Tissue homeostasis in sponges: Quantitative analysis of cell proliferation and apoptosis
Tissues of multicellular animals are maintained due to a tight balance between cell proliferation and programmed cell death. Sponges are early branching metazoans essential to understanding the key mechanisms of tissue homeostasis. This article is dedicated to the comparative analysis of proliferati...
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Veröffentlicht in: | Journal of experimental zoology. Part B, Molecular and developmental evolution Molecular and developmental evolution, 2022-09, Vol.338 (6), p.360-381 |
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container_title | Journal of experimental zoology. Part B, Molecular and developmental evolution |
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creator | Melnikov, Nikolai P. Bolshakov, Fyodor V. Frolova, Veronika S. Skorentseva, Kseniia V. Ereskovsky, Alexander V. Saidova, Alina A. Lavrov, Andrey I. |
description | Tissues of multicellular animals are maintained due to a tight balance between cell proliferation and programmed cell death. Sponges are early branching metazoans essential to understanding the key mechanisms of tissue homeostasis. This article is dedicated to the comparative analysis of proliferation and apoptosis in intact tissues of two sponges, Halisarca dujardinii (class Demospongiae) and Leucosolenia variabilis (class Calcarea). Labeled nucleotides EdU and anti‐phosphorylated histone 3 antibodies reveal a considerable number of cycling cells in intact tissues of both species. Quantitative DNA staining reveals the classic cell cycle distribution curve. The main type of cycling cells are choanocytes ‐ flagellated cells of the aquiferous system. The rate of proliferation remains constant throughout various areas of sponge bodies that contain choanocytes. The EdU tracking experiments conducted in H. dujardinii indicate that choanocytes may give rise to mesohyl cells through migration. The number of apoptotic cells in tissues of both species is insignificant, although being comparable to the renewing tissues of other animals. In vivo studies with tetramethylrhodamine ethyl ester and CellEvent Caspase‐3/7 indicate that apoptosis might be independent of mitochondrial outer membrane permeabilization. Altogether, a combination of confocal laser scanning microscopy and flow cytometry provides a quantitative description of cell proliferation and apoptosis in sponges displaying either rapid growth or cell turnover.
Sponges Halisarca dujardinii and Leucosolenia variabilis contain a considerable number of cycling cells in intact tissues, with choanocytes showing the most active proliferation. The EdU tracking experiments conducted in H. dujardinii indicate that choanocytes may give rise to mesohyl cells through migration. The number of apoptotic cells in tissues of both species is insignificant, although being comparable to the renewing tissues of other animals.
Research Highlights
Intact tissues of Halisarca dujardinii and Leucosolenia variabilis are highly proliferative.
Proliferation of choanocytes maintains the renewal of feeding structures and mesohyl cells.
Apoptosis is involved in regular cell turnover. |
doi_str_mv | 10.1002/jez.b.23138 |
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Sponges Halisarca dujardinii and Leucosolenia variabilis contain a considerable number of cycling cells in intact tissues, with choanocytes showing the most active proliferation. The EdU tracking experiments conducted in H. dujardinii indicate that choanocytes may give rise to mesohyl cells through migration. The number of apoptotic cells in tissues of both species is insignificant, although being comparable to the renewing tissues of other animals.
Research Highlights
Intact tissues of Halisarca dujardinii and Leucosolenia variabilis are highly proliferative.
Proliferation of choanocytes maintains the renewal of feeding structures and mesohyl cells.
