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TET knockout cells transit between pluripotent states and exhibit precocious germline entry

Raphaël Pantier, Elisa Barbieri, Sara Gonzalez Brito, Ella Thomson, Tülin Tatar, Douglas Colby, Man Zhang, Ian Chambers

Posted on: 5 August 2025 , updated on: 6 August 2025

Preprint posted on 3 December 2024

Genetic gatekeepers of gametogenesis? TET proteins jointly jam germline specification, synergistically steering cells towards somatic fates.

Selected by Justin Gutkowski

Categories: cell biology, developmental biology, genetics

Background:

Shortly after the discovery of genetic inheritance, scientists observed that not all traits could be attributed solely to genetic variation. They theorized that something “on top of” (“epi-”) the genome was influencing the expression of genes. The field of epigenetics has budded from this observation. Epigenetics explains how different cell types express different genes, despite containing the same genetic information, as well as how the body can modify the expression of its genes in response to the environment. There are several mechanisms of epigenetic modification, but the most common is the addition and removal of methyl (CH3) groups to DNA bases. Transcription factors, which bind to DNA meant to be expressed, are affected by methylation. There are also specific proteins responsible for methylating and demethylating DNA, and understanding more about them can help us understand how gene expression is regulated during development, in different cell types, and in response to the environment.

This preprint covers three demethylase proteins, known as Ten Eleven Translocation (TET) proteins. Mammalian genomes contain three tet genes: tet1, tet2, and tet3. Previous studies in mice and cell culture have shown that these proteins are partially redundant. The loss of tet1 or tet2 is non-lethal in mice, but the loss of more than one of these genes causes severe phenotypes, including the inability to produce certain cell types. The authors of this preprint investigated the individual and synergistic effects of these proteins on cellular differentiation down multiple lineages, including the germline, or reproductive cells.

Methods:

To answer this question, the authors genetically engineered six groups of Embryonic Stem Cells (ESCs): unmodified (WT), tet1 knockout (T1KO), tet2 knockout (T2KO), tet3 knockout (T3KO), tet1/tet2 double knockout (DKO), and tet1/tet2/tet3 triple knockout (TKO). Each group was then cultured through multiple protocols to observe the effects of each gene on the cells’ ability to 1) maintain their pluripotent identity, 2) differentiate into somatic lineages, and 3) differentiate into the germline. The researchers used qPCR and antibody staining to measure the gene and protein expression of the cells after differentiation to compare them to the target cell types.

Results:

Undifferentiated Culture Protocol:

When ESCs in each of the six groups were cultured, no group exhibited significant differences in morphology or expression of pluripotency-associated genes. However, when cultured at clonal density in the presence of leukemia inhibitory factor (LIF), a cytokine that promotes the self-renewal of pluripotent stem cells, the DKO and TKO groups exhibited an increase in colonies exhibiting alkaline phosphatase activity, indicating that they maintain an undifferentiated state more strongly than colonies with lower activity. No other groups exhibited significant changes when cultured with LIF. This indicates that tet1 and tet2 redundantly reduce the efficiency of self-renewal in ESCs, as changes were only observed when both were knocked out.

Somatic Differentiation Protocols:

To measure the effects of each TET gene on somatic differentiation, ESCs in each group were cultured through protocols meant to induce differentiation into 1) a 2D culture of neuroectodermal progenitor cells (NPCs), and 2) an embryoid body, or a 3D structure that exhibits characteristics of early embryonic development, including differentiation into multiple cell types.

In the first protocol, the WT, T2KO, and T3KO cells exhibited the morphological and genetic signatures of differentiation: flattening out and expressing genes characteristic of NPCs. However, the T1KO, DKO, and TKO cells did not exhibit signs of differentiation. Cultures retained colonies with a compact, rounded morphology and expressed pluripotency-associated genes. This indicates that tet1 is specifically required for neural differentiation, as groups without this gene failed to differentiate.

In the second protocol, the WT, T1KO, T2KO, and T3KO cells exhibited morphological differentiation, including the formation of beating cardiomyocyte colonies. These groups also expressed the genes associated with multiple germ layers. However, the DKO and TKO groups did not exhibit morphological differentiation and retained expression of pluripotency-associated genes. This indicates that the activity of multiple TET genes is required for early development, including germ layer formation and cardiomyocyte differentiation.

