{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,10]],"date-time":"2026-03-10T04:50:21Z","timestamp":1773118221698,"version":"3.50.1"},"reference-count":32,"publisher":"The Company of Biologists","issue":"3","license":[{"start":{"date-parts":[[2024,2,1]],"date-time":"2024-02-01T00:00:00Z","timestamp":1706745600000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/www.biologists.com\/user-licence-1-1\/"}],"funder":[{"name":"National Key Research and Development Program of China","award":["2023YFA1801100"],"award-info":[{"award-number":["2023YFA1801100"]}]},{"DOI":"10.13039\/501100001809","name":"Natural Science Foundation of China","doi-asserted-by":"crossref","award":["32070694"],"award-info":[{"award-number":["32070694"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100001809","name":"Natural Science Foundation of China","doi-asserted-by":"crossref","award":["32270774"],"award-info":[{"award-number":["32270774"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2024,2,1]]},"abstract":"<jats:title>ABSTRACT<\/jats:title>\n               <jats:p>Mitochondria are the powerhouses of many biological processes. During spermatogenesis, post-transcriptional regulation of mitochondrial gene expression is mediated by nuclear-encoded mitochondrial RNA-binding proteins (mtRBPs). We identified AMG-1 as an mtRBP required for reproductive success in Caenorhabditis elegans. amg-1 mutation led to defects in mitochondrial structure and sperm budding, resulting in mitochondria being discarded into residual bodies, which ultimately delayed spermatogenesis in the proximal gonad. In addition, mitochondrial defects triggered the gonadal mitochondrial unfolded protein response and phagocytic clearance to ensure spermatogenesis but ultimately failed to rescue hermaphroditic fertility. These findings reveal a previously undiscovered role for AMG-1 in regulating C. elegans spermatogenesis, in which mitochondrial-damaged sperm prevented the transmission of defective mitochondria to mature sperm by budding and phagocytic clearance, a process which may also exist in the reproductive systems of higher organisms.<\/jats:p>","DOI":"10.1242\/dev.202165","type":"journal-article","created":{"date-parts":[[2024,1,15]],"date-time":"2024-01-15T10:40:35Z","timestamp":1705315235000},"source":"Crossref","is-referenced-by-count":8,"title":["Mitochondrial defects triggered by <i>amg-1<\/i> mutation elicit UPRmt and phagocytic clearance during spermatogenesis in <i>C. elegans<\/i>"],"prefix":"10.1242","volume":"151","author":[{"ORCID":"https:\/\/orcid.org\/0009-0005-5686-0995","authenticated-orcid":false,"given":"Peng","family":"Wang","sequence":"first","affiliation":[{"name":"CAS Center for Excellence in Biomacromolecules, Institute of Biophysics, Chinese Academy of Sciences 1 Key Laboratory of RNA Biology , , Beijing 100101 , China"},{"name":"University of Chinese Academy of Sciences 2 , Beijing 100049 , China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Lianwan","family":"Chen","sequence":"additional","affiliation":[{"name":"CAS Center for Excellence in Biomacromolecules, Institute of Biophysics, Chinese Academy of Sciences 1 Key Laboratory of RNA Biology , , Beijing 100101 , China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ning","family":"Wang","sequence":"additional","affiliation":[{"name":"CAS Center for Excellence in Biomacromolecules, Institute of Biophysics, Chinese Academy of Sciences 1 Key Laboratory of RNA Biology , , Beijing 100101 , China"},{"name":"University of Chinese Academy of Sciences 2 , Beijing 100049 , China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0562-6681","authenticated-orcid":false,"given":"Long","family":"Miao","sequence":"additional","affiliation":[{"name":"CAS Center for Excellence in Biomacromolecules, Institute of Biophysics, Chinese Academy of Sciences 1 Key Laboratory of RNA Biology , , Beijing 100101 , China"},{"name":"University of Chinese Academy of Sciences 2 , Beijing 100049 , China"},{"name":", Core