Apoptosis is involved in regular cell turnover.</description><identifier>ISSN: 1552-5007</identifier><identifier>EISSN: 1552-5015</identifier><identifier>DOI: 10.1002/jez.b.23138</identifier><identifier>PMID: 35468249</identifier><language>eng</language><publisher>United States: Wiley</publisher><subject>apoptosis ; calcarea ; cell proliferation ; cell turnover ; Cellular Biology ; demospongiae ; Development Biology ; Life Sciences ; porifera ; Subcellular Processes</subject><ispartof>Journal of experimental zoology. Part B, Molecular and developmental evolution, 2022-09, Vol.338 (6), p.360-381</ispartof><rights>2022 Wiley Periodicals LLC.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4038-936adcc817fd213a14e1c35abbc369279d19561a48de9d77530a3b0b1a516c4a3</citedby><cites>FETCH-LOGICAL-c4038-936adcc817fd213a14e1c35abbc369279d19561a48de9d77530a3b0b1a516c4a3</cites><orcidid>0000-0003-1079-7204 ; 0000-0002-0788-9039</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1002%2Fjez.b.23138$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1002%2Fjez.b.23138$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>230,314,780,784,885,1417,27924,27925,45574,45575</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35468249$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-03651888$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Melnikov, Nikolai P.</creatorcontrib><creatorcontrib>Bolshakov, Fyodor V.</creatorcontrib><creatorcontrib>Frolova, Veronika S.</creatorcontrib><creatorcontrib>Skorentseva, Kseniia V.</creatorcontrib><creatorcontrib>Ereskovsky, Alexander V.</creatorcontrib><creatorcontrib>Saidova, Alina A.</creatorcontrib><creatorcontrib>Lavrov, Andrey I.</creatorcontrib><title>Tissue homeostasis in sponges: Quantitative analysis of cell proliferation and apoptosis</title><title>Journal of experimental zoology. Part B, Molecular and developmental evolution</title><addtitle>J Exp Zool B Mol Dev Evol</addtitle><description>Tissues of multicellular animals are maintained due to a tight balance between cell proliferation and programmed cell death. Sponges are early branching metazoans essential to understanding the key mechanisms of tissue homeostasis. This article is dedicated to the comparative analysis of proliferation and apoptosis in intact tissues of two sponges, Halisarca dujardinii (class Demospongiae) and Leucosolenia variabilis (class Calcarea). Labeled nucleotides EdU and anti‐phosphorylated histone 3 antibodies reveal a considerable number of cycling cells in intact tissues of both species. Quantitative DNA staining reveals the classic cell cycle distribution curve. The main type of cycling cells are choanocytes ‐ flagellated cells of the aquiferous system. The rate of proliferation remains constant throughout various areas of sponge bodies that contain choanocytes. The EdU tracking experiments conducted in H. dujardinii indicate that choanocytes may give rise to mesohyl cells through migration. The number of apoptotic cells in tissues of both species is insignificant, although being comparable to the renewing tissues of other animals. In vivo studies with tetramethylrhodamine ethyl ester and CellEvent Caspase‐3/7 indicate that apoptosis might be independent of mitochondrial outer membrane permeabilization. Altogether, a combination of confocal laser scanning microscopy and flow cytometry provides a quantitative description of cell proliferation and apoptosis in sponges displaying either rapid growth or cell turnover.
Sponges Halisarca dujardinii and Leucosolenia variabilis contain a considerable number of cycling cells in intact tissues, with choanocytes showing the most active proliferation. The EdU tracking experiments conducted in H. dujardinii indicate that choanocytes may give rise to mesohyl cells through migration. The number of apoptotic cells in tissues of both species is insignificant, although being comparable to the renewing tissues of other animals.
Research Highlights
Intact tissues of Halisarca dujardinii and Leucosolenia variabilis are highly proliferative.
Proliferation of choanocytes maintains the renewal of feeding structures and mesohyl cells.
Apoptosis is involved in regular cell turnover.</description><subject>apoptosis</subject><subject>calcarea</subject><subject>cell proliferation</subject><subject>cell turnover</subject><subject>Cellular Biology</subject><subject>demospongiae</subject><subject>Development Biology</subject><subject>Life Sciences</subject><subject>porifera</subject><subject>Subcellular Processes</subject><issn>1552-5007</issn><issn>1552-5015</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><recordid>eNp90M1LwzAYBvAgipvTk3fpUZHOfDT98DbHdMpAhAniJbxtU5fRNrVpJ_OvN7VzR08JeX88SR6EzgkeE4zpzVp-j-MxZYSFB2hIOKcux4Qf7vc4GKATY9YW-5jzYzRg3PND6kVD9LZUxrTSWelCatOAUcZRpWMqXX5Ic-u8tFA2qoFGbaQDJeTbTujMSWSeO1Wtc5XJ2o51acepA5WuGm3NKTrKIDfybLeO0Ov9bDmdu4vnh8fpZOEmHmahGzEf0iQJSZCllDAgniQJ4xDHCfMjGkQpibhPwAtTGaVBwBkGFuOYACd-4gEboas-dwW5qGpVQL0VGpSYTxaiO8PM5yQMww2x9rK39t2frTSNKJTpPgKl1K0R1OfcXkYZt_S6p0mtjallts8mWHS1C1u7iMVv7VZf7ILbuJDp3v71bAHtwZfK5fa_LPE0e7_rU38A8wCN1g</recordid><startdate>202209</startdate><enddate>202209</enddate><creator>Melnikov, Nikolai P.</creator><creator>Bolshakov, Fyodor V.