Germline Differentiation Protocol:

To measure the effects of each TET gene on the ability of cells to differentiate into non-somatic lineages, they were cultured through a protocol meant to induce differentiation into primordial germ cell-like cells (PGCLCs), or cells that resemble the progenitors of eggs and sperm.

When cells in each of the six groups were cultured through this protocol, the WT, T1KO, T2KO, and T3KO cells did not differentiate efficiently, with cells in each group exhibiting low levels of PGCLC markers. The DKO and TKO groups differentiated much more efficiently, with a large proportion of cells strongly expressing these markers. This result was unaffected by the inclusion and exclusion of PGC-promoting cytokines. Interestingly, these results are the opposite of those observed in the EB formation protocol, indicating that the presence of multiple TET genes influences the cell to differentiate into somatic lineages, while the absence of these genes influences cells towards germline specification.

RNA sequencing and analysis of WT and TKO cells during PGCLC differentiation revealed that during the 6-day PGCLC differentiation protocol, TKO cells become transcriptionally similar to fully differentiated WT cells after only 2 days. Analysis of the genes expressed in both groups of PGCLCs at this timepoint revealed that they were mostly related to “stem cell population maintenance” and “reproductive structure development”. However, when TKO cells reach day 6 of differentiation, they upregulate genes associated with “germline or gonad development” and later germline markers. This indicates that the loss of TET genes may accelerate germline specification and development.

The final figure from the preprint, which shows the main findings of the study: TET deficiency increases the efficiency of PSC self-renewal and biases PSC differentiation towards the germline.

Significance:

I highlighted this preprint because I am interested in the specification of different cell types in early development, especially germ cells, as well as the mechanisms that regulate this process, especially in mammals. Research into this area has the potential to uncover the causes of numerous developmental disorders and infertility conditions, allowing us to develop treatments for these conditions. This preprint describes three gene paralogs that play roles in the process of germline specification and examines the redundant and unique roles of each in this process.

Questions for the Authors:

  1. Did you suspect that the TET proteins had a role in inhibiting germline specification when you began this study, or did that line of questioning emerge naturally from the other experiments?
  2. Gene groups 2 and 3 of the hierarchical clustering of the PCA are upregulated in wild-type ESCs after 6 days of PGCLC differentiation culture without cytokines, but downregulated in wild-type ESCs differentiated with cytokines and in triple-KO ESCS. You note that these genes are “mostly related to the neural fate”, suggesting that this is the fate that wild-type cells will follow in the absence of cytokines. Does this mean that totipotent cells that do not receive any specific differentiation signals are biased towards a neural fate, or are there other factors in the protocol that may have influenced their differentiation? Did you expect this?

 

doi: https://doi.org/10.1242/prelights.41150

Read preprint (No Ratings Yet)

Author's response

Dr. Ian Chambers shared

Question: Did you suspect that the TET proteins had a role in inhibiting germline specification when you began this study, or did that line of questioning emerge naturally from the other experiments?

Answer: Previous studies had indicated that TET proteins are required for somatic lineage commitment (Dawlaty et al, 2014; Li et al, 2016; Verma et al, 2018), although the exact contribution of each isoform was unclear. However, the inhibiting action of TET proteins during germline commitment was a surprise. Given the specific role of TET1 during later germ cell maturation, and in female meiosis, we would probably have expected the opposite phenotype for TET-deficient cells in PGCLC differentiation.

Question: Gene groups 2 and 3 of the hierarchical clustering of the PCA are upregulated in wild-type ESCs after 6 days of PGCLC differentiation culture without cytokines, but downregulated in wild-type ESCs differentiated with cytokines and in triple-KO ESCS. You note that these genes are “mostly related to the neural fate”, suggesting that this is the fate that wild-type cells will follow in the absence of cytokines. Does this mean that totipotent cells that do not receive any specific differentiation signals are biased towards a neural fate, or are there other factors in the protocol that may have influenced their differentiation? Did you expect this?

