Membrane dynamics of ATG4B and LC3 in autophagosome formation
Abstract The biogenesis of autophagosomes provides the basis for macroautophagy to capture and degrade intracellular cargoes. Binding of the autophagy-related protein ATG8/LC3 to autophagic membranes is essential to autophagosome formation, which involves the specific and dynamic processing of ATG8/...
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Veröffentlicht in: | Journal of molecular cell biology 2022-01, Vol.13 (12), p.853-863 |
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creator | Zhou, Yuanyuan Wang, Zhenkun Huang, Yijia Bai, Chujie Zhang, Xianli Fang, Mengdie Ju, Zhenyu Liu, Bo |
description | Abstract
The biogenesis of autophagosomes provides the basis for macroautophagy to capture and degrade intracellular cargoes. Binding of the autophagy-related protein ATG8/LC3 to autophagic membranes is essential to autophagosome formation, which involves the specific and dynamic processing of ATG8/LC3 by cysteine protease ATG4. However, to date, the mechanism whereby ATG4 is recruited to the membranes, the interaction of ATG4 and ATG8/LC3 on the membranes, and its role in the growth of phagophore are not completely understood. Here, we used fluorescence recovery after photobleaching to monitor the turnover of GFP-tagged ATG4B and LC3B in living animal cells. The data show that ATG4B localizes to early autophagic membranes in an LC3B-dependent manner. During autophagy, ATG4B and LC3B undergo rapid cytosol/isolation membrane exchange but not at the cytosol/completed autophagosome. In addition, ATG4B activity controls the efficiency of autophagosome formation by impacting the membrane binding/dissociation of LC3B. These data suggest that ATG4 and LC3 play interdependent roles in the formation of autophagosomes. |
doi_str_mv | 10.1093/jmcb/mjab059 |
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The biogenesis of autophagosomes provides the basis for macroautophagy to capture and degrade intracellular cargoes. Binding of the autophagy-related protein ATG8/LC3 to autophagic membranes is essential to autophagosome formation, which involves the specific and dynamic processing of ATG8/LC3 by cysteine protease ATG4. However, to date, the mechanism whereby ATG4 is recruited to the membranes, the interaction of ATG4 and ATG8/LC3 on the membranes, and its role in the growth of phagophore are not completely understood. Here, we used fluorescence recovery after photobleaching to monitor the turnover of GFP-tagged ATG4B and LC3B in living animal cells. The data show that ATG4B localizes to early autophagic membranes in an LC3B-dependent manner. During autophagy, ATG4B and LC3B undergo rapid cytosol/isolation membrane exchange but not at the cytosol/completed autophagosome. In addition, ATG4B activity controls the efficiency of autophagosome formation by impacting the membrane binding/dissociation of LC3B. These data suggest that ATG4 and LC3 play interdependent roles in the formation of autophagosomes.</description><identifier>ISSN: 1759-4685</identifier><identifier>ISSN: 1674-2788</identifier><identifier>EISSN: 1759-4685</identifier><identifier>DOI: 10.1093/jmcb/mjab059</identifier><identifier>PMID: 34562084</identifier><language>eng</language><publisher>United States: Oxford University Press</publisher><subject>Animals ; Autophagosomes - metabolism ; Autophagy ; Autophagy-Related Proteins - metabolism ; Macroautophagy ; Microtubule-Associated Proteins - metabolism</subject><ispartof>Journal of molecular cell biology, 2022-01, Vol.13 (12), p.853-863</ispartof><rights>The Author(s) (2021). Published by Oxford University Press on behalf of Journal of Molecular Cell Biology , CEMCS, CAS. 2021</rights><rights>The Author(s) (2021). Published by Oxford University Press on behalf of Journal of Molecular Cell Biology, CEMCS, CAS.</rights><rights>The Author(s) (2021). Published by Oxford University Press on behalf of , CEMCS, CAS. 2021</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c416t-9669fa74ed7128721226921357a48980687c3e39d777fa431e400a2310cdc4bb3</citedby><cites>FETCH-LOGICAL-c416t-9669fa74ed7128721226921357a48980687c3e39d777fa431e400a2310cdc4bb3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8800521/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8800521/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,1604,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34562084$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Zhou, Yuanyuan</creatorcontrib><creatorcontrib>Wang, Zhenkun</creatorcontrib><creatorcontrib>Huang, Yijia</creatorcontrib><creatorcontrib>Bai, Chujie</creatorcontrib><creatorcontrib>Zhang, Xianli</creatorcontrib><creatorcontrib>Fang, Mengdie</creatorcontrib><creatorcontrib>Ju, Zhenyu</creatorcontrib><creatorcontrib>Liu, Bo</creatorcontrib><title>Membrane dynamics of ATG4B and LC3 in autophagosome formation</title><title>Journal of molecular cell biology</title><addtitle>J Mol Cell Biol</addtitle><description>Abstract
