Elucidation of the pluripotent potential of bovine embryonic lineages facilitates the establishment of formative stem cell lines | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Research Article Elucidation of the pluripotent potential of bovine embryonic lineages facilitates the establishment of formative stem cell lines Minglei Zhi, Dengfeng Gao, Yixuan Yao, Zimo Zhao, Yingjie Wang, and 21 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-4649336/v1 This work is licensed under a CC BY 4.0 License Status: Published Journal Publication published 08 Oct, 2024 Read the published version in Cellular and Molecular Life Sciences → Version 1 posted 5 You are reading this latest preprint version Abstract The establishment of epiblast-derived pluripotent stem cells (PSCs) from cattle, which are important domestic animals that provide humans with milk and meat while also serving as bioreactors for producing valuable proteins, poses a challenge due to the unclear molecular signaling required for embryonic epiblast development and maintenance of PSC self-renewal. Here, we selected six key stages of bovine embryo development (E5, E6, E7, E10, E12, and E14) to track changes in pluripotency and the dependence on signaling pathways via modified single-cell transcription sequencing technology. The remarkable similarity of the gene expression patterns between cattle and pigs during embryonic lineage development contributed to the successful establishment of bovine epiblast stem cells (bEpiSCs) using 3i/LAF (WNTi, GSK3βi, SRCi, LIF, Activin A, and FGF2) culture systems. The generated bEpiSCs exhibited consistent expression patterns of formative epiblast pluripotency genes and maintained clonal morphology, normal karyotypes, and proliferative capacity for more than 112 passages. Moreover, these cells exhibited high-efficiency teratoma formation as well as the ability to differentiate into various cell lineages. The potential of bEpiSCs for myogenic differentiation, primordial germ cell like cells (PGCLCs) induction and as donor cells for somatic cell nuclear transfer (SCNT) was also assessed, indicating their promise in advancing cell-cultured meat production, gene editing, and animal breeding. Bovine single cell RNA seq embryo development epiblast stem cell formative pluripotency cross-species comparisons Full Text Supplementary Files FigureS1240124.jpg FigureS2240124.jpg FigureS3240318.jpg FigureS4240124.jpg TableS1240128.xlsx TableS2240128.xlsx TableS3240128.xlsx TableS4240128.xlsx TableS5240128.xlsx TableS6240128.xlsx TableS7240128.xlsx TableS8240128.xlsx SupplementalInformation240312.docx Cite Share Download PDF Status: Published Journal Publication published 08 Oct, 2024 Read the published version in Cellular and Molecular Life Sciences → Version 1 posted Editorial decision: Accept as is 19 Sep, 2024 Reviewers agreed at journal 07 Jul, 2024 Reviewers invited by journal 05 Jul, 2024 Editor assigned by journal 28 Jun, 2024 First submitted to journal 27 Jun, 2024 You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. As a division of Research Square Company, we’re committed to making research communication faster, fairer, and more useful. We do this by developing innovative software and high quality services for the global research community. Our growing team is made up of researchers and industry professionals working together to solve the most critical problems facing scientific publishing. Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-4649336","acceptedTermsAndConditions":true,"allowDirectSubmit":false,"archivedVersions":[],"articleType":"Research Article","associatedPublications":[],"authors":[{"id":323217904,"identity":"4d1adc85-54f4-4dcc-987c-e48e980bb40d","order_by":0,"name":"Minglei Zhi","email":"","orcid":"","institution":"China Agricultural University","correspondingAuthor":false,"prefix":"","firstName":"Minglei","middleName":"","lastName":"Zhi","suffix":""},{"id":323217905,"identity":"4e5c1b14-bf0f-42b7-9b7f-220f302837e6","order_by":1,"name":"Dengfeng Gao","email":"","orcid":"","institution":"Sichuan Agricultural University","correspondingAuthor":false,"prefix":"","firstName":"Dengfeng","middleName":"","lastName":"Gao","suffix":""},{"id":323217906,"identity":"a497601f-7717-48a6-b35a-fc9037aa7361","order_by":2,"name":"Yixuan Yao","email":"","orcid":"","institution":"China Agricultural University","correspondingAuthor":false,"prefix":"","firstName":"Yixuan","middleName":"","lastName":"Yao","suffix":""},{"id":323217907,"identity":"79fba1d3-d28e-4fb6-94e7-f2d23a78f1d0","order_by":3,"name":"Zimo Zhao","email":"","orcid":"","institution":"China Agricultural University","correspondingAuthor":false,"prefix":"","firstName":"Zimo","middleName":"","lastName":"Zhao","suffix":""},{"id":323217908,"identity":"d7bc5ed2-4eeb-4060-86e0-1d6257a4bd5e","order_by":4,"name":"Yingjie Wang","email":"","orcid":"","institution":"China Agricultural University","correspondingAuthor":false,"prefix":"","firstName":"Yingjie","middleName":"","lastName":"Wang","suffix":""},{"id":323217909,"identity":"da926ba0-7202-4a91-95cb-dd5007a64bc9","order_by":5,"name":"Pengcheng He","email":"","orcid":"","institution":"China Agricultural University","correspondingAuthor":false,"prefix":"","firstName":"Pengcheng","middleName":"","lastName":"He","suffix":""},{"id":323217910,"identity":"e59f3e53-b463-489d-9b03-76146599dce5","order_by":6,"name":"Zhiqiang Feng","email":"","orcid":"","institution":"China Agricultural University","correspondingAuthor":false,"prefix":"","firstName":"Zhiqiang","middleName":"","lastName":"Feng","suffix":""},{"id":323217911,"identity":"e36974d8-be58-4c8a-952d-001bb8e4b4a4","order_by":7,"name":"Jinying Zhang","email":"","orcid":"","institution":"China Agricultural University","correspondingAuthor":false,"prefix":"","firstName":"Jinying","middleName":"","lastName":"Zhang","suffix":""},{"id":323217912,"identity":"8e3f3123-e6b3-4944-9ede-f97ddccca157","order_by":8,"name":"Ziqi Huang","email":"","orcid":"","institution":"Capital Medical University","correspondingAuthor":false,"prefix":"","firstName":"Ziqi","middleName":"","lastName":"Huang","suffix":""},{"id":323217913,"identity":"9ebc22b1-a4f3-4e0a-bfbe-63315171c524","order_by":9,"name":"Wenyuan Gu","email":"","orcid":"","institution":"Tianquan Elite Dairy Co., Ltd.","correspondingAuthor":false,"prefix":"","firstName":"Wenyuan","middleName":"","lastName":"Gu","suffix":""},{"id":323217914,"identity":"28754afd-29ac-4185-83a1-85e0da19c754","order_by":10,"name":"Jianglin Zhao","email":"","orcid":"","institution":"Northwest Agriculture University: Northwest A\u0026F University","correspondingAuthor":false,"prefix":"","firstName":"Jianglin","middleName":"","lastName":"Zhao","suffix":""},{"id":323217915,"identity":"58f12326-3e98-4240-9fd6-0ae7eb9c9f1f","order_by":11,"name":"He Zhang","email":"","orcid":"","institution":"China Agricultural University","correspondingAuthor":false,"prefix":"","firstName":"He","middleName":"","lastName":"Zhang","suffix":""},{"id":323217916,"identity":"f6270763-ae62-4d68-b0ce-682275416f60","order_by":12,"name":"Shunxin Wang","email":"","orcid":"","institution":"China Agricultural University","correspondingAuthor":false,"prefix":"","firstName":"Shunxin","middleName":"","lastName":"Wang","suffix":""},{"id":323217917,"identity":"81c4268b-6558-428b-939f-89de70c81b61","order_by":13,"name":"Xin Li","email":"","orcid":"","institution":"Tianquan Elite Dairy Co., Ltd.","correspondingAuthor":false,"prefix":"","firstName":"Xin","middleName":"","lastName":"Li","suffix":""},{"id":323217918,"identity":"9ae8204f-93e6-412f-b449-8f36a9ac15a0","order_by":14,"name":"Qiang