Allorecognition mechanisms during ascidian fertilization

Harada, Yasuji; Sawada, Hitoshi

doi:10.1387/ijdb.072544yh

Cited by 47 publications

(30 citation statements)

References 55 publications

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“…In Brassicaceae, it is controlled by S-locus, which has multiple alleles, and each allele encodes male and female recognition molecules, which enables an allele-specific interaction (28). The self/nonself discrimination between the male and female recognition molecules takes place on the basis of recognition (and then rejection) of "self" in these species (1,28). We recently revealed the molecular mechanism of the self-incompatibility system in the ascidian C. intestinalis (29).…”

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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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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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“…However, we do not know whether the CiLgals are components of the VC involved in the allorecognition mechanism responsible of the FC/VC-mediated self-incompatibility barrier established by the FCs against autologous sperms during the follicle maturation [50,51,72]. Our findings on the labeling of the VC layer may merely depend on the passive capture of galectins released from the FCs, as also shown by the labeling with CinPO2 riboprobe and antibody.…”

Section: Discussionmentioning

confidence: 70%

In the ovary of Ciona intestinalis (Type A), immune-related galectin and phenoloxidase genes are differentially expressed by the follicle accessory cells

Parrinello¹,

Sanfratello²,

Parisi³

et al. 2018

Fish & Shellfish Immunology

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A B S T R A C TRiboprobes (in situ hybridization) and antibodies (immunohistochemistry), previously used to show the upregulation of Ciona intestinalis (Type A) galectins (CiLgals-a, CiLgals-b) and phenoloxidase (CinPO2) immunerelated genes, were tested on histological sections of the ovary. The ovarian follicles are composed of oocytes encased by follicular cells (FCs) and test cells (TCs). Results show the transcription upregulation of both CiLgals and CinPO2 genes in the vitellogenic FCs, conversely distinct cytolocalization of the proteins are shown. At vitellogenic stage, the CiLgals are localized in the FCs, in the oocyte cytoplasm, and close to the germinal vesicle (GV), whereas the CinPO2 was never identified in the FCs. In a presumptive advanced phase and at the postvitellogenic stage the TCs appear to be labelled by the CinPO2 riboprobe, and the protein identified by the antibody suggesting an mRNA transcytosis process from FCs. At post-vitellogenic stage the CiLgals mainly enrich the GV nucleoplasm, whereas the CinPO2 is contained in TCs and in the ooplasm but never found in the GV. This finding sheds new light on a former paper in which TCs were reported to be the only CinPO2-producing cells in the ovarian follicle. Finally, CiLgals and CinPO2 genes transcription and proteins production seem to be associated with accessory cells during their differentiation from vitellogenic to post-vitellogenic stage. The present findings promote further research on the early upregulation of immune-related genes, and the potential multifunctional role of the produced proteins. In addition further insight on the accessory cells involvement in ascidian oogenesis are reported.

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“…In Brassicaceae, pollen SP11/SCP and stigma S-locus receptor kinase (SRK) genes are tightly linked in the same chromosome, making respective haplotypes; even in this family, an increase in intracellular Ca 2+ in papilla cells in the stigma appears to play a key role in the SI system (1,25). Taking into account these data, the SI system or the self/nonself-recognition system may be much more common between animals and plants than we have thought previously, even in the intracellular signaling pathway (26).…”

Section: Resultsmentioning

confidence: 82%

Self-incompatibility response induced by calcium increase in sperm of the ascidian Ciona intestinalis

Saitô

Shiba

Inaba

et al. 2012

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

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Many hermaphroditic organisms possess a self-incompatibility system to avoid self-fertilization. Recently, we identified the genes responsible for self-sterility in a hermaphroditic primitive chordate (ascidian), Ciona intestinalis: sperm-side polycystin 1-like receptors s-Themis-A/B and egg-side fibrinogen-like ligands on the vitelline coat (VC) v-Themis-A/B. Here, we investigated the sperm behavior and intracellular Ca 2+ concentration ([Ca 2+ ] i ) in response to self/ nonself-recognition. We found that sperm motility markedly decreased within 5 min after attachment to the VC of self-eggs but not after attachment to the VC of nonself-eggs and that the apparent decrease in sperm motility was suppressed in low Ca 2+ seawater. High-speed video analysis revealed that sperm detached from the self-VC or stopped motility within 5 min after binding to the self-VC. Because s-Themis-B contains a cation channel domain in its C terminus, we monitored sperm [Ca 2+ ] i by real-time [Ca 2+ ] i imaging using Fluo-8H-AM (AAT Bioquest, Inc.). Interestingly, we found that sperm [Ca 2+ ] i rapidly and dramatically increased and was maintained at a high level in the head and flagellar regions when sperm interacted with the self-VC but not when the sperm interacted with the nonself-VC. The increase in [Ca 2+ ] i was also suppressed by low-Ca 2+ seawater. These results indicate that the sperm self-recognition signal triggers [Ca 2+ ] i increase and/or Ca 2+ influx, which elicits a self-incompatibility response to reject selffertilization in C. intestinalis. Sexual reproduction is an essential process to elicit genetic diversity in the next generation. Therefore, many hermaphrodite species have acquired a self-incompatibility (SI) system that prevents inbreeding. In flowering plants, SI systems depend on S proteins, which are encoded in an SI specificity-determining locus (1). The invertebrate chordate Ciona intestinalis is a hermaphroditic animal that releases sperm and eggs nearly simultaneously and exhibits strict self-sterility. These features were reported by Tomas Hunt Morgan about a century ago (2). Rosati and De Santis (3) and Kawamura et al. (4) later clarified that a self/nonself-discrimination site resides on the vitelline coat (VC), an acellular matrix surrounding the egg, and that the VC shows higher affinity to allogeneic (nonself) sperm than to autologous (self) sperm (3, 4). Recently, we revealed that the SI system in C. intestinalis is controlled by two multiallelic independent loci, loci A and B. Each of the loci contains a pair of SI candidate genes, egg-side v-Themis-A/B and sperm-side sThemis-A/B. All four proteins show high polymorphisms among individuals. Comprehensive proteome analysis of the isolated VC revealed that both v-Themis-A and v-Themis-B exist in the VC (5, 6). Interestingly, v-Themis-A/B genes reside in the cDNA strand of the first intron of s-Themis-A/B genes, respectively, suggesting that these egg-and sperm-side SI factors would be hardly segregated by homologous recombinatio...

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Allorecognition mechanisms during ascidian fertilization

Cited by 47 publications

References 55 publications

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

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

In the ovary of Ciona intestinalis (Type A), immune-related galectin and phenoloxidase genes are differentially expressed by the follicle accessory cells

Self-incompatibility response induced by calcium increase in sperm of the ascidian Ciona intestinalis

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