Drosophila embryos allocate lipid droplets to specific lineages to ensure punctual development and redox homeostasis
Lipid droplets (LDs) are ubiquitous organelles that facilitate neutral lipid storage in cells, including energy-dense triglycerides. They are found in all investigated metazoan embryos where they are thought to provide energy for development. Intriguingly, early embryos of diverse metazoan species a...
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description | Lipid droplets (LDs) are ubiquitous organelles that facilitate neutral lipid storage in cells, including energy-dense triglycerides. They are found in all investigated metazoan embryos where they are thought to provide energy for development. Intriguingly, early embryos of diverse metazoan species asymmetrically allocate LDs amongst cellular lineages, a process which can involve massive intracellular redistribution of LDs. However, the biological reason for asymmetric lineage allocation is unknown. To address this issue, we utilize the Drosophila embryo where the cytoskeletal mechanisms that drive allocation are well characterized. We disrupt allocation by two different means: Loss of the LD protein Jabba results in LDs adhering inappropriately to glycogen granules; loss of Klar alters the activities of the microtubule motors that move LDs. Both mutants cause the same dramatic change in LD tissue inheritance, shifting allocation of the majority of LDs to the yolk cell instead of the incipient epithelium. Embryos with such mislocalized LDs do not fully consume their LDs and are delayed in hatching. Through use of a dPLIN2 mutant, which appropriately localizes a smaller pool of LDs, we find that failed LD transport and a smaller LD pool affect embryogenesis in a similar manner. Embryos of all three mutants display overlapping changes in their transcriptome and proteome, suggesting that lipid deprivation results in a shared embryonic response and a widespread change in metabolism. Excitingly, we find abundant changes related to redox homeostasis, with many proteins related to glutathione metabolism upregulated. LD deprived embryos have an increase in peroxidized lipids and rely on increased utilization of glutathione-related proteins for survival. Thus, embryos are apparently able to mount a beneficial response upon lipid stress, rewiring their metabolism to survive. In summary, we demonstrate that early embryos allocate LDs into specific lineages for subsequent optimal utilization, thus protecting against oxidative stress and ensuring punctual development. |
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They are found in all investigated metazoan embryos where they are thought to provide energy for development. Intriguingly, early embryos of diverse metazoan species asymmetrically allocate LDs amongst cellular lineages, a process which can involve massive intracellular redistribution of LDs. However, the biological reason for asymmetric lineage allocation is unknown. To address this issue, we utilize the Drosophila embryo where the cytoskeletal mechanisms that drive allocation are well characterized. We disrupt allocation by two different means: Loss of the LD protein Jabba results in LDs adhering inappropriately to glycogen granules; loss of Klar alters the activities of the microtubule motors that move LDs. Both mutants cause the same dramatic change in LD tissue inheritance, shifting allocation of the majority of LDs to the yolk cell instead of the incipient epithelium. Embryos with such mislocalized LDs do not fully consume their LDs and are delayed in hatching. Through use of a dPLIN2 mutant, which appropriately localizes a smaller pool of LDs, we find that failed LD transport and a smaller LD pool affect embryogenesis in a similar manner. Embryos of all three mutants display overlapping changes in their transcriptome and proteome, suggesting that lipid deprivation results in a shared embryonic response and a widespread change in metabolism. Excitingly, we find abundant changes related to redox homeostasis, with many proteins related to glutathione metabolism upregulated. LD deprived embryos have an increase in peroxidized lipids and rely on increased utilization of glutathione-related proteins for survival. Thus, embryos are apparently able to mount a beneficial response upon lipid stress, rewiring their metabolism to survive. In summary, we demonstrate that early embryos allocate LDs into specific lineages for subsequent optimal utilization, thus protecting against oxidative stress and ensuring punctual development.</description><identifier>ISSN: 1553-7404</identifier><identifier>ISSN: 1553-7390</identifier><identifier>EISSN: 1553-7404</identifier><identifier>DOI: 10.1371/journal.pgen.1010875</identifier><identifier>PMID: 37578970</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Analysis ; Biology and Life Sciences ; Cell organelles ; Cytoskeleton ; Drosophila ; Embryogenesis ; Embryonic development ; Embryos ; Epithelium ; Glutathione ; Glycogen ; Growth ; Hatching ; Homeostasis ; Identification and classification ; Insects ; Lipid metabolism ; Lipid peroxidation ; Lipids ; Metabolism ; Mollusks ; Mutants ; Mutation ; Organelles ; Oxidative stress ; Physiological aspects ; Proteins ; Proteomes ; Research and Analysis Methods ; Transcriptomes ; Triglycerides</subject><ispartof>PLoS genetics, 2023-08, Vol.19 (8), p.e1010875</ispartof><rights>Copyright: © 2023 Kilwein et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</rights><rights>COPYRIGHT 2023 Public Library of Science</rights><rights>2023 Kilwein 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>2023 Kilwein et al 2023 Kilwein et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c655t-afa664fc41403dfc87733e0285d8fe057fae658727584728ad21cc209d05715e3</citedby><cites>FETCH-LOGICAL-c655t-afa664fc41403dfc87733e0285d8fe057fae658727584728ad21cc209d05715e3</cites><orcidid>0000-0002-1185-7881 ; 0000-0001-5741-4720</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10449164/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10449164/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79569,79570</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37578970$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kilwein, Marcus D</creatorcontrib><creatorcontrib>Dao, T Kim</creatorcontrib><creatorcontrib>Welte, Michael A</creatorcontrib><title>Drosophila embryos allocate lipid droplets to specific lineages to ensure punctual development and redox homeostasis</title><title>PLoS genetics</title><addtitle>PLoS Genet</addtitle><description>Lipid droplets (LDs) are ubiquitous organelles that facilitate neutral lipid storage in cells, including energy-dense triglycerides. They are found in all investigated metazoan embryos where they are thought to provide energy for development. Intriguingly, early embryos of diverse metazoan species asymmetrically allocate LDs amongst cellular lineages, a process which can involve massive intracellular redistribution of LDs. However, the biological reason for asymmetric lineage allocation is unknown. To address this issue, we utilize the Drosophila embryo where the cytoskeletal mechanisms that drive allocation are well characterized. We disrupt allocation by two different means: Loss of the LD protein Jabba results in LDs adhering inappropriately to glycogen granules; loss of Klar alters the activities of the microtubule motors that move LDs. Both mutants cause the same dramatic change in LD tissue inheritance, shifting allocation of the majority of LDs to the yolk cell instead of the incipient epithelium. Embryos with such mislocalized LDs do not fully consume their LDs and are delayed in hatching. Through use of a dPLIN2 mutant, which appropriately localizes a smaller pool of LDs, we find that failed LD transport and a smaller LD pool affect embryogenesis in a similar manner. Embryos of all three mutants display overlapping changes in their transcriptome and proteome, suggesting that lipid deprivation results in a shared embryonic response and a widespread change in metabolism. Excitingly, we find abundant changes related to redox homeostasis, with many proteins related to glutathione metabolism upregulated. LD deprived embryos have an increase in peroxidized lipids and rely on increased utilization of glutathione-related proteins for survival. Thus, embryos are apparently able to mount a beneficial response upon lipid stress, rewiring their metabolism to survive. In summary, we demonstrate that early embryos allocate LDs into specific lineages for subsequent optimal utilization, thus protecting against oxidative stress and ensuring punctual development.</description><subject>Analysis</subject><subject>Biology and Life Sciences</subject><subject>Cell organelles</subject><subject>Cytoskeleton</subject><subject>Drosophila</subject><subject>Embryogenesis</subject><subject>Embryonic development</subject><subject>Embryos</subject><subject>Epithelium</subject><subject>Glutathione</subject><subject>Glycogen</subject><subject>Growth</subject><subject>Hatching</subject><subject>Homeostasis</subject><subject>Identification and classification</subject><subject>Insects</subject><subject>Lipid metabolism</subject><subject>Lipid peroxidation</subject><subject>Lipids</subject><subject>Metabolism</subject><subject>Mollusks</subject><subject>Mutants</subject><subject>Mutation</subject><subject>Organelles</subject><subject>Oxidative stress</subject><subject>Physiological aspects</subject><subject>Proteins</subject><subject>Proteomes</subject><subject>Research and Analysis Methods</subject><subject>Transcriptomes</subject><subject>Triglycerides</subject><issn>1553-7404</issn><issn>1553-7390</issn><issn>1553-7404</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNqVkltr3DAQhU1padK0_6C0hkKhD7uVbMnyPpWQ3hZCA729illp5FXQWo4kh-TfV5t1wu5DoX3SoPnmaHQ4RfGSkjmtBX1_6cfQg5sPHfZzSihpBX9UHFPO65lghD3eq4-KZzFeElLzdiGeFke14CJX5LhIH4OPflhbByVuVuHWxxKc8woSls4OVpc6-MFhimXyZRxQWWNVbvUIHd5dYh_HgOUw9iqN4EqN1-j8sME-ldDrMqD2N-Xab9DHBNHG58UTAy7ii-k8KX59_vTz7Ovs_OLL8uz0fKYaztMMDDQNM4pRRmptVCtEXSOpWq5bg4QLA9jwVlSCt0xULeiKKlWRhc49yrE-KV7vdAfno5wMi7JqszzhC8EzsdwR2sOlHILdQLiVHqy8u_ChkxCSVQ5lxRQzDRqRF2INbaFdUbEwnGhApbnKWh-m18bVBrXK3w_gDkQPO71dy85fS0oYW9CGZYU3k0LwVyPG9JedJ6qDvJbtjc9qamOjkqeiqUVDGN1S7w4o5fuEN6mDMUa5_PH9P9hv_85e_D5k3-6xawSX1tG7MVnfx0OQ7UCV0xgDmgfXKJHbtN8bIbdpl1Pa89irfccfhu7jXf8Br4T8NA</recordid><startdate>20230814</startdate><enddate>20230814</enddate><creator>Kilwein, Marcus D</creator><creator>Dao, T Kim</creator><creator>Welte, Michael A</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>IOV</scope><scope>ISN</scope><scope>ISR</scope><scope>3V.