Facilities for Protein Science, Institute of Biophysics, Chinese Academy of Sciences 3 Center for Biological Imaging , Beijing 100101 , China"},{"name":"College of Life Sciences, Beijing Normal University 4 MOE Key Laboratory of Cell Proliferation and Regulation Biology , , Beijing 100875 , China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3294-6971","authenticated-orcid":false,"given":"Yanmei","family":"Zhao","sequence":"additional","affiliation":[{"name":"CAS Center for Excellence in Biomacromolecules, Institute of Biophysics, Chinese Academy of Sciences 1 Key Laboratory of RNA Biology , , Beijing 100101 , China"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"237","published-online":{"date-parts":[[2024,2,5]]},"reference":[{"key":"2024020510182733200_DEV202165C1","doi-asserted-by":"crossref","first-page":"e0125617","DOI":"10.1371\/journal.pone.0125617","article-title":"OXPHOS-mediated induction of NAD+ promotes complete oxidation of fatty acids and interdicts non-alcoholic fatty liver disease","volume":"10","author":"Akie","year":"2015","journal-title":"PLoS ONE"},{"key":"2024020510182733200_DEV202165C2","doi-asserted-by":"publisher","first-page":"71","DOI":"10.1093\/genetics\/77.1.71","article-title":"The genetics of Caenorhabditis elegans","volume":"77","author":"Brenner","year":"1974","journal-title":"Genetics"},{"key":"2024020510182733200_DEV202165C3","doi-asserted-by":"publisher","first-page":"183","DOI":"10.1136\/jmg.2010.081976","article-title":"LRPPRC mutations cause a phenotypically distinct form of Leigh syndrome with cytochrome c oxidase deficiency","volume":"48","author":"Debray","year":"2011","journal-title":"J. Med. Genet."},{"key":"2024020510182733200_DEV202165C4","doi-asserted-by":"publisher","first-page":"79","DOI":"10.1016\/j.cell.2010.12.016","article-title":"The cell-non-autonomous nature of electron transport chain-mediated longevity","volume":"144","author":"Durieux","year":"2011","journal-title":"Cell"},{"key":"2024020510182733200_DEV202165C5","doi-asserted-by":"publisher","DOI":"10.1895\/wormbook.1.145.1","article-title":"Germline survival and apoptosis","author":"Gartner","year":"2018","journal-title":"WormBook"},{"key":"2024020510182733200_DEV202165C6","doi-asserted-by":"publisher","first-page":"1011","DOI":"10.1242\/dev.126.5.1011","article-title":"Genetic control of programmed cell death in the Caenorhabditis elegans hermaphrodite germline","volume":"126","author":"Gumienny","year":"1999","journal-title":"Development"},{"key":"2024020510182733200_DEV202165C7","doi-asserted-by":"publisher","first-page":"529","DOI":"10.1016\/j.molcel.2010.01.015","article-title":"The matrix peptide exporter HAF-1 signals a mitochondrial UPR by activating the transcription factor ZC376. 7 in C. elegans","volume":"37","author":"Haynes","year":"2010","journal-title":"Mol. Cell"},{"key":"2024020510182733200_DEV202165C8","doi-asserted-by":"publisher","first-page":"311","DOI":"10.1016\/j.tcb.2013.02.002","article-title":"Evaluating and responding to mitochondrial dysfunction: the mitochondrial unfolded-protein response and beyond","volume":"23","author":"Haynes","year":"2013","journal-title":"Trends Cell Biol."},{"key":"2024020510182733200_DEV202165C9","doi-asserted-by":"publisher","first-page":"43","DOI":"10.1093\/genetics\/103.1.43","article-title":"Male phenotypes and mating efficiency in Caenorhabditis elegans","volume":"103","author":"Hodgkin","year":"1983","journal-title":"Genetics"},{"key":"2024020510182733200_DEV202165C10","doi-asserted-by":"publisher","first-page":"477","DOI":"10.1016\/j.cub.2010.01.062","article-title":"Engulfment of apoptotic cells in C. elegans is mediated by integrin alpha\/SRC signaling","volume":"20","author":"Hsu","year":"2010","journal-title":"Curr. Biol."