Development of branchial ionocytes in embryonic and larval stages of cloudy catshark, Scyliorhinus torazame
In teleost fish, branchial ionocytes are important sites for osmoregulation and acid-base regulation by maintaining ionic balance in the body fluid. During the early developmental stages before the formation of the gills, teleost ionocytes are localized in the yolk-sac membrane and body skin. By com...
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| creator | Inokuchi, Mayu Someya, Yumiko Endo, Keitaro Kamioka, Katsunori Katano, Wataru Takagi, Wataru Honda, Yuki Ogawa, Nobuhiro Koshiba-Takeuchi, Kazuko Ohtani-Kaneko, Ritsuko Hyodo, Susumu |
| description | In teleost fish, branchial ionocytes are important sites for osmoregulation and acid-base regulation by maintaining ionic balance in the body fluid. During the early developmental stages before the formation of the gills, teleost ionocytes are localized in the yolk-sac membrane and body skin. By comparing with teleost fish, much less is known about ionocytes in developing embryos of elasmobranch fish. The present study investigated the development of ionocytes in the embryo and larva of cloudy catshark,
Scyliorhinus torazame
. We first observed ionocyte distribution by immunohistochemical staining with anti-Na
+
/K
+
-ATPase (NKA) and anti-vacuolar-type H
+
-ATPase (V-ATPase) antibodies. The NKA- and V-ATPase-rich ionocytes appeared as single cells in the gill filaments from stage 31, the stage of pre-hatching, while the ionocytes on the body skin and yolk-sac membrane were also observed. From stage 32, in addition to single ionocytes on the gill filaments, some outstanding follicular structures of NKA-immunoreactive cells were developed to fill the inter-filament region of the gill septa. The follicular ionocytes possess NKA in the basolateral membrane and Na
+
/H
+
exchanger 3 in the apical membrane, indicating that they are involved in acid-base regulation like single NKA-rich ionocytes. Three-dimensional analysis and whole-mount immunohistochemistry revealed that the distribution of follicular ionocytes was limited to the rostral side of gill septum. The rostral sides of gill septum might be exposed to faster water flow than caudal side because the gills of sharks gently curved backward. This dissymmetric distribution of follicular ionocytes is considered to facilitate efficient body-fluid homeostasis of catshark embryo. |
| doi_str_mv | 10.1007/s00441-024-03897-4 |
| format | Article |
| fullrecord | <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_11291541</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>3055453452</sourcerecordid><originalsourceid>FETCH-LOGICAL-c426t-a5342b5d6cb711ba1682b8833e3eaa7a229d1647937e8cf3d2f0dc11828c11963</originalsourceid><addsrcrecordid>eNp9kUtv1DAUhS0EokPhD7BAltiwIOBXbGeFqvKUKrEAJHbWjePMuHXswU5GCr8elynlsWDju7jfOb5HB6HHlLyghKiXhRAhaEOYaAjXnWrEHbShgrOGaKXvog3hhDVKyq8n6EEpl4RQIWV3H51wrYRmtN2gq9fu4ELaTy7OOI24zxDtzkPAPsVk19kV7CN2U5_XFL3FEAccIB8qUWbY1nVV2ZCWYcUW5rKDfPUcf7Jr8CnvfFwKnlOG7zC5h-jeCKG4RzfzFH15--bz-fvm4uO7D-dnF40VTM4NtFywvh2k7RWlPVCpWa815447AAWMdQOVQnVcOW1HPrCRDJZSzXR9O8lP0auj737pJzfYGi1DMPvsJ8irSeDN35vod2abDoZS1tFW0Orw7MYhp2-LK7OZfLEuBIguLcVw0raintmyij79B71MS441X6W0FB1jXFSKHSmbUynZjbfXUGKuyzTHMk0t0_ws01yLnvyZ41byq70K8CNQ6ipuXf79939sfwBuraws</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>3086492234</pqid></control><display><type>article</type><title>Development of branchial ionocytes in embryonic and larval stages of cloudy catshark, Scyliorhinus torazame</title><source>MEDLINE</source><source>SpringerLink Journals - AutoHoldings</source><creator>Inokuchi, Mayu ; Someya, Yumiko ; Endo, Keitaro ; Kamioka, Katsunori ; Katano, Wataru ; Takagi, Wataru ; Honda, Yuki ; Ogawa, Nobuhiro ; Koshiba-Takeuchi, Kazuko ; Ohtani-Kaneko, Ritsuko ; Hyodo, Susumu</creator><creatorcontrib>Inokuchi, Mayu ; Someya, Yumiko ; Endo, Keitaro ; Kamioka, Katsunori ; Katano, Wataru ; Takagi, Wataru ; Honda, Yuki ; Ogawa, Nobuhiro ; Koshiba-Takeuchi, Kazuko ; Ohtani-Kaneko, Ritsuko ; Hyodo, Susumu</creatorcontrib><description>In teleost fish, branchial ionocytes are important sites for osmoregulation and acid-base regulation by maintaining ionic balance in the body fluid. During the early developmental stages before the formation of the gills, teleost ionocytes are localized in the yolk-sac membrane and body skin. By comparing with teleost fish, much less is known about ionocytes in developing embryos of elasmobranch fish. The present study investigated the development of ionocytes in the embryo and larva of cloudy catshark,
Scyliorhinus torazame
. We first observed ionocyte distribution by immunohistochemical staining with anti-Na
+
/K
+
-ATPase (NKA) and anti-vacuolar-type H
+
-ATPase (V-ATPase) antibodies. The NKA- and V-ATPase-rich ionocytes appeared as single cells in the gill filaments from stage 31, the stage of pre-hatching, while the ionocytes on the body skin and yolk-sac membrane were also observed. From stage 32, in addition to single ionocytes on the gill filaments, some outstanding follicular structures of NKA-immunoreactive cells were developed to fill the inter-filament region of the gill septa. The follicular ionocytes possess NKA in the basolateral membrane and Na
+
/H
+
exchanger 3 in the apical membrane, indicating that they are involved in acid-base regulation like single NKA-rich ionocytes. Three-dimensional analysis and whole-mount immunohistochemistry revealed that the distribution of follicular ionocytes was limited to the rostral side of gill septum. The rostral sides of gill septum might be exposed to faster water flow than caudal side because the gills of sharks gently curved backward. This dissymmetric distribution of follicular ionocytes is considered to facilitate efficient body-fluid homeostasis of catshark embryo.</description><identifier>ISSN: 0302-766X</identifier><identifier>ISSN: 1432-0878</identifier><identifier>EISSN: 1432-0878</identifier><identifier>DOI: 10.1007/s00441-024-03897-4</identifier><identifier>PMID: 38748215</identifier><language>eng</language><publisher>Berlin/Heidelberg: Springer Berlin Heidelberg</publisher><subject>Acid-base regulation ; Animals ; Biomedical and Life Sciences ; Biomedicine ; Developmental stages ; Dimensional analysis ; Embryo, Nonmammalian - cytology ; Embryo, Nonmammalian - metabolism ; Embryogenesis ; Embryos ; Filaments ; Fluid flow ; Gills ; Gills - cytology ; Gills - embryology ; Gills - metabolism ; H+-transporting ATPase ; Hatching ; Homeostasis ; Human Genetics ; Immunohistochemistry ; Larva - metabolism ; Molecular Medicine ; Na+/H+-exchanging ATPase ; Na+/K+-exchanging ATPase ; Osmoregulation ; Proteomics ; Regular ; Regular Article ; Scyliorhinus torazame ; Septum ; Sharks - embryology ; Sharks - metabolism ; Sodium-Potassium-Exchanging ATPase - metabolism ; Vacuolar Proton-Translocating ATPases - metabolism ; Water flow</subject><ispartof>Cell and tissue research, 2024-08, Vol.397 (2), p.81-95</ispartof><rights>The Author(s) 2024</rights><rights>2024. The Author(s).</rights><rights>The Author(s) 2024. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>The Author(s) 2024 2024</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c426t-a5342b5d6cb711ba1682b8833e3eaa7a229d1647937e8cf3d2f0dc11828c11963</cites><orcidid>0000-0001-6309-4567</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1007/s00441-024-03897-4$$EPDF$$P50$$Gspringer$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1007/s00441-024-03897-4$$EHTML$$P50$$Gspringer$$Hfree_for_read</linktohtml><link.rule.ids>230,314,780,784,885,27924,27925,41488,42557,51319</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38748215$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Inokuchi, Mayu</creatorcontrib><creatorcontrib>Someya, Yumiko</creatorcontrib><creatorcontrib>Endo, Keitaro</creatorcontrib><creatorcontrib>Kamioka, Katsunori</creatorcontrib><creatorcontrib>Katano, Wataru</creatorcontrib><creatorcontrib>Takagi, Wataru</creatorcontrib><creatorcontrib>Honda, Yuki</creatorcontrib><creatorcontrib>Ogawa, Nobuhiro</creatorcontrib><creatorcontrib>Koshiba-Takeuchi, Kazuko</creatorcontrib><creatorcontrib>Ohtani-Kaneko, Ritsuko</creatorcontrib><creatorcontrib>Hyodo, Susumu</creatorcontrib><title>Development