Cohesin composition and dosage independently affect early development in zebrafish
Cohesin, a chromatin-associated protein complex with four core subunits (Smc1a, Smc3, Rad21 and either Stag1 or 2), has a central role in cell proliferation and gene expression in metazoans. Human developmental disorders termed 'cohesinopathies' are characterized by germline variants of co...
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creator | Labudina, Anastasia A Meier, Michael Gimenez, Gregory Tatarakis, David Ketharnathan, Sarada Mackie, Bridget Schilling, Thomas F Antony, Jisha Horsfield, Julia A |
description | Cohesin, a chromatin-associated protein complex with four core subunits (Smc1a, Smc3, Rad21 and either Stag1 or 2), has a central role in cell proliferation and gene expression in metazoans. Human developmental disorders termed 'cohesinopathies' are characterized by germline variants of cohesin or its regulators that do not entirely eliminate cohesin function. However, it is not clear whether mutations in individual cohesin subunits have independent developmental consequences. Here, we show that zebrafish rad21 or stag2b mutants independently influence embryonic tailbud development. Both mutants have altered mesoderm induction, but only homozygous or heterozygous rad21 mutation affects cell cycle gene expression. stag2b mutants have narrower notochords and reduced Wnt signaling in neuromesodermal progenitors as revealed by single-cell RNA sequencing. Stimulation of Wnt signaling rescues transcription and morphology in stag2b, but not rad21, mutants. Our results suggest that mutations altering the quantity versus composition of cohesin have independent developmental consequences, with implications for the understanding and management of cohesinopathies. |
doi_str_mv | 10.1242/dev.202593 |
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Human developmental disorders termed 'cohesinopathies' are characterized by germline variants of cohesin or its regulators that do not entirely eliminate cohesin function. However, it is not clear whether mutations in individual cohesin subunits have independent developmental consequences. Here, we show that zebrafish rad21 or stag2b mutants independently influence embryonic tailbud development. Both mutants have altered mesoderm induction, but only homozygous or heterozygous rad21 mutation affects cell cycle gene expression. stag2b mutants have narrower notochords and reduced Wnt signaling in neuromesodermal progenitors as revealed by single-cell RNA sequencing. Stimulation of Wnt signaling rescues transcription and morphology in stag2b, but not rad21, mutants. Our results suggest that mutations altering the quantity versus composition of cohesin have independent developmental consequences, with implications for the understanding and management of cohesinopathies.</description><identifier>ISSN: 0950-1991</identifier><identifier>ISSN: 1477-9129</identifier><identifier>EISSN: 1477-9129</identifier><identifier>DOI: 10.1242/dev.202593</identifier><identifier>PMID: 38975838</identifier><language>eng</language><publisher>England: The Company of Biologists Ltd</publisher><subject>Animals ; Cell Cycle Proteins - genetics ; Cell Cycle Proteins - metabolism ; Chromosomal Proteins, Non-Histone - genetics ; Chromosomal Proteins, Non-Histone - metabolism ; Cohesins ; Embryonic Development - genetics ; Gene Dosage ; Gene Expression Regulation, Developmental ; Mesoderm - embryology ; Mesoderm - metabolism ; Mutation - genetics ; Wnt Signaling Pathway - genetics ; Zebrafish - embryology ; Zebrafish - genetics ; Zebrafish - metabolism ; Zebrafish Proteins - genetics ; Zebrafish Proteins - metabolism</subject><ispartof>Development (Cambridge), 2024-08, Vol.151 (15)</ispartof><rights>2024. 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Human developmental disorders termed 'cohesinopathies' are characterized by germline variants of cohesin or its regulators that do not entirely eliminate cohesin function. However, it is not clear whether mutations in individual cohesin subunits have independent developmental consequences. Here, we show that zebrafish rad21 or stag2b mutants independently influence embryonic tailbud development. Both mutants have altered mesoderm induction, but only homozygous or heterozygous rad21 mutation affects cell cycle gene expression. stag2b mutants have narrower notochords and reduced Wnt signaling in neuromesodermal progenitors as revealed by single-cell RNA sequencing. Stimulation of Wnt signaling rescues transcription and morphology in stag2b, but not rad21, mutants. Our results suggest that mutations altering the quantity versus composition of cohesin have independent developmental consequences, with implications for the understanding and management of cohesinopathies.