An integrated genome-wide multi-omics analysis of gene expression dynamics in the preimplantation mouse embryo

Steffen Israel, Mathias Ernst, Olympia E Psathaki, Hannes C A Drexler, Ellen Casser, Yutaka Suzuki, Wojciech Makalowski, Michele Boiani, Georg Fuellen, Leila Taher

Research output: Contribution to journalArticleResearchpeer-review

Abstract

Early mouse embryos have an atypical translational machinery that consists of cytoplasmic lattices and is poorly competent for translation. Hence, the impact of transcriptomic changes on the operational level of proteins is predicted to be relatively modest. To investigate this, we performed liquid chromatography-tandem mass spectrometry and mRNA sequencing at seven developmental stages, from the mature oocyte to the blastocyst, and independently validated our data by immunofluorescence and qPCR. We detected and quantified 6,550 proteins and 20,535 protein-coding transcripts. In contrast to the transcriptome - where changes occur early, mostly at the 2-cell stage - our data indicate that the most substantial changes in the proteome take place towards later stages, between the morula and blastocyst. We also found little to no concordance between the changes in protein and transcript levels, especially for early stages, but observed that the concordance increased towards the morula and blastocyst, as did the number of free ribosomes. These results are consistent with the cytoplasmic lattice-to-free ribosome transition being a key mediator of developmental regulation. Finally, we show how these data can be used to appraise the strengths and limitations of mRNA-based studies of pre-implantation development and expand on the list of known developmental markers.

Original languageEnglish
Pages (from-to)13356
JournalScientific reports
Volume9
Issue number1
DOIs
Publication statusPublished - 16 Sep 2019
Externally publishedYes

Fingerprint

Blastocyst
Genome
Gene Expression
Morula
Ribosomes
Proteins
Messenger RNA
Proteome
Tandem Mass Spectrometry
Transcriptome
Liquid Chromatography
Oocytes
Fluorescent Antibody Technique
Embryonic Structures

Cite this

An integrated genome-wide multi-omics analysis of gene expression dynamics in the preimplantation mouse embryo. / Israel, Steffen; Ernst, Mathias; Psathaki, Olympia E; Drexler, Hannes C A; Casser, Ellen; Suzuki, Yutaka; Makalowski, Wojciech; Boiani, Michele; Fuellen, Georg; Taher, Leila.

In: Scientific reports, Vol. 9, No. 1, 16.09.2019, p. 13356.

Research output: Contribution to journalArticleResearchpeer-review

Israel, S, Ernst, M, Psathaki, OE, Drexler, HCA, Casser, E, Suzuki, Y, Makalowski, W, Boiani, M, Fuellen, G & Taher, L 2019, 'An integrated genome-wide multi-omics analysis of gene expression dynamics in the preimplantation mouse embryo' Scientific reports, vol. 9, no. 1, pp. 13356. https://doi.org/10.1038/s41598-019-49817-3
Israel, Steffen ; Ernst, Mathias ; Psathaki, Olympia E ; Drexler, Hannes C A ; Casser, Ellen ; Suzuki, Yutaka ; Makalowski, Wojciech ; Boiani, Michele ; Fuellen, Georg ; Taher, Leila. / An integrated genome-wide multi-omics analysis of gene expression dynamics in the preimplantation mouse embryo. In: Scientific reports. 2019 ; Vol. 9, No. 1. pp. 13356.
@article{2afedc531abf41ca8324fb3ab1cf4d51,
title = "An integrated genome-wide multi-omics analysis of gene expression dynamics in the preimplantation mouse embryo",
abstract = "Early mouse embryos have an atypical translational machinery that consists of cytoplasmic lattices and is poorly competent for translation. Hence, the impact of transcriptomic changes on the operational level of proteins is predicted to be relatively modest. To investigate this, we performed liquid chromatography-tandem mass spectrometry and mRNA sequencing at seven developmental stages, from the mature oocyte to the blastocyst, and independently validated our data by immunofluorescence and qPCR. We detected and quantified 6,550 proteins and 20,535 protein-coding transcripts. In contrast to the transcriptome - where changes occur early, mostly at the 2-cell stage - our data indicate that the most substantial changes in the proteome take place towards later stages, between the morula and blastocyst. We also found little to no concordance between the changes in protein and transcript levels, especially for early stages, but observed that the concordance increased towards the morula and blastocyst, as did the number of free ribosomes. These results are consistent with the cytoplasmic lattice-to-free ribosome transition being a key mediator of developmental regulation. Finally, we show how these data can be used to appraise the strengths and limitations of mRNA-based studies of pre-implantation development and expand on the list of known developmental markers.",
author = "Steffen Israel and Mathias Ernst and Psathaki, {Olympia E} and Drexler, {Hannes C A} and Ellen Casser and Yutaka Suzuki and Wojciech Makalowski and Michele Boiani and Georg Fuellen and Leila Taher",
year = "2019",
month = "9",
day = "16",
doi = "10.1038/s41598-019-49817-3",
language = "English",
volume = "9",
pages = "13356",
journal = "Scientific reports",
issn = "2045-2322",
publisher = "Nature Publishing Group",
number = "1",