Zhang","email":"","orcid":"","institution":"China Agricultural University","correspondingAuthor":false,"prefix":"","firstName":"Qiang","middleName":"","lastName":"Zhang","suffix":""},{"id":323217919,"identity":"fee1cdde-f9e1-47f0-b1da-8e16b4248636","order_by":15,"name":"Zengyuan Zhao","email":"","orcid":"","institution":"China Agricultural University","correspondingAuthor":false,"prefix":"","firstName":"Zengyuan","middleName":"","lastName":"Zhao","suffix":""},{"id":323217920,"identity":"3f166110-e2e2-4417-9b11-a93f007ad4f4","order_by":16,"name":"Xinze Chen","email":"","orcid":"","institution":"China Agricultural University","correspondingAuthor":false,"prefix":"","firstName":"Xinze","middleName":"","lastName":"Chen","suffix":""},{"id":323217921,"identity":"b55c438f-ddeb-4e20-9f35-78906d068bb0","order_by":17,"name":"Xiaowei Zhang","email":"","orcid":"","institution":"China Agricultural University","correspondingAuthor":false,"prefix":"","firstName":"Xiaowei","middleName":"","lastName":"Zhang","suffix":""},{"id":323217922,"identity":"5ded3a7e-2aa4-4591-b9ac-547eb77688da","order_by":18,"name":"Lun Qin","email":"","orcid":"","institution":"Beijing University of Agriculture","correspondingAuthor":false,"prefix":"","firstName":"Lun","middleName":"","lastName":"Qin","suffix":""},{"id":323217923,"identity":"3c2333ab-3321-4642-a299-fa9b88738f6c","order_by":19,"name":"Jun Liu","email":"","orcid":"","institution":"Northwest Agriculture University: Northwest A\u0026F University","correspondingAuthor":false,"prefix":"","firstName":"Jun","middleName":"","lastName":"Liu","suffix":""},{"id":323217924,"identity":"633ed9ab-89cd-43c6-9d9c-ef2118289d19","order_by":20,"name":"Chengjun Liu","email":"","orcid":"","institution":"Beijing Dairy Cattle Center","correspondingAuthor":false,"prefix":"","firstName":"Chengjun","middleName":"","lastName":"Liu","suffix":""},{"id":323217925,"identity":"826dface-84f3-4a6f-8bc2-fa53615be6cc","order_by":21,"name":"Suying Cao","email":"","orcid":"","institution":"Beijing University of Agriculture","correspondingAuthor":false,"prefix":"","firstName":"Suying","middleName":"","lastName":"Cao","suffix":""},{"id":323217926,"identity":"b5076e3b-45c2-4254-93ac-fe537108394a","order_by":22,"name":"Shuai Gao","email":"","orcid":"","institution":"China Agricultural University","correspondingAuthor":false,"prefix":"","firstName":"Shuai","middleName":"","lastName":"Gao","suffix":""},{"id":323217927,"identity":"aca12cc2-dfd3-44f6-9ee6-c2db4da9c5ed","order_by":23,"name":"Wenli Yu","email":"","orcid":"","institution":"Tianquan elite dairy co., ltd.","correspondingAuthor":false,"prefix":"","firstName":"Wenli","middleName":"","lastName":"Yu","suffix":""},{"id":323217928,"identity":"6e30b396-3136-4716-b471-0efbe566f1ea","order_by":24,"name":"Jianyong Han","email":"data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAZAAAAAyAQMAAABI0h/eAAAABlBMVEX///8AAABVwtN+AAAACXBIWXMAAA7EAAAOxAGVKw4bAAAAuElEQVRIiWNgGAWjYBACAzCugHAkSNByhlQtDIxtpGgxZz97oJh3np28wQHmg7d5GOzyCGqx7MlLMObdlmy44QBbsjUPQ3IxYYcdyDEAajnAuOEAj5k0D8OBxAaCWs6/AWqZc8B+wwH+b0RquQGypeFAItAWNmK1vDEwnHMsOXnmYTZjyzkGycQ4LMfM4E2NnW3f8eaHN95U2BHWAgRsRjwgihlsAhHqQWof/iBO4SgYBaNgFIxUAAD4iznZxCbNEAAAAABJRU5ErkJggg==","orcid":"https://orcid.org/0000-0002-9549-3279","institution":"China Agricultural University","correspondingAuthor":true,"prefix":"","firstName":"Jianyong","middleName":"","lastName":"Han","suffix":""},{"id":323217929,"identity":"82d32d95-9d83-4db9-abf6-a8515568901c","order_by":25,"name":"Zhu Ma","email":"","orcid":"","institution":"beijing dairy cattle center","correspondingAuthor":false,"prefix":"","firstName":"Zhu","middleName":"","lastName":"Ma","suffix":""}],"badges":[],"createdAt":"2024-06-27 