of branchial ionocytes in embryonic and larval stages of cloudy catshark, Scyliorhinus torazame</title><title>Cell and tissue research</title><addtitle>Cell Tissue Res</addtitle><addtitle>Cell Tissue Res</addtitle><description>In teleost fish, branchial ionocytes are important sites for osmoregulation and acid-base regulation by maintaining ionic balance in the body fluid. During the early developmental stages before the formation of the gills, teleost ionocytes are localized in the yolk-sac membrane and body skin. By comparing with teleost fish, much less is known about ionocytes in developing embryos of elasmobranch fish. The present study investigated the development of ionocytes in the embryo and larva of cloudy catshark,
Scyliorhinus torazame
. We first observed ionocyte distribution by immunohistochemical staining with anti-Na
+
/K
+
-ATPase (NKA) and anti-vacuolar-type H
+
-ATPase (V-ATPase) antibodies. The NKA- and V-ATPase-rich ionocytes appeared as single cells in the gill filaments from stage 31, the stage of pre-hatching, while the ionocytes on the body skin and yolk-sac membrane were also observed. From stage 32, in addition to single ionocytes on the gill filaments, some outstanding follicular structures of NKA-immunoreactive cells were developed to fill the inter-filament region of the gill septa. The follicular ionocytes possess NKA in the basolateral membrane and Na
+
/H
+
exchanger 3 in the apical membrane, indicating that they are involved in acid-base regulation like single NKA-rich ionocytes. Three-dimensional analysis and whole-mount immunohistochemistry revealed that the distribution of follicular ionocytes was limited to the rostral side of gill septum. The rostral sides of gill septum might be exposed to faster water flow than caudal side because the gills of sharks gently curved backward. This dissymmetric distribution of follicular ionocytes is considered to facilitate efficient body-fluid homeostasis of catshark embryo.</description><subject>Acid-base regulation</subject><subject>Animals</subject><subject>Biomedical and Life Sciences</subject><subject>Biomedicine</subject><subject>Developmental stages</subject><subject>Dimensional analysis</subject><subject>Embryo, Nonmammalian - cytology</subject><subject>Embryo, Nonmammalian - metabolism</subject><subject>Embryogenesis</subject><subject>Embryos</subject><subject>Filaments</subject><subject>Fluid flow</subject><subject>Gills</subject><subject>Gills - cytology</subject><subject>Gills - embryology</subject><subject>Gills - metabolism</subject><subject>H+-transporting ATPase</subject><subject>Hatching</subject><subject>Homeostasis</subject><subject>Human Genetics</subject><subject>Immunohistochemistry</subject><subject>Larva - metabolism</subject><subject>Molecular Medicine</subject><subject>Na+/H+-exchanging ATPase</subject><subject>Na+/K+-exchanging ATPase</subject><subject>Osmoregulation</subject><subject>Proteomics</subject><subject>Regular</subject><subject>Regular Article</subject><subject>Scyliorhinus torazame</subject><subject>Septum</subject><subject>Sharks - embryology</subject><subject>Sharks - metabolism</subject><subject>Sodium-Potassium-Exchanging ATPase - metabolism</subject><subject>Vacuolar Proton-Translocating ATPases - metabolism</subject><subject>Water