},{"key":"2024020510182733200_DEV202165C11","doi-asserted-by":"publisher","first-page":"4613","DOI":"10.1242\/dev.086769","article-title":"Residual body removal during spermatogenesis in C. elegans requires genes that mediate cell corpse clearance","volume":"139","author":"Huang","year":"2012","journal-title":"Development"},{"key":"2024020510182733200_DEV202165C12","doi-asserted-by":"publisher","first-page":"137","DOI":"10.1242\/jeb.090738","article-title":"The mitochondrial unfolded protein response, a conserved stress response pathway with implications in health and disease","volume":"217","author":"Jovaisaite","year":"2014","journal-title":"J. Exp. Biol."},{"key":"2024020510182733200_DEV202165C13","doi-asserted-by":"crossref","first-page":"270","DOI":"10.3389\/fphys.2016.00270","article-title":"Increased hepatic fatty acids uptake and oxidation by LRPPRC-driven oxidative phosphorylation reduces blood lipid levels","volume":"7","author":"Lei","year":"2016","journal-title":"Front. Physiol."},{"key":"2024020510182733200_DEV202165C14","doi-asserted-by":"publisher","first-page":"95","DOI":"10.1038\/35083620","article-title":"Endonuclease G is an apoptotic DNase when released from mitochondria","volume":"412","author":"Li","year":"2001","journal-title":"Nature"},{"key":"2024020510182733200_DEV202165C15","doi-asserted-by":"publisher","first-page":"41253","DOI":"10.1074\/jbc.M111.276121","article-title":"LRP130 protein remodels mitochondria and stimulates fatty acid oxidation","volume":"286","author":"Liu","year":"2011","journal-title":"J. Biol. Chem."},{"key":"2024020510182733200_DEV202165C16","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1006\/dbio.1996.9999","article-title":"A novel chloride channel localizes to Caenorhabditis elegans spermatids and chloride channel blockers induce spermatid differentiation","volume":"176","author":"Machaca","year":"1996","journal-title":"Dev. Biol."},{"key":"2024020510182733200_DEV202165C17","doi-asserted-by":"publisher","first-page":"4972","DOI":"10.1128\/MCB.23.14.4972-4982.2003","article-title":"LRP130, a pentatricopeptide motif protein with a noncanonical RNA-binding domain, is bound in vivo to mitochondrial and nuclear RNAs","volume":"23","author":"Mili","year":"2003","journal-title":"Mol. Cell. Biol."},{"key":"2024020510182733200_DEV202165C18","doi-asserted-by":"publisher","first-page":"605","DOI":"10.1073\/pnas.242716699","article-title":"Identification of a gene causing human cytochrome c oxidase deficiency by integrative genomics","volume":"100","author":"Mootha","year":"2003","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2024020510182733200_DEV202165C19","doi-asserted-by":"publisher","first-page":"587","DOI":"10.1126\/science.1223560","article-title":"Mitochondrial import efficiency of ATFS-1 regulates mitochondrial UPR activation","volume":"337","author":"Nargund","year":"2012","journal-title":"Science"},{"key":"2024020510182733200_DEV202165C20","doi-asserted-by":"publisher","first-page":"90","DOI":"10.1038\/35083608","article-title":"Mitochondrial endonuclease G is important for apoptosis in C. elegans","volume":"412","author":"Parrish","year":"2001","journal-title":"Nature"},{"key":"2024020510182733200_DEV202165C21","doi-asserted-by":"publisher","first-page":"171","DOI":"10.1038\/nprot.2014.006","article-title":"Full-length RNA-seq from single cells using Smart-seq2","volume":"9","author":"Picelli","year":"2014","journal-title":"Nat. Protocol."},{"key":"2024020510182733200_DEV202165C22","doi-asserted-by":"publisher","first-page":"153","DOI":"10.1038\/sj.cdd.4401539","article-title":"C. elegans ced-13 can promote apoptosis and is induced in response to DNA damage","volume":"12","author":"Schumacher","year":"2005","journal-title":"Cell Death Differ."},{"key":"2024020510182733200_DEV202165C23","doi-asserted-by":"publisher","first-page":"541","DOI":"10.1038\/ncb1574","article-title":"C. elegans mitochondrial factor WAH-1 promotes phosphatidylserine externalization in apoptotic cells through phospholipid scramblase SCRM-1","volume":"9","author":"Wang","year":"2007","journal-title":"Nat. Cell Biol."