Answer: The idea that pluripotent stem cells commit to neural lineages “by default” in vitro has been proposed (Tropepe et al, 2001; Muñoz-Sanjuán & Brivanlou, 2002), potentially explained by their epiblastic origin. So, differentiation toward endoderm/mesoderm might require more extensive reprogramming of the epigenome and the transcriptome. In line with this, a single-cell epigenomic study in developing mouse embryos showed that enhancers associated with neuroectodermal lineages are already “primed” (carrying active marks, but without active transcription) in epiblast cells as early as embryonic day E4.5, well before the formation of neural tissues (Argelaguet et al, 2019).
One final point to consider with respect to default differentiation relates to previous findings that pluripotent cells lacking Otx2 can differentiate into the germline in the absence of cytokines (Zhang et al, 2018). Notably, PGCLC differentiation in Otx2-/- cells is not fully efficient unless cytokines are added. For TET triple-KOs, the presence or absence of cytokines makes no difference, and the differentiation of these cells into the germline is fully efficient. So, without TET function, all cells default to germline differentiation. This is interesting in view of the ancestral nature of induced germline specification in mammals, compared to species with germplasm (eg, birds, frogs) (Johnson & Alberio, 2015) and suggests that germline may be the default option that needs to be overcome in order to produce the familiar somatic structures of mammalian bodies.

References:

Argelaguet R, Clark SJ, Mohammed H, Stapel LC, Krueger C, Kapourani C-A, Imaz-Rosshandler I, Lohoff T, Xiang Y, Hanna CW, et al (2019) Multi-omics profiling of mouse gastrulation at single-cell resolution. Nature 576: 487–491

Dawlaty MM, Breiling A, Le T, Barrasa MI, Raddatz G, Gao Q, Powell BE, Cheng AW, Faull KF, Lyko F, et al (2014) Loss of Tet Enzymes Compromises Proper Differentiation of Embryonic Stem Cells. Developmental Cell 29: 102–111

Johnson, A. D. & Alberio, R. Primordial germ cells: the first cell lineage or the last cells standing? Development 142, 2730–2739 (2015).

Li X, Yue X, Pastor WA, Lin L, Georges R, Chavez L, Evans SM & Rao A (2016) Tet proteins influence the balance between neuroectodermal and mesodermal fate choice by inhibiting Wnt signaling. Proceedings of the National Academy of Sciences 113: E8267–E8276

Muñoz-Sanjuán I & Brivanlou AH (2002) Neural induction, the default model and embryonic stem cells. Nat Rev Neurosci 3: 271–280

Tropepe V, Hitoshi S, Sirard C, Mak TW, Rossant J & van der Kooy D (2001) Direct Neural Fate Specification from Embryonic Stem Cells: A Primitive Mammalian Neural Stem Cell Stage Acquired through a Default Mechanism. Neuron 30: 65–78

Verma N, Pan H, Doré LC, Shukla A, Li QV, Pelham-Webb B, Teijeiro V, González F, Krivtsov A, Chang C-J, et al (2018) TET proteins safeguard bivalent promoters from de novo methylation in human embryonic stem cells. Nat Genet 50: 83–95

Zhang J, Zhang M, Acampora D, et al. OTX2 restricts entry to the mouse germline. Nature. 2018;562:595–599.

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List by Ana Dorrego-Rivas

Planar Cell Polarity – PCP

This preList contains preprints about the latest findings on Planar Cell Polarity (PCP) in various model organisms at the molecular, cellular and tissue levels.

 



List by Ana Dorrego-Rivas

Cell Polarity

Recent research from the field of cell polarity is summarized in this list of preprints. It comprises of studies focusing on various forms of cell polarity ranging from epithelial polarity, planar cell polarity to front-to-rear polarity.

 



List by Yamini Ravichandran

TAGC 2020

Preprints recently presented at the virtual Allied Genetics Conference, April 22-26, 2020. #TAGC20

 



List by Maiko Kitaoka et al.

3D Gastruloids

A curated list of preprints related to Gastruloids (in vitro models of early development obtained by 3D aggregation of embryonic cells). Updated until July 2021.

 



List by Paul Gerald L. Sanchez and Stefano Vianello

ASCB EMBO Annual Meeting 2019

A collection of preprints presented at the 2019 ASCB EMBO Meeting in Washington, DC (December 7-11)

 



List by Madhuja Samaddar et al.

EDBC Alicante 2019

Preprints presented at the European Developmental Biology Congress (EDBC) in Alicante, October 23-26 2019.

 



List by Sergio Menchero et al.