14:46:58","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-4649336/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-4649336/v1","draftVersion":[],"editorialEvents":[{"content":"https://doi.org/10.1007/s00018-024-05457-z","type":"published","date":"2024-10-08T15:57:26+00:00"}],"editorialNote":"","failedWorkflow":false,"files":[{"id":66597579,"identity":"fe0b760a-a4bf-477c-9b37-897fffaf0300","added_by":"auto","created_at":"2024-10-14 16:11:03","extension":"pdf","order_by":1,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":2837013,"visible":true,"origin":"","legend":"","description":"","filename":"MainText240626.pdf","url":"https://assets-eu.researchsquare.com/files/rs-4649336/v1_covered_669a8caa-fe1f-4862-8de6-30a0921a3e3d.pdf"},{"id":61427232,"identity":"6161050e-6fa4-4d03-b73a-9d8ee775fb96","added_by":"auto","created_at":"2024-07-30 15:02:40","extension":"jpg","order_by":1,"title":"","display":"","copyAsset":false,"role":"supplement","size":2728577,"visible":true,"origin":"","legend":"","description":"","filename":"FigureS1240124.jpg","url":"https://assets-eu.researchsquare.com/files/rs-4649336/v1/f585c518c912425633d8410c.jpg"},{"id":61427238,"identity":"b8398a8d-a789-4fc7-a2af-ca44b8e9f61f","added_by":"auto","created_at":"2024-07-30 15:02:41","extension":"jpg","order_by":2,"title":"","display":"","copyAsset":false,"role":"supplement","size":1177713,"visible":true,"origin":"","legend":"","description":"","filename":"FigureS2240124.jpg","url":"https://assets-eu.researchsquare.com/files/rs-4649336/v1/d0a189f7aa2d80a247a4a2d6.jpg"},{"id":61427244,"identity":"15b10336-ec9e-4b33-ab94-e153875eb868","added_by":"auto","created_at":"2024-07-30 15:02:42","extension":"jpg","order_by":3,"title":"","display":"","copyAsset":false,"role":"supplement","size":3874555,"visible":true,"origin":"","legend":"","description":"","filename":"FigureS3240318.jpg","url":"https://assets-eu.researchsquare.com/files/rs-4649336/v1/2cfa565361f22b69cb5c998e.jpg"},{"id":61427245,"identity":"1986f8e6-52ad-470e-aa5a-653aea786e1b","added_by":"auto","created_at":"2024-07-30 15:02:42","extension":"jpg","order_by":4,"title":"","display":"","copyAsset":false,"role":"supplement","size":2218810,"visible":true,"origin":"","legend":"","description":"","filename":"FigureS4240124.jpg","url":"https://assets-eu.researchsquare.com/files/rs-4649336/v1/998d1d2d15de5fab459dd75f.jpg"},{"id":61427233,"identity":"6dfae433-a47a-496b-8a81-291611184edf","added_by":"auto","created_at":"2024-07-30 15:02:41","extension":"xlsx","order_by":5,"title":"","display":"","copyAsset":false,"role":"supplement","size":48610,"visible":true,"origin":"","legend":"","description":"","filename":"TableS1240128.xlsx","url":"https://assets-eu.researchsquare.com/files/rs-4649336/v1/6552f924b2d530ffc0002249.xlsx"},{"id":61427234,"identity":"2da49193-e867-4ea8-9841-46e69d7c391d","added_by":"auto","created_at":"2024-07-30 15:02:41","extension":"xlsx","order_by":6,"title":"","display":"","copyAsset":false,"role":"supplement","size":267603,"visible":true,"origin":"","legend":"","description":"","filename":"TableS2240128.xlsx","url":"https://assets-eu.researchsquare.com/files/rs-4649336/v1/7e316080e715aa665bf06978.xlsx"},{"id":61427242,"identity":"e2597e9f-d800-4c5c-9f13-4a880a699382","added_by":"auto","created_at":"2024-07-30 15:02:41","extension":"xlsx","order_by":7,"title":"","display":"","copyAsset":false,"role":"supplement","size":252904,"visible":true,"origin":"","legend":"","description":"","filename":"TableS3240128.xlsx","url":"https://assets-eu.researchsquare.com/files/rs-4649336/v1/0eb545b2dea0e7437f0aba02.xlsx"},{"id":61427235,"identity":"cf664e59-b5fc-4b0f-8d86-f25356200acc","added_by":"auto","created_at":"2024-07-30 15:02:41","extension":"xlsx","order_by":8,"title":"","display":"","copyAsset":false,"role":"supplement","size":263064,"visible":true,"origin":"","legend":"","description":"","filename":"TableS4240128.xlsx","url":"https://assets-eu.researchsquare.com/files/rs-4649336/v1/fdff66e803df060705b6dec7.xlsx"},{"id":61427239,"identity":"d920c898-5157-4dd5-8a4f-2106cf240dc6","added_by":"auto","created_at":"2024-07-30 