},{"key":"2024020510182733200_DEV202165C24","doi-asserted-by":"publisher","first-page":"1631","DOI":"10.1016\/j.devcel.2021.05.002","article-title":"Membrane contact site-dependent cholesterol transport regulates Na+\/K+-ATPase polarization and spermiogenesis in Caenorhabditis elegans","volume":"56","author":"Wang","year":"2021","journal-title":"Dev. Cell"},{"key":"2024020510182733200_DEV202165C25","doi-asserted-by":"publisher","first-page":"1399","DOI":"10.1016\/j.scib.2023.05.029","article-title":"RNA-binding protein complex AMG-1\/SLRP-1 mediates germline development and spermatogenesis by maintaining mitochondrial homeostasis in Caenorhabditis elegans","volume":"68","author":"Wang","year":"2023","journal-title":"Sci. Bull."},{"key":"2024020510182733200_DEV202165C32","doi-asserted-by":"publisher","first-page":"102720","DOI":"10.1016\/j.xpro.2023.102720","article-title":"Protocol for CRISPR-Cas9-mediated genome editing to study spermatogenesis in Caenorhabditis elegans","volume":"4","author":"Wang","year":"2023","journal-title":"STAR Protoc"},{"key":"2024020510182733200_DEV202165C26","first-page":"75","article-title":"The asymmetric localization of gene products during the development of Caenorhabditis elegans spermatozoa","volume":"55","author":"Ward","year":"1986","journal-title":"Gametogenesis and the Early Embryo"},{"key":"2024020510182733200_DEV202165C27","doi-asserted-by":"publisher","first-page":"70","DOI":"10.1016\/0012-1606(83)90336-6","article-title":"The initiation of spermiogenesis in the nematode Caenorhabditis elegans","volume":"98","author":"Ward","year":"1983","journal-title":"Dev. Biol."},{"key":"2024020510182733200_DEV202165C28","doi-asserted-by":"publisher","first-page":"331","DOI":"10.1042\/BJ20040469","article-title":"The role of the LRPPRC (leucine-rich pentatricopeptide repeat cassette) gene in cytochrome oxidase assembly: mutation causes lowered levels of COX (cytochrome c oxidase) I and COX III mRNA","volume":"382","author":"Xu","year":"2004","journal-title":"Biochem. J."},{"key":"2024020510182733200_DEV202165C29","doi-asserted-by":"publisher","first-page":"4055","DOI":"10.1242\/jcs.01275","article-title":"Compartment-specific perturbation of protein handling activates genes encoding mitochondrial chaperones","volume":"117","author":"Yoneda","year":"2004","journal-title":"J. Cell Sci."},{"key":"2024020510182733200_DEV202165C30","doi-asserted-by":"publisher","first-page":"870","DOI":"10.1016\/j.cell.2018.06.029","article-title":"The mitochondrial unfolded protein response is mediated cell-non-autonomously by retromer-dependent Wnt signaling","volume":"174","author":"Zhang","year":"2018","journal-title":"Cell"},{"key":"2024020510182733200_DEV202165C31","doi-asserted-by":"publisher","first-page":"4411","DOI":"10.1093\/emboj\/cdf445","article-title":"A mitochondrial specific stress response in mammalian cells","volume":"21","author":"Zhao","year":"2002","journal-title":"EMBO J."}],"container-title":["Development"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/journals.biologists.com\/dev\/article-pdf\/doi\/10.1242\/dev.202165\/3356836\/dev202165.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/journals.biologists.com\/dev\/article-pdf\/doi\/10.1242\/dev.202165\/3361790\/dev202165.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/journals.biologists.com\/dev\/article-pdf\/doi\/10.1242\/dev.202165\/3361790\/dev202165.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,2,5]],"date-time":"2024-02-05T10:18:40Z","timestamp":1707128320000},"score":1,"resource":{"primary":{"URL":"https:\/\/journals.biologists.com\/dev\/article\/151\/3\/dev202165\/342710\/Mitochondrial-defects-triggered-by-amg-1-mutation"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,2,1]]},"references-count":32,"journal-issue":{"issue":"3","published-print":{"date-parts":[[2024,2,1]]}},"URL":"https:\/\/doi.org\/10.1242\/dev.202165","relation":{},"ISSN":["0950-1991","1477-9129"],"issn-type":[{"value":"0950-1991","type":"print"},{"value":"1477-9129","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,2,1]]},"article-number":"dev202165"}}