</scope><scope>7QP</scope><scope>7QR</scope><scope>7SS</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>P64</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>RC3</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0002-1185-7881</orcidid><orcidid>https://orcid.org/0000-0001-5741-4720</orcidid></search><sort><creationdate>20230814</creationdate><title>Drosophila embryos allocate lipid droplets to specific lineages to ensure punctual development and redox homeostasis</title><author>Kilwein, Marcus D ; Dao, T Kim ; Welte, Michael A</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c655t-afa664fc41403dfc87733e0285d8fe057fae658727584728ad21cc209d05715e3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Analysis</topic><topic>Biology and Life Sciences</topic><topic>Cell organelles</topic><topic>Cytoskeleton</topic><topic>Drosophila</topic><topic>Embryogenesis</topic><topic>Embryonic development</topic><topic>Embryos</topic><topic>Epithelium</topic><topic>Glutathione</topic><topic>Glycogen</topic><topic>Growth</topic><topic>Hatching</topic><topic>Homeostasis</topic><topic>Identification and classification</topic><topic>Insects</topic><topic>Lipid metabolism</topic><topic>Lipid peroxidation</topic><topic>Lipids</topic><topic>Metabolism</topic><topic>Mollusks</topic><topic>Mutants</topic><topic>Mutation</topic><topic>Organelles</topic><topic>Oxidative stress</topic><topic>Physiological aspects</topic><topic>Proteins</topic><topic>Proteomes</topic><topic>Research and Analysis Methods</topic><topic>Transcriptomes</topic><topic>Triglycerides</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kilwein, Marcus D</creatorcontrib><creatorcontrib>Dao, T Kim</creatorcontrib><creatorcontrib>Welte, Michael A</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Opposing Viewpoints</collection><collection>Gale In Context: Canada</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Publicly Available Content (ProQuest)</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>Genetics Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS genetics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kilwein, Marcus D</au><au>Dao, T Kim</au><au>Welte, Michael A</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Drosophila embryos allocate lipid droplets to specific lineages to ensure punctual development and redox homeostasis</atitle><jtitle>PLoS genetics</jtitle><addtitle>PLoS Genet</addtitle><date>2023-08-14</date><risdate>2023</risdate><volume>19</volume><issue>8</issue><spage>e1010875</spage><pages>e1010875-</pages><issn>1553-7404</issn><issn>1553-7390</issn><eissn>1553-7404</eissn><abstract>Lipid droplets (LDs) are ubiquitous organelles that facilitate neutral lipid storage in cells, including energy-dense triglycerides. They are found in all investigated metazoan embryos where they are thought to provide energy for development. Intriguingly, early embryos of diverse metazoan species asymmetrically allocate LDs amongst cellular lineages, a process which can involve massive intracellular redistribution of LDs. However, the biological reason for asymmetric lineage allocation is unknown. To address this issue, we utilize the Drosophila embryo where the cytoskeletal mechanisms that drive allocation are well characterized. We disrupt allocation by two different means: Loss of the LD protein Jabba results in LDs adhering inappropriately to glycogen granules; loss of Klar alters the activities of the microtubule motors that move LDs. Both mutants cause the same dramatic change in LD tissue inheritance, shifting allocation of the majority of LDs to the yolk cell instead of the incipient epithelium. Embryos with such mislocalized LDs do not fully consume their LDs and are delayed in hatching. Through use of a dPLIN2 mutant, which appropriately localizes a smaller pool of LDs, we find that failed LD transport and a smaller LD pool affect embryogenesis in a similar manner. Embryos of all three mutants display overlapping changes in their transcriptome and proteome, suggesting that lipid deprivation results in a shared embryonic response and a widespread change in metabolism. Excitingly, we find abundant changes related to redox homeostasis, with many proteins related to glutathione metabolism upregulated. LD deprived embryos have an increase in peroxidized lipids and rely on increased utilization of glutathione-related proteins for survival. Thus, embryos are apparently able to mount a beneficial response upon lipid stress, rewiring their metabolism to survive. In summary, we demonstrate that early embryos allocate LDs into specific lineages for subsequent optimal utilization, thus protecting against oxidative stress and ensuring punctual development.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>37578970</pmid><doi>10.1371/journal.pgen.1010875</doi><tpages>e1010875</tpages><orcidid>https://orcid.org/0000-0002-1185-7881</orcidid><orcidid>https://orcid.org/0000-0001-5741-4720</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Analysis Biology and Life Sciences Cell organelles Cytoskeleton Drosophila Embryogenesis Embryonic development Embryos Epithelium Glutathione Glycogen Growth Hatching Homeostasis Identification and classification Insects Lipid metabolism Lipid peroxidation Lipids Metabolism Mollusks Mutants Mutation Organelles Oxidative stress Physiological aspects Proteins Proteomes Research and Analysis Methods Transcriptomes Triglycerides |
title | Drosophila embryos allocate lipid droplets to specific lineages to ensure punctual development and redox homeostasis |
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