EMBL Seeing is Believing – Imaging the Molecular Processes of Life

Preprints discussed at the 2019 edition of Seeing is Believing, at EMBL Heidelberg from the 9th-12th October 2019

 



List by Dey Lab

SDB 78th Annual Meeting 2019

A curation of the preprints presented at the SDB meeting in Boston, July 26-30 2019. The preList will be updated throughout the duration of the meeting.

 



List by Alex Eve

Lung Disease and Regeneration

This preprint list compiles highlights from the field of lung biology.

 



List by Rob Hynds

Young Embryologist Network Conference 2019

Preprints presented at the Young Embryologist Network 2019 conference, 13 May, The Francis Crick Institute, London

 



List by Alex Eve

Pattern formation during development

The aim of this preList is to integrate results about the mechanisms that govern patterning during development, from genes implicated in the processes to theoritical models of pattern formation in nature.

 



List by Alexa Sadier

BSCB/BSDB Annual Meeting 2019

Preprints presented at the BSCB/BSDB Annual Meeting 2019

 



List by Dey Lab

Zebrafish immunology

A compilation of cutting-edge research that uses the zebrafish as a model system to elucidate novel immunological mechanisms in health and disease.

 



List by Shikha Nayar

Also in the genetics category:

October in preprints – DevBio & Stem cell biology

Each month, preLighters with expertise across developmental and stem cell biology nominate a few recent developmental and stem cell biology (and related) preprints they’re excited about and explain in a single paragraph why. Short, snappy picks from working scientists — a quick way to spot fresh ideas, bold methods and papers worth reading in full. These preprints can all be found in the October preprint list published on the Node.

 



List by Deevitha Balasubramanian et al.

September in preprints – Cell biology edition

A group of preLighters, with expertise in different areas of cell biology, have worked together to create this preprint reading list. This month, categories include: (1) Cell organelles and organisation, (2) Cell signalling and mechanosensing, (3) Cell metabolism, (4) Cell cycle and division, (5) Cell migration

 



List by Sristilekha Nath et al.

July in preprints – the CellBio edition

A group of preLighters, with expertise in different areas of cell biology, have worked together to create this preprint reading lists for researchers with an interest in cell biology. This month, categories include: (1) Cell Signalling and Mechanosensing (2) Cell Cycle and Division (3) Cell Migration and Cytoskeleton (4) Cancer Biology (5) Cell Organelles and Organisation

 



List by Girish Kale et al.

June in preprints – the CellBio edition

A group of preLighters, with expertise in different areas of cell biology, have worked together to create this preprint reading lists for researchers with an interest in cell biology. This month, categories include: (1) Cell organelles and organisation (2) Cell signaling and mechanosensation (3) Genetics/gene expression (4) Biochemistry (5) Cytoskeleton

 



List by Barbora Knotkova et al.

May in preprints – the CellBio edition

A group of preLighters, with expertise in different areas of cell biology, have worked together to create this preprint reading lists for researchers with an interest in cell biology. This month, categories include: 1) Biochemistry/metabolism 2) Cancer cell Biology 3) Cell adhesion, migration and cytoskeleton 4) Cell organelles and organisation 5) Cell signalling and 6) Genetics

 



List by Barbora Knotkova et al.

Keystone Symposium – Metabolic and Nutritional Control of Development and Cell Fate

This preList contains preprints discussed during the Metabolic and Nutritional Control of Development and Cell Fate Keystone Symposia. This conference was organized by Lydia Finley and Ralph J. DeBerardinis and held in the Wylie Center and Tupper Manor at Endicott College, Beverly, MA, United States from May 7th to 9th 2025. This meeting marked the first in-person gathering of leading researchers exploring how metabolism influences development, including processes like cell fate, tissue patterning, and organ function, through nutrient availability and metabolic regulation. By integrating modern metabolic tools with genetic and epidemiological insights across model organisms, this event highlighted key mechanisms and identified open questions to advance the emerging field of developmental metabolism.

 



List by Virginia Savy, Martin Estermann

April in preprints – the CellBio edition

A group of preLighters, with expertise in different areas of cell biology, have worked together to create this preprint reading lists for researchers with an interest in cell biology. This month, categories include: 1) biochemistry/metabolism 2) cell cycle and division 3) cell organelles and organisation 4) cell signalling and mechanosensing 5) (epi)genetics

 



List by Vibha SINGH et al.

