline coat protein HrVC70 is a candidate allorecognition molecule

Self/nonself recognition in ascidian fertilization: Vitelline coat protein HrVC70 is a candidate allorecognition molecule

Signaling pathways in ascidian oocyte maturation: Effects of various inhibitors and activators on germinal vesicle breakdown

Ascidian Sperm Glycosylphosphatidylinositol-anchored CRISP-like Protein as a Binding Partner for an Allorecognizable Sperm Receptor on the Vitelline Coat

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