flow</subject><issn>0302-766X</issn><issn>1432-0878</issn><issn>1432-0878</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>C6C</sourceid><sourceid>EIF</sourceid><recordid>eNp9kUtv1DAUhS0EokPhD7BAltiwIOBXbGeFqvKUKrEAJHbWjePMuHXswU5GCr8elynlsWDju7jfOb5HB6HHlLyghKiXhRAhaEOYaAjXnWrEHbShgrOGaKXvog3hhDVKyq8n6EEpl4RQIWV3H51wrYRmtN2gq9fu4ELaTy7OOI24zxDtzkPAPsVk19kV7CN2U5_XFL3FEAccIB8qUWbY1nVV2ZCWYcUW5rKDfPUcf7Jr8CnvfFwKnlOG7zC5h-jeCKG4RzfzFH15--bz-fvm4uO7D-dnF40VTM4NtFywvh2k7RWlPVCpWa815447AAWMdQOVQnVcOW1HPrCRDJZSzXR9O8lP0auj737pJzfYGi1DMPvsJ8irSeDN35vod2abDoZS1tFW0Orw7MYhp2-LK7OZfLEuBIguLcVw0raintmyij79B71MS441X6W0FB1jXFSKHSmbUynZjbfXUGKuyzTHMk0t0_ws01yLnvyZ41byq70K8CNQ6ipuXf79939sfwBuraws</recordid><startdate>20240801</startdate><enddate>20240801</enddate><creator>Inokuchi, Mayu</creator><creator>Someya, Yumiko</creator><creator>Endo, Keitaro</creator><creator>Kamioka, Katsunori</creator><creator>Katano, Wataru</creator><creator>Takagi, Wataru</creator><creator>Honda, Yuki</creator><creator>Ogawa, Nobuhiro</creator><creator>Koshiba-Takeuchi, Kazuko</creator><creator>Ohtani-Kaneko, Ritsuko</creator><creator>Hyodo, Susumu</creator><general>Springer Berlin Heidelberg</general><general>Springer Nature B.V</general><scope>C6C</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QP</scope><scope>7QR</scope><scope>7SS</scope><scope>7TK</scope><scope>8FD</scope><scope>FR3</scope><scope>K9.</scope><scope>NAPCQ</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-6309-4567</orcidid></search><sort><creationdate>20240801</creationdate><title>Development of branchial ionocytes in embryonic and larval stages of cloudy catshark, Scyliorhinus torazame</title><author>Inokuchi, Mayu ; Someya, Yumiko ; Endo, Keitaro ; Kamioka, Katsunori ; Katano, Wataru ; Takagi, Wataru ; Honda, Yuki ; Ogawa, Nobuhiro ; Koshiba-Takeuchi, Kazuko ; Ohtani-Kaneko, Ritsuko ; Hyodo, Susumu</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c426t-a5342b5d6cb711ba1682b8833e3eaa7a229d1647937e8cf3d2f0dc11828c11963</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Acid-base regulation</topic><topic>Animals</topic><topic>Biomedical and Life Sciences</topic><topic>Biomedicine</topic><topic>Developmental stages</topic><topic>Dimensional analysis</topic><topic>Embryo, Nonmammalian - cytology</topic><topic>Embryo, Nonmammalian - metabolism</topic><topic>Embryogenesis</topic><topic>Embryos</topic><topic>Filaments</topic><topic>Fluid flow</topic><topic>Gills</topic><topic>Gills - cytology</topic><topic>Gills - embryology</topic><topic>Gills - metabolism</topic><topic>H+-transporting ATPase</topic><topic>Hatching</topic><topic>Homeostasis</topic><topic>Human Genetics</topic><topic>Immunohistochemistry</topic><topic>Larva - metabolism</topic><topic>Molecular Medicine</topic><topic>Na+/H+-exchanging ATPase</topic><topic>Na+/K+-exchanging ATPase</topic><topic>Osmoregulation</topic><topic>Proteomics</topic><topic>Regular</topic><topic>Regular Article</topic><topic>Scyliorhinus torazame</topic><topic>Septum</topic><topic>Sharks - embryology</topic><topic>Sharks - metabolism</topic><topic>Sodium-Potassium-Exchanging ATPase - metabolism</topic><topic>Vacuolar Proton-Translocating ATPases - metabolism</topic><topic>Water flow</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Inokuchi, Mayu</creatorcontrib><creatorcontrib>Someya, Yumiko</creatorcontrib><creatorcontrib>Endo, Keitaro</creatorcontrib><creatorcontrib>Kamioka, Katsunori</creatorcontrib><creatorcontrib>Katano, Wataru</creatorcontrib><creatorcontrib>Takagi, Wataru</creatorcontrib><creatorcontrib>Honda, Yuki</creatorcontrib><creatorcontrib>Ogawa, Nobuhiro</creatorcontrib><creatorcontrib>Koshiba-Takeuchi, Kazuko</creatorcontrib><creatorcontrib>Ohtani-Kaneko, Ritsuko</creatorcontrib><creatorcontrib>Hyodo, Susumu</creatorcontrib><collection>Springer Nature OA/Free Journals</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Neurosciences Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Nursing & Allied Health Premium</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Cell and tissue