Temporal and Spatial Patterns of Gene Expression for the Hatching Enzyme in the Teleost Embryo, Oryzias latipes

Inohaya, Keiji; Yasumasu, Shigeki; Ishimaru, Mika; Ohyama, Ayako; Iuchi, Ichiro; Yamagami, Kenjiro

doi:10.1006/dbio.1995.1289

Cited by 90 publications

(79 citation statements)

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“…Recent studies have characterized multiple tissue-specific astacin proteins in a variety of organisms from crayfish to mammals. The astacin gene family includes digestive enzymes (18), hatching enzymes (19,20), bone morphogenic proteins (21), meprins (22), and the recently discovered proteins cimp1 (23) and nephrosin (24), which are expressed in the gills and kidney of bony fishes. We obtained the complete coding sequence of patristacin from the brood pouches of pregnant male S. scovelli, Syngnathus rostellatus, and Syngnathus acus, as well as representative sequences from the kidney and liver of several syngnathids and other fishes ( Table 1, which is published as supporting information on the PNAS web site).…”

Section: Resultsmentioning

confidence: 99%

“…3). For example, choriolysin proteins have two isoforms (''high'' and ''low'') that originated through gene duplication and now function together to break down the egg chorion before hatching (19,20). Likewise, our results suggest that nephrosin, a relatively new member of the astacin subfamily, has two forms (i.e., gill/kidney and liver) that were each coopted for tissue-specific expression after gene duplication (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…Another intriguing possibility is that patristacin may have evolved a function similar to the related hatching enzymes. In oviparous species, choriolytic enzymes are produced by the embryo to facilitate hatching (19,20). One interesting feature of male pregnancy is that the egg chorion breaks down relatively early in gestation, as paternal tissue proliferates and surrounds the embryos.…”

Section: Resultsmentioning

confidence: 99%

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Gene cooption without duplication during the evolution of a male-pregnancy gene in pipefish

Harlin-Cognato

Hoffman

Jones

2006

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

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Comparative studies of developmental processes suggest that novel traits usually evolve through the cooption of preexisting genes and proteins, mainly via gene duplication and functional specialization of paralogs. However, an alternative hypothesis is that novel protein function can evolve without gene duplication, through changes in the spatiotemporal patterns of gene expression (e.g., via cis-regulatory elements), or functional modifications (e.g., addition of functional domains) of the proteins they encode, or both. Here we present an astacin metalloprotease, dubbed patristacin, which has been coopted without duplication, via alteration in the expression of a preexisting gene from the kidney and liver of bony fishes, for a novel role in the brood pouch of pregnant male pipefish. We examined the molecular evolution of patristacin and found conservation of astacin-specific motifs but also several positively selected amino acids that may represent functional modifications for male pregnancy. Overall, our results pinpoint a clear case in which gene cooption occurred without gene duplication during the genesis of an evolutionarily significant novel structure, the male brood pouch. These findings contribute to a growing understanding of morphological innovation, a critically important but poorly understood process in evolutionary biology.novel trait evolution ͉ patristacin ͉ Syngnathidae E volutionary innovation has been defined as ''the origin of a novel body part which may serve a novel function or specialize in a function that was already performed in the ancestral lineage but without a dedicated organ' ' (ref. 1, p. 581). In seahorses and pipefishes (family Syngnathidae) males carry their embryos on their ventral surface, either exposed to the environment or enclosed in a fleshy brood pouch (Fig. 1). The brood pouch is a clear example of an evolutionary innovation: syngnathids are the only lineage to have evolved a morphological structure that allows males to become pregnant. In many species of syngnathid fishes, the brood pouch is a complex organ composed of highly vascularized epithelial tissue that forms a honeycomb matrix encapsulating individual eggs during gestation ( Fig. 1) (2). This placenta-like tissue apparently supplies nutrients to developing embryos (3) in a manner analogous to the placenta of female mammals. The pouch is lined with cells rich in mitochondria (CRMs) (Fig. 1) (2, 4) that transfer ions between the brood pouch fluid and the male bloodstream, maintaining an osmotically neutral environment during the early stages of gestation (4-6). A phylogeny of the Syngnathidae suggests two independent origins of the brood pouch based on its location on either the abdomen (Gastrophori) or the tail (Urophori) of the male (7), and within these two lineages there is considerable variation in the degree to which the pouch encloses developing embryos, the complexity of the ''pseudoplacenta,'' and the structure of brood pouch folds (7).Clearly, the evolution of a structure as complex as a brood pouch req...