</description><subject>Animals</subject><subject>Cell Cycle Proteins - genetics</subject><subject>Cell Cycle Proteins - metabolism</subject><subject>Chromosomal Proteins, Non-Histone - genetics</subject><subject>Chromosomal Proteins, Non-Histone - metabolism</subject><subject>Cohesins</subject><subject>Embryonic Development - genetics</subject><subject>Gene Dosage</subject><subject>Gene Expression Regulation, Developmental</subject><subject>Mesoderm - embryology</subject><subject>Mesoderm - metabolism</subject><subject>Mutation - genetics</subject><subject>Wnt Signaling Pathway - genetics</subject><subject>Zebrafish - embryology</subject><subject>Zebrafish - genetics</subject><subject>Zebrafish - metabolism</subject><subject>Zebrafish Proteins - genetics</subject><subject>Zebrafish Proteins - metabolism</subject><issn>0950-1991</issn><issn>1477-9129</issn><issn>1477-9129</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVkW1LwzAQx4Mobk7f-AGkL0XozEPbJK9Ehk8wEERfh6S5bpG2qU03mJ_ejM2hHNxx3I___7hD6JLgKaEZvbWwnlJMc8mO0JhknKeSUHmMxljmOCVSkhE6C-ETY8wKzk_RiAnJc8HEGL3N_BKCa5PSN50PbnC-TXRrE-uDXkDiWgsdxNQO9SbRVQXlkIDuYxNtofZdE0cRS77B9LpyYXmOTipdB7jY1wn6eHx4nz2n89enl9n9PC1pIYaUW51xVmVGGk2xtUVR5KXIcF4IbCjGhEtqZMYNAalFbjRwzlglhcDSFkDYBN3tdLuVacCWcY9e16rrXaP7jfLaqf-T1i3Vwq8VIYxwgrcK13uF3n-tIAyqcaGEutYt-FVQDPMiBpM8ojc7tOx9CD1UBx-C1fYLKp5D7b4Q4au_mx3Q37OzH_A1hFg</recordid><startdate>20240801</startdate><enddate>20240801</enddate><creator>Labudina, Anastasia A</creator><creator>Meier, Michael</creator><creator>Gimenez, Gregory</creator><creator>Tatarakis, David</creator><creator>Ketharnathan, Sarada</creator><creator>Mackie, Bridget</creator><creator>Schilling, Thomas F</creator><creator>Antony, Jisha</creator><creator>Horsfield, Julia A</creator><general>The Company of Biologists Ltd</general><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>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-9536-7790</orcidid></search><sort><creationdate>20240801</creationdate><title>Cohesin composition and dosage independently affect early development in zebrafish</title><author>Labudina, Anastasia A ; Meier, Michael ; Gimenez, Gregory ; Tatarakis, David ; Ketharnathan, Sarada ; Mackie, Bridget ; Schilling, Thomas F ; Antony, Jisha ; Horsfield, Julia A</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c268t-7da473f4b9ba20dd6665c8405680b2001792b947b1e9a85bae7733f98809d6e13</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Animals</topic><topic>Cell Cycle Proteins - genetics</topic><topic>Cell Cycle Proteins - metabolism</topic><topic>Chromosomal Proteins, Non-Histone - genetics</topic><topic>Chromosomal Proteins, Non-Histone - metabolism</topic><topic>Cohesins</topic><topic>Embryonic Development - genetics</topic><topic>Gene Dosage</topic><topic>Gene Expression Regulation, Developmental</topic><topic>Mesoderm - embryology</topic><topic>Mesoderm - metabolism</topic><topic>Mutation - genetics</topic><topic>Wnt Signaling Pathway - genetics</topic><topic>Zebrafish - embryology</topic><topic>Zebrafish - genetics</topic><topic>Zebrafish - metabolism</topic><topic>Zebrafish Proteins - genetics</topic><topic>Zebrafish Proteins - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Labudina, Anastasia A</creatorcontrib><creatorcontrib>Meier, Michael</creatorcontrib><creatorcontrib>Gimenez, Gregory</creatorcontrib><creatorcontrib>Tatarakis, David</creatorcontrib><creatorcontrib>Ketharnathan, Sarada</creatorcontrib><creatorcontrib>Mackie, Bridget</creatorcontrib><creatorcontrib>Schilling, Thomas F</creatorcontrib><creatorcontrib>Antony, Jisha</creatorcontrib><creatorcontrib>Horsfield, Julia A</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Development (Cambridge)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Labudina, Anastasia A</au><au>Meier, Michael</au><au>Gimenez, Gregory</au><au>Tatarakis, David</au><au>Ketharnathan, Sarada</au><au>Mackie, Bridget</au><au>Schilling, Thomas F</au><au>Antony, Jisha</au><au>Horsfield, Julia A</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Cohesin composition and dosage independently affect early development in zebrafish</atitle><jtitle>Development (Cambridge)</jtitle><addtitle>Development</addtitle><date>2024-08-01</date><risdate>2024</risdate><volume>151</volume><issue>15</issue><issn>0950-1991</issn><issn>1477-9129</issn><eissn>1477-9129</eissn><abstract>Cohesin, a chromatin-associated protein complex with four core subunits (Smc1a, Smc3, Rad21 and either Stag1 or 2), has a central role in cell proliferation and gene expression in metazoans. Human developmental disorders termed 'cohesinopathies' are characterized by germline variants of cohesin or its regulators that do not entirely eliminate cohesin function. However, it is not clear whether mutations in individual cohesin subunits have independent developmental consequences. Here, we show that zebrafish rad21 or stag2b mutants independently influence embryonic tailbud development. Both mutants have altered mesoderm induction, but only homozygous or heterozygous rad21 mutation affects cell cycle gene expression. stag2b mutants have narrower notochords and reduced Wnt signaling in neuromesodermal progenitors as revealed by single-cell RNA sequencing. Stimulation of Wnt signaling rescues transcription and morphology in stag2b, but not rad21, mutants. 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subjects | Animals Cell Cycle Proteins - genetics Cell Cycle Proteins - metabolism Chromosomal Proteins, Non-Histone - genetics Chromosomal Proteins, Non-Histone - metabolism Cohesins Embryonic Development - genetics Gene Dosage Gene Expression Regulation, Developmental Mesoderm - embryology Mesoderm - metabolism Mutation - genetics Wnt Signaling Pathway - genetics Zebrafish - embryology Zebrafish - genetics Zebrafish - metabolism Zebrafish Proteins - genetics Zebrafish Proteins - metabolism |
title | Cohesin composition and dosage independently affect early development in zebrafish |
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