</creator><creator>Frolova, Veronika S.</creator><creator>Skorentseva, Kseniia V.</creator><creator>Ereskovsky, Alexander V.</creator><creator>Saidova, Alina A.</creator><creator>Lavrov, Andrey I.</creator><general>Wiley</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>1XC</scope><scope>VOOES</scope><orcidid>https://orcid.org/0000-0003-1079-7204</orcidid><orcidid>https://orcid.org/0000-0002-0788-9039</orcidid></search><sort><creationdate>202209</creationdate><title>Tissue homeostasis in sponges: Quantitative analysis of cell proliferation and apoptosis</title><author>Melnikov, Nikolai P. ; Bolshakov, Fyodor V. ; Frolova, Veronika S. ; Skorentseva, Kseniia V. ; Ereskovsky, Alexander V. ; Saidova, Alina A. ; Lavrov, Andrey I.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4038-936adcc817fd213a14e1c35abbc369279d19561a48de9d77530a3b0b1a516c4a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>apoptosis</topic><topic>calcarea</topic><topic>cell proliferation</topic><topic>cell turnover</topic><topic>Cellular Biology</topic><topic>demospongiae</topic><topic>Development Biology</topic><topic>Life Sciences</topic><topic>porifera</topic><topic>Subcellular Processes</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Melnikov, Nikolai P.</creatorcontrib><creatorcontrib>Bolshakov, Fyodor V.</creatorcontrib><creatorcontrib>Frolova, Veronika S.</creatorcontrib><creatorcontrib>Skorentseva, Kseniia V.</creatorcontrib><creatorcontrib>Ereskovsky, Alexander V.</creatorcontrib><creatorcontrib>Saidova, Alina A.</creatorcontrib><creatorcontrib>Lavrov, Andrey I.</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><jtitle>Journal of experimental zoology. Part B, Molecular and developmental evolution</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Melnikov, Nikolai P.</au><au>Bolshakov, Fyodor V.</au><au>Frolova, Veronika S.</au><au>Skorentseva, Kseniia V.</au><au>Ereskovsky, Alexander V.</au><au>Saidova, Alina A.</au><au>Lavrov, Andrey I.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Tissue homeostasis in sponges: Quantitative analysis of cell proliferation and apoptosis</atitle><jtitle>Journal of experimental zoology. Part B, Molecular and developmental evolution</jtitle><addtitle>J Exp Zool B Mol Dev Evol</addtitle><date>2022-09</date><risdate>2022</risdate><volume>338</volume><issue>6</issue><spage>360</spage><epage>381</epage><pages>360-381</pages><issn>1552-5007</issn><eissn>1552-5015</eissn><abstract>Tissues of multicellular animals are maintained due to a tight balance between cell proliferation and programmed cell death. Sponges are early branching metazoans essential to understanding the key mechanisms of tissue homeostasis. This article is dedicated to the comparative analysis of proliferation and apoptosis in intact tissues of two sponges, Halisarca dujardinii (class Demospongiae) and Leucosolenia variabilis (class Calcarea). Labeled nucleotides EdU and anti‐phosphorylated histone 3 antibodies reveal a considerable number of cycling cells in intact tissues of both species. Quantitative DNA staining reveals the classic cell cycle distribution curve. The main type of cycling cells are choanocytes ‐ flagellated cells of the aquiferous system. The rate of proliferation remains constant throughout various areas of sponge bodies that contain choanocytes. The EdU tracking experiments conducted in H. dujardinii indicate that choanocytes may give rise to mesohyl cells through migration. The number of apoptotic cells in tissues of both species is insignificant, although being comparable to the renewing tissues of other animals. In vivo studies with tetramethylrhodamine ethyl ester and CellEvent Caspase‐3/7 indicate that apoptosis might be independent of mitochondrial outer membrane permeabilization. Altogether, a combination of confocal laser scanning microscopy and flow cytometry provides a quantitative description of cell proliferation and apoptosis in sponges displaying either rapid growth or cell turnover.
Sponges Halisarca dujardinii and Leucosolenia variabilis contain a considerable number of cycling cells in intact tissues, with choanocytes showing the most active proliferation. The EdU tracking experiments conducted in H. dujardinii indicate that choanocytes may give rise to mesohyl cells through migration. The number of apoptotic cells in tissues of both species is insignificant, although being comparable to the renewing tissues of other animals.
Research Highlights
Intact tissues of Halisarca dujardinii and Leucosolenia variabilis are highly proliferative.
Proliferation of choanocytes maintains the renewal of feeding structures and mesohyl cells.
Apoptosis is involved in regular cell turnover.</abstract><cop>United States</cop><pub>Wiley</pub><pmid>35468249</pmid><doi>10.1002/jez.b.23138</doi><tpages>22</tpages><orcidid>https://orcid.org/0000-0003-1079-7204</orcidid><orcidid>https://orcid.org/0000-0002-0788-9039</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | apoptosis calcarea cell proliferation cell turnover Cellular Biology demospongiae Development Biology Life Sciences porifera Subcellular Processes |
title | Tissue homeostasis in sponges: Quantitative analysis of cell proliferation and apoptosis |
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