Vitellogenin C-terminal fragments participate in fertilization as egg-coat binding partners of sperm trypsin-like proteases in the ascidian Halocynthia roretzi

Akasaka, Mari; Harada, Yasuji; Sawada, Hitoshi

doi:10.1016/j.bbrc.2010.01.006

Cited by 33 publications

(41 citation statements)

References 30 publications

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“…These proteins include a multiple EGF-like domain protein, three vitellogenins, one zonadhesin-like protein, one melanotransferrin-like protein, a matrilin and an apolipoprotein B-like protein. A recent study showed that in the ascidian Halocynthia roretzi , vitellogenin is a component of the vitelline coat and participates in fertilization as the egg-coat binding partner of sperm proteases [32]. In addition, an apolipoprotein B-like protein has been demonstrated to reside both on the VC and in the egg cytoplasm of the ascidian C. intestinalis [22].…”

Section: Resultsmentioning

confidence: 99%

“…Notably, comparisons of the MS results of B. belcheri with those from C. intestinalis reveal that the number of ZP proteins identified in this study is significantly less than those observed in C. intestinalis (5 vs 11), which suggests that the number of ZP protein genes in the basal chordate species might be fewer than those of the urochordates. In addition to the ZP proteins, there are some non-ZP proteins that might also be constituents of the egg coat, for example, vitellogenin and apolipoprotein B-like protein, which are also the known components of egg coats in urochordates [22,32]. Whereas mammals use ZP proteins as the sole components to compose the zona pellucida matrix that surrounds the egg, the lower chordates appear more variable in selecting the egg coat composition.…”

Section: Discussionmentioning

confidence: 99%

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Proteomic characterization and evolutionary analyses of zona pellucida domain-containing proteins in the egg coat of the cephalochordate, Branchiostoma belcheri

Cao

et al. 2012

BMC Evol Biol

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BackgroundZona pellucida domain-containing proteins (ZP proteins) have been identified as the principle constituents of the egg coat (EC) of diverse metazoan taxa, including jawed vertebrates, urochordates and molluscs that span hundreds of millions of years of evolutionary divergence. Although ZP proteins generally contain the zona pellucida (ZP) structural modules to fulfill sperm recognition and EC polymerization functions during fertilization, the primary sequences of the ZP proteins from the above-mentioned animal classes are drastically different, which makes it difficult to assess the evolutionary relationships of ZP proteins. To understand the origin of vertebrate ZP proteins, we characterized the egg coat components of Branchiostoma belcheri, an invertebrate species that belongs to the chordate subphylum Cephalochordata.ResultsFive ZP proteins (BbZP1-5) were identified by mass spectrometry analyses using the egg coat extracts from both unfertilized and fertilized eggs. In addition to the C-terminal ZP module in each of the BbZPs, the majority contain a low-density lipoprotein receptor domain and a von Willebrand factor type A (vWFA) domain, but none possess an EGF-like domain that is frequently observed in the ZP proteins of urochordates. Fluorescence in situ hybridization and immuno-histochemical analyses of B. belcheri ovaries showed that the five BbZPs are synthesized predominantly in developing eggs and deposited around the extracellular space of the egg, which indicates that they are bona fide egg coat ZP proteins. BbZP1, BbZP3 and BbZP4 are significantly more abundant than BbZP2 and BbZP5 in terms of gene expression levels and the amount of mature proteins present on the egg coats. The major ZP proteins showed high polymorphism because multiple variants are present with different molecular weights. Sequence comparison and phylogenetic analysis between the ZP proteins from cephalochordates, urochordates and vertebrates showed that BbZP1-5 form a monophyletic group and share no significant sequence similarities with the ZP proteins of urochordates and the ZP3 subtype of jawed vertebrates. By contrast, small regions of homology were identifiable between the BbZP and ZP proteins of the non-jawed vertebrate, the sea lamprey Petromyzon marinus. The lamprey ZP proteins were highly similar to the ZP1 and ZP2 subtypes of the jawed vertebrates, which suggests that the ZP proteins of basal chordates most likely shared a recent common ancestor with vertebrate ZP1/2 subtypes and lamprey ZP proteins.ConclusionsThe results document the spectra of zona pellucida domain-containing proteins of the egg coat of basal chordates. Particularly, the study provides solid evidence for an invertebrate origin of vertebrate ZP proteins and indicates that there are diverse domain architectures in ZP proteins of various metazoan groups.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Proteomic characterization and evolutionary analyses of zona pellucida domain-containing proteins in the egg coat of the cephalochordate, Branchiostoma belcheri