research</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Inokuchi, Mayu</au><au>Someya, Yumiko</au><au>Endo, Keitaro</au><au>Kamioka, Katsunori</au><au>Katano, Wataru</au><au>Takagi, Wataru</au><au>Honda, Yuki</au><au>Ogawa, Nobuhiro</au><au>Koshiba-Takeuchi, Kazuko</au><au>Ohtani-Kaneko, Ritsuko</au><au>Hyodo, Susumu</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Development of branchial ionocytes in embryonic and larval stages of cloudy catshark, Scyliorhinus torazame</atitle><jtitle>Cell and tissue research</jtitle><stitle>Cell Tissue Res</stitle><addtitle>Cell Tissue Res</addtitle><date>2024-08-01</date><risdate>2024</risdate><volume>397</volume><issue>2</issue><spage>81</spage><epage>95</epage><pages>81-95</pages><issn>0302-766X</issn><issn>1432-0878</issn><eissn>1432-0878</eissn><abstract>In teleost fish, branchial ionocytes are important sites for osmoregulation and acid-base regulation by maintaining ionic balance in the body fluid. During the early developmental stages before the formation of the gills, teleost ionocytes are localized in the yolk-sac membrane and body skin. By comparing with teleost fish, much less is known about ionocytes in developing embryos of elasmobranch fish. The present study investigated the development of ionocytes in the embryo and larva of cloudy catshark,
Scyliorhinus torazame
. We first observed ionocyte distribution by immunohistochemical staining with anti-Na
+
/K
+
-ATPase (NKA) and anti-vacuolar-type H
+
-ATPase (V-ATPase) antibodies. The NKA- and V-ATPase-rich ionocytes appeared as single cells in the gill filaments from stage 31, the stage of pre-hatching, while the ionocytes on the body skin and yolk-sac membrane were also observed. From stage 32, in addition to single ionocytes on the gill filaments, some outstanding follicular structures of NKA-immunoreactive cells were developed to fill the inter-filament region of the gill septa. The follicular ionocytes possess NKA in the basolateral membrane and Na
+
/H
+
exchanger 3 in the apical membrane, indicating that they are involved in acid-base regulation like single NKA-rich ionocytes. Three-dimensional analysis and whole-mount immunohistochemistry revealed that the distribution of follicular ionocytes was limited to the rostral side of gill septum. The rostral sides of gill septum might be exposed to faster water flow than caudal side because the gills of sharks gently curved backward. This dissymmetric distribution of follicular ionocytes is considered to facilitate efficient body-fluid homeostasis of catshark embryo.</abstract><cop>Berlin/Heidelberg</cop><pub>Springer Berlin Heidelberg</pub><pmid>38748215</pmid><doi>10.1007/s00441-024-03897-4</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0001-6309-4567</orcidid><oa>free_for_read</oa></addata></record> |
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| ispartof | Cell and tissue research, 2024-08, Vol.397 (2), p.81-95 |
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| language | eng |
| recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_11291541 |
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| subjects | Acid-base regulation Animals Biomedical and Life Sciences Biomedicine Developmental stages Dimensional analysis Embryo, Nonmammalian - cytology Embryo, Nonmammalian - metabolism Embryogenesis Embryos Filaments Fluid flow Gills Gills - cytology Gills - embryology Gills - metabolism H+-transporting ATPase Hatching Homeostasis Human Genetics Immunohistochemistry Larva - metabolism Molecular Medicine Na+/H+-exchanging ATPase Na+/K+-exchanging ATPase Osmoregulation Proteomics Regular Regular Article Scyliorhinus torazame Septum Sharks - embryology Sharks - metabolism Sodium-Potassium-Exchanging ATPase - metabolism Vacuolar Proton-Translocating ATPases - metabolism Water flow |
| title | Development of branchial ionocytes in embryonic and larval stages of cloudy catshark, Scyliorhinus torazame |
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