The biogenesis of autophagosomes provides the basis for macroautophagy to capture and degrade intracellular cargoes. Binding of the autophagy-related protein ATG8/LC3 to autophagic membranes is essential to autophagosome formation, which involves the specific and dynamic processing of ATG8/LC3 by cysteine protease ATG4. However, to date, the mechanism whereby ATG4 is recruited to the membranes, the interaction of ATG4 and ATG8/LC3 on the membranes, and its role in the growth of phagophore are not completely understood. Here, we used fluorescence recovery after photobleaching to monitor the turnover of GFP-tagged ATG4B and LC3B in living animal cells. The data show that ATG4B localizes to early autophagic membranes in an LC3B-dependent manner. During autophagy, ATG4B and LC3B undergo rapid cytosol/isolation membrane exchange but not at the cytosol/completed autophagosome. In addition, ATG4B activity controls the efficiency of autophagosome formation by impacting the membrane binding/dissociation of LC3B. These data suggest that ATG4 and LC3 play interdependent roles in the formation of autophagosomes.</description><subject>Animals</subject><subject>Autophagosomes - metabolism</subject><subject>Autophagy</subject><subject>Autophagy-Related Proteins - metabolism</subject><subject>Macroautophagy</subject><subject>Microtubule-Associated Proteins - metabolism</subject><issn>1759-4685</issn><issn>1674-2788</issn><issn>1759-4685</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>TOX</sourceid><sourceid>EIF</sourceid><recordid>eNp9kE1PwkAQhjdGIwS5eTZ782Jlt7vdj4MmSBRNMF7wvJlut1DCdpu2kPDvLQEJXpzLTDLPvJM8CN1S8kiJZqOVt-nIryAlib5AfSoTHXGhksuzuYeGTbMiXTHFmCLXqMd4ImKieB89fTqf1lA6nO1K8IVtcMjxeD7lLxjKDM8mDBclhk0bqiUsQhO8w3moPbRFKG_QVQ7rxg2PfYC-317nk_do9jX9mIxnkeVUtJEWQucgucskjZWMaRwLHVOWSOBKKyKUtMwxnUkpc-CMOk4IxIwSm1mepmyAng-51Sb1LrOubGtYm6ouPNQ7E6AwfzdlsTSLsDVKEZJ0nwbo4RBg69A0tctPt5SYvUmzN2mOJjv87vzfCf711gH3ByBsqv-jfgDdgHx8</recordid><startdate>20220129</startdate><enddate>20220129</enddate><creator>Zhou, Yuanyuan</creator><creator>Wang, Zhenkun</creator><creator>Huang, Yijia</creator><creator>Bai, Chujie</creator><creator>Zhang, Xianli</creator><creator>Fang, Mengdie</creator><creator>Ju, Zhenyu</creator><creator>Liu, Bo</creator><general>Oxford University Press</general><scope>TOX</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>5PM</scope></search><sort><creationdate>20220129</creationdate><title>Membrane dynamics of ATG4B and LC3 in autophagosome formation</title><author>Zhou, Yuanyuan ; Wang, Zhenkun ; Huang, Yijia ; Bai, Chujie ; Zhang, Xianli ; Fang, Mengdie ; Ju, Zhenyu ; Liu, Bo</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c416t-9669fa74ed7128721226921357a48980687c3e39d777fa431e400a2310cdc4bb3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Animals</topic><topic>Autophagosomes - metabolism</topic><topic>Autophagy</topic><topic>Autophagy-Related Proteins - metabolism</topic><topic>Macroautophagy</topic><topic>Microtubule-Associated Proteins - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Zhou, Yuanyuan</creatorcontrib><creatorcontrib>Wang, Zhenkun</creatorcontrib><creatorcontrib>Huang, Yijia</creatorcontrib><creatorcontrib>Bai, Chujie</creatorcontrib><creatorcontrib>Zhang, Xianli</creatorcontrib><creatorcontrib>Fang, Mengdie</creatorcontrib><creatorcontrib>Ju, Zhenyu</creatorcontrib><creatorcontrib>Liu, Bo</creatorcontrib><collection>Oxford Journals Open Access Collection</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Journal of molecular cell biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zhou, Yuanyuan</au><au>Wang, Zhenkun</au><au>Huang, Yijia</au><au>Bai, Chujie</au><au>Zhang, Xianli</au><au>Fang, Mengdie</au><au>Ju, Zhenyu</au><au>Liu, Bo</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Membrane dynamics of ATG4B and LC3 in autophagosome formation</atitle><jtitle>Journal of molecular cell biology</jtitle><addtitle>J Mol Cell Biol</addtitle><date>2022-01-29</date><risdate>2022</risdate><volume>13</volume><issue>12</issue><spage>853</spage><epage>863</epage><pages>853-863</pages><issn>1759-4685</issn><issn>1674-2788</issn><eissn>1759-4685</eissn><abstract>Abstract
The biogenesis of autophagosomes provides the basis for macroautophagy to capture and degrade intracellular cargoes. Binding of the autophagy-related protein ATG8/LC3 to autophagic membranes is essential to autophagosome formation, which involves the specific and dynamic processing of ATG8/LC3 by cysteine protease ATG4. However, to date, the mechanism whereby ATG4 is recruited to the membranes, the interaction of ATG4 and ATG8/LC3 on the membranes, and its role in the growth of phagophore are not completely understood. Here, we used fluorescence recovery after photobleaching to monitor the turnover of GFP-tagged ATG4B and LC3B in living animal cells. The data show that ATG4B localizes to early autophagic membranes in an LC3B-dependent manner. During autophagy, ATG4B and LC3B undergo rapid cytosol/isolation membrane exchange but not at the cytosol/completed autophagosome. In addition, ATG4B activity controls the efficiency of autophagosome formation by impacting the membrane binding/dissociation of LC3B. These data suggest that ATG4 and LC3 play interdependent roles in the formation of autophagosomes.</abstract><cop>United States</cop><pub>Oxford University Press</pub><pmid>34562084</pmid><doi>10.1093/jmcb/mjab059</doi><tpages>11</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Animals Autophagosomes - metabolism Autophagy Autophagy-Related Proteins - metabolism Macroautophagy Microtubule-Associated Proteins - metabolism |
title | Membrane dynamics of ATG4B and LC3 in autophagosome formation |
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