Intrinsic factors and the embryonic environment influence the formation of extragonadal teratomas during gestation
Identifieur interne : 002C02 ( Ncbi/Curation ); précédent : 002C01; suivant : 002C03Intrinsic factors and the embryonic environment influence the formation of extragonadal teratomas during gestation
Auteurs : Constantinos Economou [Royaume-Uni] ; Anestis Tsakiridis [Royaume-Uni] ; Filip J. Wymeersch [Royaume-Uni] ; Sabrina Gordon-Keylock [Royaume-Uni] ; Robert E. Dewhurst ; Dawn Fisher [Royaume-Uni] ; Alexander Medvinsky [Royaume-Uni] ; Andrew Jh Smith [Royaume-Uni] ; Valerie Wilson [Royaume-Uni]Source :
- BMC Developmental Biology [ 1471-213X ] ; 2015.
Descripteurs français
- KwdFr :
- Animaux, Cellules souches embryonnaires (métabolisme), Cellules souches pluripotentes (métabolisme), Embryon de mammifère (anatomopathologie), Embryon de mammifère (métabolisme), Facteur de transcription Oct-3 (génétique), Facteur de transcription Oct-3 (métabolisme), Humains, Protéine homéotique Nanog, Protéines foetales (métabolisme), Protéines à domaine boîte-T (métabolisme), Protéines à homéodomaine (génétique), Queue (embryologie), Souris, Tératome (anatomopathologie), Tératome (métabolisme).
- MESH :
- anatomopathologie : Embryon de mammifère, Tératome.
- embryologie : Queue.
- génétique : Facteur de transcription Oct-3, Protéines à homéodomaine.
- métabolisme : Cellules souches embryonnaires, Cellules souches pluripotentes, Embryon de mammifère, Facteur de transcription Oct-3, Protéines foetales, Protéines à domaine boîte-T, Tératome.
- Animaux, Humains, Protéine homéotique Nanog, Souris.
English descriptors
- KwdEn :
- Animals, Embryo, Mammalian (metabolism), Embryo, Mammalian (pathology), Embryonic Stem Cells (metabolism), Fetal Proteins (metabolism), Homeodomain Proteins (genetics), Humans, Mice, Nanog Homeobox Protein, Octamer Transcription Factor-3 (genetics), Octamer Transcription Factor-3 (metabolism), Pluripotent Stem Cells (metabolism), T-Box Domain Proteins (metabolism), Tail (embryology), Teratoma (metabolism), Teratoma (pathology).
- MESH :
- chemical , genetics : Homeodomain Proteins, Octamer Transcription Factor-3.
- chemical , metabolism : Fetal Proteins, Octamer Transcription Factor-3, T-Box Domain Proteins.
- embryology : Tail.
- metabolism : Embryo, Mammalian, Embryonic Stem Cells, Pluripotent Stem Cells, Teratoma.
- pathology : Embryo, Mammalian, Teratoma.
- Animals, Humans, Mice, Nanog Homeobox Protein.
Abstract
Pluripotent cells are present in early embryos until the levels of the pluripotency regulator Oct4 drop at the beginning of somitogenesis. Elevating Oct4 levels in explanted post-pluripotent cells in vitro restores their pluripotency. Cultured pluripotent cells can participate in normal development when introduced into host embryos up to the end of gastrulation. In contrast, pluripotent cells efficiently seed malignant teratocarcinomas in adult animals. In humans, extragonadal teratomas and teratocarcinomas are most frequently found in the sacrococcygeal region of neonates, suggesting that these tumours originate from cells in the posterior of the embryo that either reactivate or fail to switch off their pluripotent status. However, experimental models for the persistence or reactivation of pluripotency during embryonic development are lacking.
We manually injected embryonic stem cells into conceptuses at E9.5 to test whether the presence of pluripotent cells at this stage correlates with teratocarcinoma formation. We then examined the effects of reactivating embryonic Oct4 expression ubiquitously or in combination with Nanog within the primitive streak (PS)/tail bud (TB) using a transgenic mouse line and embryo chimeras carrying a PS/TB-specific heterologous gene expression cassette respectively.
Here, we show that pluripotent cells seed teratomas in post-gastrulation embryos. However, at these stages, induced ubiquitous expression of Oct4 does not lead to restoration of pluripotency (indicated by Nanog expression) and tumour formation
Our findings show that although pluripotent cells with teratocarcinogenic potential can be produced in vitro by the overexpression of pluripotency regulators in explanted somitogenesis-stage somatic cells, the
The online version of this article (doi:10.1186/s12861-015-0084-7) contains supplementary material, which is available to authorized users.