Cao

et al. 2012

BMC Evol Biol

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Section: Lysin In H Roretzimentioning

confidence: 99%

“…Two VC proteins (25-and 30-kDa VC proteins) were identifi ed as binding proteins to these proteases (Akasaka et al 2010 ). By cDNA sequencing, it was revealed that the 25-and 30-kDa proteins correspond to the C-terminal region of high molecular mass vitellogenin, which belongs to a family of lipid transfer proteins (Akasaka et al 2010(Akasaka et al , 2013. We propose that sperm binds to the C-terminal fragments of vitellogenin located on the VC, the binding being mediated by the sperm-side HrProacrosin CUB domain and HrSpermosin Pro-rich region, and then sperm proteases degrade these VC proteins or the precursor regions, enabling sperm to detach from and penetrate the VC.…”

Section: Lysin In H Roretzimentioning

confidence: 99%

Allorecognition and Lysin Systems During Ascidian Fertilization

Sawada

Yamamoto

Otsuka

et al. 2014

Sexual Reproduction in Animals and Plants

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Ascidians (primitive chordates) are hermaphroditic animals that release sperm and eggs almost simultaneously, but several species, including Halocynthia roretzi and Ciona intestinalis , show strict self-sterility. In H. roretzi , a 70-kDa vitelline coat (VC) protein consisting of 12 EGF-like repeats (HrVC70) appears to be a promising candidate for the self/non-self-recognition (or allorecognition) system during gamete interaction. After sperm recognizes the VC as non-self, the sperm extracellular ubiquitin-proteasome system appears to degrade HrVC70, allowing sperm to penetrate through the VC with the aid of sperm trypsin-like proteases.In C. intestinalis , egg-side highly polymorphic fi brinogen-like ligands on the VC (v-Themis-A and v-Themis-B) and cognate sperm-side hypervariable regioncontaining polysystin-1-like receptors (s-Themis-A and s-Themis-B) seem to be responsible for allorecognition in gamete interaction. Recently, we noticed that a novel pair of v-Themis-B2 and s-Themis-B2 and an acid-extractable VC protein called Ci-v-Themis-like may take part in gamete interaction or allorecognition. When sperm recognizes the VC as self, the sperm undergoes a drastic Ca 2+ infl ux, which is one of the major intracellular self-recognition responses within sperm, resulting in sperm detachment from the VC or in sperm becoming quiescent. These allorecognition systems and self-recognition responses within sperm are very similar to the self-incompatibility system in fl owering plants.

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“…Recently, we carried out 5′-and 3′-rapid amplifi cation of cDNA ends (5′-RACE)-polymerase chain reaction (PCR) on the basis of these N-terminal sequences, showing that some of these VC proteins are identical to the C-terminal coding region (CT) and von Willebrand factor type D (vWF-D) domain, which is located at the C-terminal region of vitellogenin (Akasaka et al 2010 ). The binding ability between the vitellogenin C-terminus and CUB domain of HrProacrosin was confi rmed by an in vitro pulldown assay (Fig.…”

Section: Vitellogenin Is a Binding Partner Of Sperm Proteasesmentioning

confidence: 99%

Novel Isoform of Vitellogenin Expressed in Eggs Is a Binding Partner of the Sperm Proteases, HrProacrosin and HrSpermosin, in the Ascidian Halocynthia roretzi

Akasaka

Kato

Kitajima

et al. 2014

Sexual Reproduction in Animals and Plants

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Vitellogenin is a precursor of yolk protein that is necessary for embryonic development. Vitellogenin is a large multidomain protein consisting of a signal peptide, a heavy-chain lipovitellin, a phosvitin, a light-chain lipovitellin, a von Willebrand factor type D domain (vWF-D), and a C-terminal coding region (CT), which are processed to respective domains after uptake into oocytes. It is currently believed that only lipovitellin and phosvitin domains are necessary for nutrient supply to oocytes. Thus, molecular species of vitellogenin lacking these domains are not known. We recently found that two novel isoforms of vitellogenin, both of which possess vWF-D and CT domains but not a lipovitellin or phosvitin domain, are expressed in the gonad of the ascidian Halocynthia roretzi . In situ hybridization revealed that mRNAs of these proteins are specifi cally expressed in oocytes and test cells, accessory cells in the perivitelline space of ascidian eggs. Immunocytochemistry showed that these proteins are localized around the surface of test cells in immature oocytes. Immunoelectron microscopy revealed that vitellogenin associates with vesicles located beneath the vitelline coat (VC) before fertilization but that it dissociates from the VC after fertilization. These results, together with our previous

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Vitellogenin C-terminal fragments participate in fertilization as egg-coat binding partners of sperm trypsin-like proteases in the ascidian Halocynthia roretzi

Cited by 33 publications

References 30 publications

Proteomic characterization and evolutionary analyses of zona pellucida domain-containing proteins in the egg coat of the cephalochordate, Branchiostoma belcheri

Proteomic characterization and evolutionary analyses of zona pellucida domain-containing proteins in the egg coat of the cephalochordate, Branchiostoma belcheri

Allorecognition and Lysin Systems During Ascidian Fertilization

Novel Isoform of Vitellogenin Expressed in Eggs Is a Binding Partner of the Sperm Proteases, HrProacrosin and HrSpermosin, in the Ascidian Halocynthia roretzi

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