15:02:41","extension":"xlsx","order_by":9,"title":"","display":"","copyAsset":false,"role":"supplement","size":81905,"visible":true,"origin":"","legend":"","description":"","filename":"TableS5240128.xlsx","url":"https://assets-eu.researchsquare.com/files/rs-4649336/v1/06757bf565aaf0d537b9b8ad.xlsx"},{"id":61427237,"identity":"16920c04-47e0-4273-bc2d-c60e7479c548","added_by":"auto","created_at":"2024-07-30 15:02:41","extension":"xlsx","order_by":10,"title":"","display":"","copyAsset":false,"role":"supplement","size":6843440,"visible":true,"origin":"","legend":"","description":"","filename":"TableS6240128.xlsx","url":"https://assets-eu.researchsquare.com/files/rs-4649336/v1/b59f08c0a26ffc8e72948f9b.xlsx"},{"id":61427240,"identity":"d5f8021f-9afc-4358-8cbd-2e4ee16ddf51","added_by":"auto","created_at":"2024-07-30 15:02:41","extension":"xlsx","order_by":11,"title":"","display":"","copyAsset":false,"role":"supplement","size":1556466,"visible":true,"origin":"","legend":"","description":"","filename":"TableS7240128.xlsx","url":"https://assets-eu.researchsquare.com/files/rs-4649336/v1/4b148b90b3f7a2e98ce87488.xlsx"},{"id":61427243,"identity":"3a6cad0d-96ad-4ee7-9dbb-1c118f4f24c7","added_by":"auto","created_at":"2024-07-30 15:02:42","extension":"xlsx","order_by":12,"title":"","display":"","copyAsset":false,"role":"supplement","size":11133,"visible":true,"origin":"","legend":"","description":"","filename":"TableS8240128.xlsx","url":"https://assets-eu.researchsquare.com/files/rs-4649336/v1/6b96d6f6036c7cf037ae6788.xlsx"},{"id":61427236,"identity":"c097dce1-0ab5-49ba-97b0-9f2231723de7","added_by":"auto","created_at":"2024-07-30 15:02:41","extension":"docx","order_by":13,"title":"","display":"","copyAsset":false,"role":"supplement","size":17762,"visible":true,"origin":"","legend":"","description":"","filename":"SupplementalInformation240312.docx","url":"https://assets-eu.researchsquare.com/files/rs-4649336/v1/5289e6b8682382ae6c3c13dd.docx"}],"financialInterests":"","formattedTitle":"Elucidation of the pluripotent potential of bovine embryonic lineages facilitates the establishment of formative stem cell lines","fulltext":[],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":false,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":false,"highlight":"","institution":"","isAcceptedByJournal":true,"isAuthorSuppliedPdf":true,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":true,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"
[email protected]","identity":"cellular-and-molecular-life-sciences","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"life","sideBox":"Learn more about [Cellular and Molecular Life Sciences](https://link.springer.com/journal/18)","snPcode":"18","submissionUrl":"https://www.editorialmanager.com/life/default2.aspx","title":"Cellular and Molecular Life Sciences","twitterHandle":"","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"em","reportingPortfolio":"Springer Open","inReviewEnabled":true,"inReviewRevisionsEnabled":true},"keywords":"Bovine, single cell RNA seq, embryo development, epiblast stem cell, formative pluripotency, cross-species comparisons","lastPublishedDoi":"10.21203/rs.3.rs-4649336/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-4649336/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003eThe establishment of epiblast-derived pluripotent stem cells (PSCs) from cattle, which are important domestic animals that provide humans with milk and meat while also serving as bioreactors for producing valuable proteins, poses a challenge due to the unclear molecular signaling required for embryonic epiblast development and maintenance of PSC self-renewal. Here, we