Programming of pluripotency and the germ line co-evolved from a Nanog ancestor.

IF 7.5 1区生物学 Q1 CELL BIOLOGY

Cell reports Pub Date : 2025-03-25 Epub Date: 2025-03-08 DOI:10.1016/j.celrep.2025.115396

Darren Crowley, Luke Simpson, Jodie Chatfield, Teri Forey, Cinzia Allegrucci, Fei Sang, Nadine Holmes, Grigory Genikhovich, Ulrich Technau, Doreen Cunningham, Elena Silva, Nicholas Mullin, James E Dixon, Matthew Loose, Ramiro Alberio, Andrew D Johnson

{"title":"Programming of pluripotency and the germ line co-evolved from a Nanog ancestor.","authors":"Darren Crowley, Luke Simpson, Jodie Chatfield, Teri Forey, Cinzia Allegrucci, Fei Sang, Nadine Holmes, Grigory Genikhovich, Ulrich Technau, Doreen Cunningham, Elena Silva, Nicholas Mullin, James E Dixon, Matthew Loose, Ramiro Alberio, Andrew D Johnson","doi":"10.1016/j.celrep.2025.115396","DOIUrl":null,"url":null,"abstract":"Francois Jacob proposed that evolutionary novelty arises through incremental tinkering with pre-existing genetic mechanisms. Vertebrate evolution was predicated on pluripotency, the ability of embryonic cells to form somatic germ layers and primordial germ cells (PGCs). The origins of pluripotency remain unclear, as key regulators, such as Nanog, are not conserved outside of vertebrates. Given NANOG's role in mammalian development, we hypothesized that NANOG activity might exist in ancestral invertebrate genes. Here, we find that Vent from the hemichordate Saccoglossus kowalevskii exhibits NANOG activity, programming pluripotency in Nanog-/- mouse pre-induced pluripotent stem cells (iPSCs) and NANOG-depleted axolotl embryos. Vent from the cnidarian Nematostella vectensis showed partial activity, whereas Vent from sponges and vertebrates had no activity. VENTX knockdown in axolotls revealed a role in germline-competent mesoderm, which Saccoglossus Vent could rescue but Nematostella Vent could not. This suggests that the last deuterostome ancestor had a Vent gene capable of programming pluripotency and germline competence.","PeriodicalId":9798,"journal":{"name":"Cell reports","volume":"44 3","pages":"115396"},"PeriodicalIF":7.5000,"publicationDate":"2025-03-25","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Cell reports","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1016/j.celrep.2025.115396","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2025/3/8 0:00:00","PubModel":"Epub","JCR":"Q1","JCRName":"CELL BIOLOGY","Score":null,"Total":0}

引用次数: 0

Abstract

Francois Jacob proposed that evolutionary novelty arises through incremental tinkering with pre-existing genetic mechanisms. Vertebrate evolution was predicated on pluripotency, the ability of embryonic cells to form somatic germ layers and primordial germ cells (PGCs). The origins of pluripotency remain unclear, as key regulators, such as Nanog, are not conserved outside of vertebrates. Given NANOG's role in mammalian development, we hypothesized that NANOG activity might exist in ancestral invertebrate genes. Here, we find that Vent from the hemichordate Saccoglossus kowalevskii exhibits NANOG activity, programming pluripotency in Nanog^-/- mouse pre-induced pluripotent stem cells (iPSCs) and NANOG-depleted axolotl embryos. Vent from the cnidarian Nematostella vectensis showed partial activity, whereas Vent from sponges and vertebrates had no activity. VENTX knockdown in axolotls revealed a role in germline-competent mesoderm, which Saccoglossus Vent could rescue but Nematostella Vent could not. This suggests that the last deuterostome ancestor had a Vent gene capable of programming pluripotency and germline competence.

查看原文本刊更多论文

求助全文

约1分钟内获得全文求助全文

来源期刊

Cell reports CELL BIOLOGY-

CiteScore

13.80

自引率

1.10%

发文量

1305

审稿时长

77 days

期刊介绍： Cell Reports publishes high-quality research across the life sciences and focuses on new biological insight as its primary criterion for publication. The journal offers three primary article types: Reports, which are shorter single-point articles, research articles, which are longer and provide deeper mechanistic insights, and resources, which highlight significant technical advances or major informational datasets that contribute to biological advances. Reviews covering recent literature in emerging and active fields are also accepted. The Cell Reports Portfolio includes gold open-access journals that cover life, medical, and physical sciences, and its mission is to make cutting-edge research and methodologies available to a wide readership. The journal's professional in-house editors work closely with authors, reviewers, and the scientific advisory board, which consists of current and future leaders in their respective fields. The advisory board guides the scope, content, and quality of the journal, but editorial decisions are independently made by the in-house scientific editors of Cell Reports.