Url:
DOI: 10.1186/s12861-015-0084-7
PubMed: 26453549
PubMed Central: 4599726
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Robert E. Dewhurst<affiliation><nlm:aff id="Aff2">Drug Discovery Unit, Telethon Kids Institute, PO Box 855, West Perth, WA 6872 Australia</nlm:aff>
<wicri:noCountry code="subfield">WA 6872 Australia</wicri:noCountry>
</affiliation>
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<series><title level="j">BMC Developmental Biology</title>
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<profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Animals</term>
<term>Embryo, Mammalian (metabolism)</term>
<term>Embryo, Mammalian (pathology)</term>
<term>Embryonic Stem Cells (metabolism)</term>
<term>Fetal Proteins (metabolism)</term>
<term>Homeodomain Proteins (genetics)</term>
<term>Humans</term>
<term>Mice</term>
<term>Nanog Homeobox Protein</term>
<term>Octamer Transcription Factor-3 (genetics)</term>
<term>Octamer Transcription Factor-3 (metabolism)</term>
<term>Pluripotent Stem Cells (metabolism)</term>
<term>T-Box Domain Proteins (metabolism)</term>
<term>Tail (embryology)</term>
<term>Teratoma (metabolism)</term>
<term>Teratoma (pathology)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr"><term>Animaux</term>
<term>Cellules souches embryonnaires (métabolisme)</term>
<term>Cellules souches pluripotentes (métabolisme)</term>
<term>Embryon de mammifère (anatomopathologie)</term>
<term>Embryon de mammifère (métabolisme)</term>
<term>Facteur de transcription Oct-3 (génétique)</term>
<term>Facteur de transcription Oct-3 (métabolisme)</term>
<term>Humains</term>
<term>Protéine homéotique Nanog</term>
<term>Protéines foetales (métabolisme)</term>
<term>Protéines à domaine boîte-T (métabolisme)</term>
<term>Protéines à homéodomaine (génétique)</term>
<term>Queue (embryologie)</term>
<term>Souris</term>
<term>Tératome (anatomopathologie)</term>
<term>Tératome (métabolisme)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en"><term>Homeodomain Proteins</term>
<term>Octamer Transcription Factor-3</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Fetal Proteins</term>
<term>Octamer Transcription Factor-3</term>
<term>T-Box Domain Proteins</term>
</keywords>
<keywords scheme="MESH" qualifier="anatomopathologie" xml:lang="fr"><term>Embryon de mammifère</term>
<term>Tératome</term>
</keywords>
<keywords scheme="MESH" qualifier="embryologie" xml:lang="fr"><term>Queue</term>
</keywords>
<keywords scheme="MESH" qualifier="embryology" xml:lang="en"><term>Tail</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr"><term>Facteur de transcription Oct-3</term>
<term>Protéines à homéodomaine</term>
</keywords>
<keywords scheme="MESH" qualifier="metabolism" xml:lang="en"><term>Embryo, Mammalian</term>
<term>Embryonic Stem Cells</term>
<term>Pluripotent Stem Cells</term>
<term>Teratoma</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>Cellules souches embryonnaires</term>
<term>Cellules souches pluripotentes</term>
<term>Embryon de mammifère</term>
<term>Facteur de transcription Oct-3</term>
<term>Protéines foetales</term>
<term>Protéines à domaine boîte-T</term>
<term>Tératome</term>
</keywords>
<keywords scheme="MESH" qualifier="pathology" xml:lang="en"><term>Embryo, Mammalian</term>
<term>Teratoma</term>
</keywords>
<keywords scheme="MESH" xml:lang="en"><term>Animals</term>
<term>Humans</term>
<term>Mice</term>
<term>Nanog Homeobox Protein</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr"><term>Animaux</term>
<term>Humains</term>
<term>Protéine homéotique Nanog</term>
<term>Souris</term>
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<front><div type="abstract" xml:lang="en"><sec><title>Background</title>
<p>Pluripotent cells are present in early embryos until the levels of the pluripotency regulator Oct4 drop at the beginning of somitogenesis. Elevating Oct4 levels in explanted post-pluripotent cells in vitro restores their pluripotency. Cultured pluripotent cells can participate in normal development when introduced into host embryos up to the end of gastrulation. In contrast, pluripotent cells efficiently seed malignant teratocarcinomas in adult animals. In humans, extragonadal teratomas and teratocarcinomas are most frequently found in the sacrococcygeal region of neonates, suggesting that these tumours originate from cells in the posterior of the embryo that either reactivate or fail to switch off their pluripotent status. However, experimental models for the persistence or reactivation of pluripotency during embryonic development are lacking. </p>
</sec>
<sec><title>Methods</title>
<p>We manually injected embryonic stem cells into conceptuses at E9.5 to test whether the presence of pluripotent cells at this stage correlates with teratocarcinoma formation. We then examined the effects of reactivating embryonic Oct4 expression ubiquitously or in combination with Nanog within the primitive streak (PS)/tail bud (TB) using a transgenic mouse line and embryo chimeras carrying a PS/TB-specific heterologous gene expression cassette respectively.</p>
</sec>
<sec><title>Results</title>
<p>Here, we show that pluripotent cells seed teratomas in post-gastrulation embryos. However, at these stages, induced ubiquitous expression of Oct4 does not lead to restoration of pluripotency (indicated by Nanog expression) and tumour formation <italic>in utero</italic>
, but instead causes a severe phenotype in the extending anteroposterior axis. Use of a more restricted T(Bra) promoter transgenic system enabling inducible ectopic expression of Oct4 and Nanog specifically in the posteriorly-located primitive streak (PS) and tail bud (TB) led to similar axial malformations to those induced by Oct4 alone. These cells underwent induction of pluripotency marker expression in Epiblast Stem Cell (EpiSC) explants derived from somitogenesis-stage embryos, but no teratocarcinoma formation was observed <italic>in vivo</italic>
.</p>
</sec>
<sec><title>Conclusions</title>
<p>Our findings show that although pluripotent cells with teratocarcinogenic potential can be produced in vitro by the overexpression of pluripotency regulators in explanted somitogenesis-stage somatic cells, the <italic>in vivo</italic>
induction of these genes does not yield tumours. This suggests a restrictive regulatory role of the embryonic microenvironment in the induction of pluripotency.</p>
</sec>
<sec><title>Electronic supplementary material</title>
<p>The online version of this article (doi:10.1186/s12861-015-0084-7) contains supplementary material, which is available to authorized users.</p>
</sec>
</div>
</front>
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