selected six key stages of bovine embryo development (E5, E6, E7, E10, E12, and E14) to track changes in pluripotency and the dependence on signaling pathways via modified single-cell transcription sequencing technology. The remarkable similarity of the gene expression patterns between cattle and pigs during embryonic lineage development contributed to the successful establishment of bovine epiblast stem cells (bEpiSCs) using 3i/LAF (WNTi, GSK3βi, SRCi, LIF, Activin A, and FGF2) culture systems. The generated bEpiSCs exhibited consistent expression patterns of formative epiblast pluripotency genes and maintained clonal morphology, normal karyotypes, and proliferative capacity for more than 112 passages. Moreover, these cells exhibited high-efficiency teratoma formation as well as the ability to differentiate into various cell lineages. The potential of bEpiSCs for myogenic differentiation, primordial germ cell like cells (PGCLCs) induction and as donor cells for somatic cell nuclear transfer (SCNT) was also assessed, indicating their promise in advancing cell-cultured meat production, gene editing, and animal breeding.\u003c/p\u003e","manuscriptTitle":"Elucidation of the pluripotent potential of bovine embryonic lineages facilitates the establishment of formative stem cell lines","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2024-07-30 15:02:35","doi":"10.21203/rs.3.rs-4649336/v1","editorialEvents":[{"type":"communityComments","content":0},{"type":"decision","content":"Accept as is","date":"2024-09-19T08:58:30+00:00","index":"","fulltext":""},{"type":"reviewerAgreed","content":"","date":"2024-07-08T02:24:06+00:00","index":0,"fulltext":""},{"type":"reviewersInvited","content":"","date":"2024-07-05T14:28:39+00:00","index":"","fulltext":""},{"type":"editorAssigned","content":"","date":"2024-06-28T05:58:35+00:00","index":"","fulltext":""},{"type":"submitted","content":"Cellular and Molecular Life Sciences","date":"2024-06-27T10:46:20+00:00","index":"","fulltext":""}],"status":"published","journal":{"display":true,"email":"
[email protected]","identity":"cellular-and-molecular-life-sciences","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"life","sideBox":"Learn more about [Cellular and Molecular Life Sciences](https://link.springer.com/journal/18)","snPcode":"18","submissionUrl":"https://www.editorialmanager.com/life/default2.aspx","title":"Cellular and Molecular Life Sciences","twitterHandle":"","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"em","reportingPortfolio":"Springer Open","inReviewEnabled":true,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"fa4d7f41-7d7e-4f88-8b89-ad5455b8ce69","owner":[],"postedDate":"July 30th, 2024","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"published-in-journal","subjectAreas":[],"tags":[],"updatedAt":"2024-10-14T16:07:36+00:00","versionOfRecord":{"articleIdentity":"rs-4649336","link":"https://doi.org/10.1007/s00018-024-05457-z","journal":{"identity":"cellular-and-molecular-life-sciences","isVorOnly":false,"title":"Cellular and Molecular Life Sciences"},"publishedOn":"2024-10-08 15:57:26","publishedOnDateReadable":"October 8th, 2024"},"versionCreatedAt":"2024-07-30 15:02:35","video":"","vorDoi":"10.1007/s00018-024-05457-z","vorDoiUrl":"https://doi.org/10.1007/s00018-024-05457-z","workflowStages":[]},"version":"v1","identity":"rs-4649336","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-4649336","identity":"rs-4649336","version":["v1"]},"buildId":"8U1c8b4HqxoKbykW_rLl7","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}
Text is read by the "Ask this paper" AI Q&A widget below.
Extraction quality varies by source — PMC NXML preserves structure
cleanly, OA-HTML may include some navigation residue, and OA-PDF can
have broken hyphenation. The publisher copy
(via DOI)
is the canonical version.