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

See 1 more Smart Citation

Gene cooption without duplication during the evolution of a male-pregnancy gene in pipefish

Harlin-Cognato

Hoffman

Jones

2006

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

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“…Both genes are expressed at early developmental stages, and the gastrula stage marks their onset of expression. The st6gal2-r gene is primarily detected in hatching gland cells, which produce metalloprotease choriolytic enzymes HCE and LCE digesting egg envelope (chorion) at the time of embryo hatching (87). This suggests a role in the process of hatching gland differentiation (same time as differentiation of notochord and paraxial mesoderm), in mucous cells and proctodeum.…”

Section: Discussionmentioning

confidence: 99%

Molecular Phylogeny and Functional Genomics of β-Galactoside α2,6-Sialyltransferases That Explain Ubiquitous Expression of st6gal1 Gene in Amniotes

Petit

Mir

Petit

et al. 2010

Journal of Biological Chemistry

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Sialyltransferases are key enzymes in the biosynthesis of sialoglycoconjugates that catalyze the transfer of sialic residue from its activated form to an oligosaccharidic acceptor. ␤-Galactoside ␣2,6-sialyltransferases ST6Gal I and ST6Gal II are the two unique members of the ST6Gal family described in higher vertebrates. The availability of genome sequences enabled the identification of more distantly related invertebrates' st6gal gene sequences and allowed us to propose a scenario of their evolution. Using a phylogenomic approach, we present further evidence of an accelerated evolution of the st6gal1 genes both in their genomic regulatory sequences and in their coding sequence in reptiles, birds, and mammals known as amniotes, whereas st6gal2 genes conserve an ancestral profile of expression throughout vertebrate evolution.

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“…Whole-Mount RNA In Situ Hybridization WISH was performed with DIG-labeled antisense RNA probes following the procedure previously described (Inohaya et al, 1995(Inohaya et al, , 1999. cDNAs as the templates for antisense RNA probes, c-myb, lmo2, gata1,a0-globin, l-plastin, and mpo1 were described previously (Kinoshita et al, 2009;Moriyama et al, 2010), and TFDP1 was cloned by PCR primers as follows: 5'-ACGGCTAGCTGAA AGGGAGTGA À3' (F) and 5'-GGGGGGTTAGGTTAGTCTTCGTCA À3' (R).…”

Section: Cell Size Measurementmentioning

confidence: 99%

Proliferation following tetraploidization regulates the size and number of erythrocytes in the blood flow during medaka development, as revealed by the abnormal karyotype of erythrocytes in the medaka TFDP1 mutant

Taimatsu

Takubo

Maruyama³

et al. 2015

Developmental Dynamics

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Background: For the delivery of oxygen, the correct size/number of erythrocytes is required for proper blood flow. Results: By combined analyses of wild-type (WT) medaka and the kyoho (kyo) mutant, we found proliferation-mediated adaptation for size/number of erythrocytes in the blood flow during medaka development. Before the start of heart beating in the WT medaka, the karyotype of erythrocytes was 2N-4N. After the start of blood flow, the karyotype changed to 4N-8N with tetraploidization, and the cell size became larger. After the start of intersegmental and pharyngeal blood flow, the erythrocytes became smaller. The medaka mutant kyo showed erythrocytes of large size, and positional cloning of kyo demonstrated the candidate gene TFDP1, indicating higher polyploidization due to arrest in S-phase in erythrocytes of the kyo mutant. Conclusions: From our findings, we uncovered a previously unrecognized system for the regulation of the size/number in the blood flow:proliferation of erythrocytes following tetraploidization during embryonic development. Developmental Dynamics 244:651-668, 2015. IntroductionBlood flow carries oxygen to the whole body, and impact to blood circulation whether by mechanical obstruction in the case of polycythemia or thrombocytosis or by functional abnormalities such as anemia may cause serious health concerns (Demirog lu, 1997;Tefferi, 2003;Weiss and Goodnough, 2005). Because of the closed system of blood circulation, blood flow requires the correct size/number of erythrocytes (Tamplin and Zon, 2010;Sankaran et al., 2012). Active angiogenesis during embryonic development introduces intricate blood flow and burdens erythrocytes with two tasks: having the proper size and number for maintenance of blood flow. As to the number, longer blood vessels require more erythrocytes; however, too many erythrocytes block the blood flow (Tefferi, 2003). Regarding size, narrower blood vessels require smaller erythrocytes; however, small erythrocytes cannot carry enough oxygen. Thus, erythrocytes are required to have adaptability to afford an adequate size/number due to the change of blood flow. In a previous study, the start of blood circulation was shown to affect angiogenesis (Udan et al., 2013), but relationships between the length and diameter of blood vessels and the size/number of erythrocytes during development have remained unclear, because mice are not suitable for such studies. Therefore, we decided to use the medaka fish as a model animal to observe blood flow in early developmental stages. Compared to mice, medaka have a transparent body and quick development, both of which are beneficial for observing erythrocytes in the change of blood flow throughout the whole developmental process (Wittbrodt et al., 2002). The question arises as to how embryonic erythrocytes regulate their size/number to adapt to the change of blood flow during medaka development. In this study, we divided the blood flow event into 3 phases during medaka development to study the relationship between angiogenesis and t...

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Temporal and Spatial Patterns of Gene Expression for the Hatching Enzyme in the Teleost Embryo, Oryzias latipes

Cited by 90 publications

References 0 publications

Gene cooption without duplication during the evolution of a male-pregnancy gene in pipefish

Gene cooption without duplication during the evolution of a male-pregnancy gene in pipefish

Molecular Phylogeny and Functional Genomics of β-Galactoside α2,6-Sialyltransferases That Explain Ubiquitous Expression of st6gal1 Gene in Amniotes

Proliferation following tetraploidization regulates the size and number of erythrocytes in the blood flow during medaka development, as revealed by the abnormal karyotype of erythrocytes in the medaka TFDP1 mutant

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