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CEH-60/PBX regulates vitellogenesis and cuticle permeability through intestinal interaction with UNC-62/MEIS in Caenorhabditis elegans
The onset of sexual maturity involves dramatic changes in physiology and gene expression in many animals. These include abundant yolk protein production in egg-laying species, an energetically costly process under extensive transcriptional control. Here, we used the model organism Caenorhabditis ele...
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| Published in: | PLoS biology 2019-11, Vol.17 (11), p.e3000499-e3000499 |
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| creator | Van de Walle, Pieter Geens, Ellen Baggerman, Geert José Naranjo-Galindo, Francisco Askjaer, Peter Schoofs, Liliane Temmerman, Liesbet |
| description | The onset of sexual maturity involves dramatic changes in physiology and gene expression in many animals. These include abundant yolk protein production in egg-laying species, an energetically costly process under extensive transcriptional control. Here, we used the model organism Caenorhabditis elegans to provide evidence for the spatiotemporally defined interaction of two evolutionarily conserved transcription factors, CEH-60/PBX and UNC-62/MEIS, acting as a gateway to yolk protein production. Via proteomics, bimolecular fluorescence complementation (BiFC), and biochemical and functional readouts, we show that this interaction occurs in the intestine of animals at the onset of sexual maturity and suffices to support the reproductive program. Our electron micrographs and functional assays provide evidence that intestinal PBX/MEIS cooperation drives another process that depends on lipid mobilization: the formation of an impermeable epicuticle. Without this lipid-rich protective layer, mutant animals are hypersensitive to exogenous oxidative stress and are poor partners for mating. Dedicated communication between the hypodermis and intestine in C. elegans likely supports these physiological outcomes, and we propose a fundamental role for the conserved PBX/MEIS interaction in multicellular signaling networks that rely on lipid homeostasis. |
| doi_str_mv | 10.1371/journal.pbio.3000499 |
| format | article |
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These include abundant yolk protein production in egg-laying species, an energetically costly process under extensive transcriptional control. Here, we used the model organism Caenorhabditis elegans to provide evidence for the spatiotemporally defined interaction of two evolutionarily conserved transcription factors, CEH-60/PBX and UNC-62/MEIS, acting as a gateway to yolk protein production. Via proteomics, bimolecular fluorescence complementation (BiFC), and biochemical and functional readouts, we show that this interaction occurs in the intestine of animals at the onset of sexual maturity and suffices to support the reproductive program. Our electron micrographs and functional assays provide evidence that intestinal PBX/MEIS cooperation drives another process that depends on lipid mobilization: the formation of an impermeable epicuticle. Without this lipid-rich protective layer, mutant animals are hypersensitive to exogenous oxidative stress and are poor partners for mating. Dedicated communication between the hypodermis and intestine in C. elegans likely supports these physiological outcomes, and we propose a fundamental role for the conserved PBX/MEIS interaction in multicellular signaling networks that rely on lipid homeostasis.</description><identifier>ISSN: 1545-7885</identifier><identifier>ISSN: 1544-9173</identifier><identifier>EISSN: 1545-7885</identifier><identifier>DOI: 10.1371/journal.pbio.3000499</identifier><identifier>PMID: 31675356</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Animals ; Biology and Life Sciences ; Caenorhabditis elegans ; Caenorhabditis elegans - genetics ; Caenorhabditis elegans - metabolism ; Caenorhabditis elegans - physiology ; Caenorhabditis elegans Proteins - genetics ; Caenorhabditis elegans Proteins - metabolism ; Caenorhabditis elegans Proteins - physiology ; Collagen - metabolism ; Complementation ; Cuticles ; Dehydrogenases ; DNA binding proteins ; Egg laying ; Electron micrographs ; Epicuticle ; Fluorescence ; Funding ; Gene expression ; Gene Expression Regulation, Developmental ; Homeodomain Proteins - genetics ; Homeodomain Proteins - metabolism ; Homeodomain Proteins - physiology ; Homeostasis ; Hypodermis ; Intestinal Mucosa - metabolism ; Intestine ; Intestines ; Kinases ; Leukemia ; Lipid Metabolism ; Lipids ; Medicine and Health Sciences ; Metabolism ; Neurobiology ; Neurons ; Neurosciences ; Oxidative Stress ; Permeability ; Physical Sciences ; Physiological aspects ; Physiology ; Proteins ; Proteomics ; Research and Analysis Methods ; Scientific equipment and supplies industry ; Sexual maturity ; Transcription Factors ; Transcription Factors, General - genetics ; Transcription Factors, General - metabolism ; Transcription Factors, General - physiology ; Vitellogenesis ; Vitellogenesis - genetics ; Yolk ; Yolk protein</subject><ispartof>PLoS biology, 2019-11, Vol.17 (11), p.e3000499-e3000499</ispartof><rights>COPYRIGHT 2019 Public Library of Science</rights><rights>2019 Van de Walle et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2019 Van de Walle et al 2019 Van de Walle et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c695t-1d799b0e812fa8e70e27f13f6137180f0dd3a85f3c2eb7404efdc4e44ecfe54a3</citedby><cites>FETCH-LOGICAL-c695t-1d799b0e812fa8e70e27f13f6137180f0dd3a85f3c2eb7404efdc4e44ecfe54a3</cites><orcidid>0000-0002-0661-931X ; 0000-0002-6020-7885 ; 0000-0003-3192-4428 ; 0000-0001-6117-2648 ; 0000-0002-1249-3995</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/2327547513/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/2327547513?