March in preprints – the CellBio edition

A group of preLighters, with expertise in different areas of cell biology, have worked together to create this preprint reading lists for researchers with an interest in cell biology. This month, categories include: 1) cancer biology 2) cell migration 3) cell organelles and organisation 4) cell signalling and mechanosensing 5) genetics and genomics 6) other

 



List by Girish Kale et al.

Biologists @ 100 conference preList

This preList aims to capture all preprints being discussed at the Biologists @100 conference in Liverpool, UK, either as part of the poster sessions or the (flash/short/full-length) talks.

 



List by Reinier Prosee, Jonathan Townson

Early 2025 preprints – the genetics & genomics edition

In this community-driven preList, a group of preLighters, with expertise in different areas of genetics and genomics have worked together to create this preprint reading list. Categories include: 1) bioinformatics 2) epigenetics 3) gene regulation 4) genomics 5) transcriptomics

 



List by Chee Kiang Ewe et al.

January in preprints – the CellBio edition

A group of preLighters, with expertise in different areas of cell biology, have worked together to create this preprint reading lists for researchers with an interest in cell biology. This month, categories include: 1) biochemistry/metabolism 2) cell migration 3) cell organelles and organisation 4) cell signalling and mechanosensing 5) genetics/gene expression

 



List by Barbora Knotkova et al.

End-of-year preprints – the genetics & genomics edition

In this community-driven preList, a group of preLighters, with expertise in different areas of genetics and genomics have worked together to create this preprint reading list. Categories include: 1) genomics 2) bioinformatics 3) gene regulation 4) epigenetics

 



List by Chee Kiang Ewe et al.

BSDB/GenSoc Spring Meeting 2024

A list of preprints highlighted at the British Society for Developmental Biology and Genetics Society joint Spring meeting 2024 at Warwick, UK.

 



List by Joyce Yu, Katherine Brown

BSCB-Biochemical Society 2024 Cell Migration meeting

This preList features preprints that were discussed and presented during the BSCB-Biochemical Society 2024 Cell Migration meeting in Birmingham, UK in April 2024. Kindly put together by Sara Morais da Silva, Reviews Editor at Journal of Cell Science.

 



List by Reinier Prosee

9th International Symposium on the Biology of Vertebrate Sex Determination

This preList contains preprints discussed during the 9th International Symposium on the Biology of Vertebrate Sex Determination. This conference was held in Kona, Hawaii from April 17th to 21st 2023.

 



List by Martin Estermann

Alumni picks – preLights 5th Birthday

This preList contains preprints that were picked and highlighted by preLights Alumni - an initiative that was set up to mark preLights 5th birthday. More entries will follow throughout February and March 2023.

 



List by Sergio Menchero et al.

Semmelweis Symposium 2022: 40th anniversary of international medical education at Semmelweis University

This preList contains preprints discussed during the 'Semmelweis Symposium 2022' (7-9 November), organised around the 40th anniversary of international medical education at Semmelweis University covering a wide range of topics.

 



List by Nándor Lipták

20th “Genetics Workshops in Hungary”, Szeged (25th, September)

In this annual conference, Hungarian geneticists, biochemists and biotechnologists presented their works. Link: http://group.szbk.u-szeged.hu/minikonf/archive/prg2021.pdf

 



List by Nándor Lipták

2nd Conference of the Visegrád Group Society for Developmental Biology

Preprints from the 2nd Conference of the Visegrád Group Society for Developmental Biology (2-5 September, 2021, Szeged, Hungary)

 



List by Nándor Lipták

EMBL Conference: From functional genomics to systems biology

Preprints presented at the virtual EMBL conference "from functional genomics and systems biology", 16-19 November 2020

 



List by Jesus Victorino

TAGC 2020

Preprints recently presented at the virtual Allied Genetics Conference, April 22-26, 2020. #TAGC20

 



List by Maiko Kitaoka et al.

ECFG15 – Fungal biology

Preprints presented at 15th European Conference on Fungal Genetics 17-20 February 2020 Rome

 



List by Hiral Shah

Autophagy

Preprints on autophagy and lysosomal degradation and its role in neurodegeneration and disease. Includes molecular mechanisms, upstream signalling and regulation as well as studies on pharmaceutical interventions to upregulate the process.

 



List by Sandra Malmgren Hill