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25753,27924,27925,37012,37013,44590,53791,53793,75126</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31675356$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Tissenbaum, Heidi A.</contributor><creatorcontrib>Van de Walle, Pieter</creatorcontrib><creatorcontrib>Geens, Ellen</creatorcontrib><creatorcontrib>Baggerman, Geert</creatorcontrib><creatorcontrib>José Naranjo-Galindo, Francisco</creatorcontrib><creatorcontrib>Askjaer, Peter</creatorcontrib><creatorcontrib>Schoofs, Liliane</creatorcontrib><creatorcontrib>Temmerman, Liesbet</creatorcontrib><title>CEH-60/PBX regulates vitellogenesis and cuticle permeability through intestinal interaction with UNC-62/MEIS in Caenorhabditis elegans</title><title>PLoS biology</title><addtitle>PLoS Biol</addtitle><description>The onset of sexual maturity involves dramatic changes in physiology and gene expression in many animals. 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These include abundant yolk protein production in egg-laying species, an energetically costly process under extensive transcriptional control. Here, we used the model organism Caenorhabditis elegans to provide evidence for the spatiotemporally defined interaction of two evolutionarily conserved transcription factors, CEH-60/PBX and UNC-62/MEIS, acting as a gateway to yolk protein production. Via proteomics, bimolecular fluorescence complementation (BiFC), and biochemical and functional readouts, we show that this interaction occurs in the intestine of animals at the onset of sexual maturity and suffices to support the reproductive program. Our electron micrographs and functional assays provide evidence that intestinal PBX/MEIS cooperation drives another process that depends on lipid mobilization: the formation of an impermeable epicuticle. Without this lipid-rich protective layer, mutant animals are hypersensitive to exogenous oxidative stress and are poor partners for mating. 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| ispartof | PLoS biology, 2019-11, Vol.17 (11), p.e3000499-e3000499 |
| issn | 1545-7885 1544-9173 1545-7885 |
| language | eng |
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| subjects | Animals Biology and Life Sciences Caenorhabditis elegans Caenorhabditis elegans - genetics Caenorhabditis elegans - metabolism Caenorhabditis elegans - physiology Caenorhabditis elegans Proteins - genetics Caenorhabditis elegans Proteins - metabolism Caenorhabditis elegans Proteins - physiology Collagen - metabolism Complementation Cuticles Dehydrogenases DNA binding proteins Egg laying Electron micrographs Epicuticle Fluorescence Funding Gene expression Gene Expression Regulation, Developmental Homeodomain Proteins - genetics Homeodomain Proteins - metabolism Homeodomain Proteins - physiology Homeostasis Hypodermis Intestinal Mucosa - metabolism Intestine Intestines Kinases Leukemia Lipid Metabolism Lipids Medicine and Health Sciences Metabolism Neurobiology Neurons Neurosciences Oxidative Stress Permeability Physical Sciences Physiological aspects Physiology Proteins Proteomics Research and Analysis Methods Scientific equipment and supplies industry Sexual maturity Transcription Factors Transcription Factors, General - genetics Transcription Factors, General - metabolism Transcription Factors, General - physiology Vitellogenesis Vitellogenesis - genetics Yolk Yolk protein |
| title | CEH-60/PBX regulates vitellogenesis and cuticle permeability through intestinal interaction with UNC-62/MEIS in Caenorhabditis elegans |
| url | http://sfxeu10.hosted.exlibrisgroup.com/loughborough?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-27T05%3A46%3A38IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=CEH-60/PBX%20regulates%20vitellogenesis%20and%20cuticle%20permeability%20through%20intestinal%20interaction%20with%20UNC-62/MEIS%20in%20Caenorhabditis%20elegans&rft.jtitle=PLoS%20biology&rft.au=Van%20de%20Walle,%20Pieter&rft.date=2019-11-01&rft.volume=17&rft.issue=11&rft.spage=e3000499&rft.epage=e3000499&rft.pages=e3000499-e3000499&rft.issn=1545-7885&rft.eissn=1545-7885&rft_id=info:doi/10.1371/journal.pbio.3000499&rft_dat=%3Cgale_plos_%3EA607431145%3C/gale_plos_%3E%3Cgrp_id%3Ecdi_FETCH-LOGICAL-c695t-1d799b0e812fa8e70e27f13f6137180f0dd3a85f3c2eb7404efdc4e44ecfe54a3%3C/grp_id%3E%3Coa%3E%3C/oa%3E%3Curl%3E%3C/url%3E&rft_id=info:oai/&rft_pqid=2327547513&rft_id=info:pmid/31675356&rft_galeid=A607431145&rfr_iscdi=true |