}

TY - JOUR

T1 - An integrated genome-wide multi-omics analysis of gene expression dynamics in the preimplantation mouse embryo

AU - Israel, Steffen

AU - Ernst, Mathias

AU - Psathaki, Olympia E

AU - Drexler, Hannes C A

AU - Casser, Ellen

AU - Suzuki, Yutaka

AU - Makalowski, Wojciech

AU - Boiani, Michele

AU - Fuellen, Georg

AU - Taher, Leila

PY - 2019/9/16

Y1 - 2019/9/16

N2 - Early mouse embryos have an atypical translational machinery that consists of cytoplasmic lattices and is poorly competent for translation. Hence, the impact of transcriptomic changes on the operational level of proteins is predicted to be relatively modest. To investigate this, we performed liquid chromatography-tandem mass spectrometry and mRNA sequencing at seven developmental stages, from the mature oocyte to the blastocyst, and independently validated our data by immunofluorescence and qPCR. We detected and quantified 6,550 proteins and 20,535 protein-coding transcripts. In contrast to the transcriptome - where changes occur early, mostly at the 2-cell stage - our data indicate that the most substantial changes in the proteome take place towards later stages, between the morula and blastocyst. We also found little to no concordance between the changes in protein and transcript levels, especially for early stages, but observed that the concordance increased towards the morula and blastocyst, as did the number of free ribosomes. These results are consistent with the cytoplasmic lattice-to-free ribosome transition being a key mediator of developmental regulation. Finally, we show how these data can be used to appraise the strengths and limitations of mRNA-based studies of pre-implantation development and expand on the list of known developmental markers.

AB - Early mouse embryos have an atypical translational machinery that consists of cytoplasmic lattices and is poorly competent for translation. Hence, the impact of transcriptomic changes on the operational level of proteins is predicted to be relatively modest. To investigate this, we performed liquid chromatography-tandem mass spectrometry and mRNA sequencing at seven developmental stages, from the mature oocyte to the blastocyst, and independently validated our data by immunofluorescence and qPCR. We detected and quantified 6,550 proteins and 20,535 protein-coding transcripts. In contrast to the transcriptome - where changes occur early, mostly at the 2-cell stage - our data indicate that the most substantial changes in the proteome take place towards later stages, between the morula and blastocyst. We also found little to no concordance between the changes in protein and transcript levels, especially for early stages, but observed that the concordance increased towards the morula and blastocyst, as did the number of free ribosomes. These results are consistent with the cytoplasmic lattice-to-free ribosome transition being a key mediator of developmental regulation. Finally, we show how these data can be used to appraise the strengths and limitations of mRNA-based studies of pre-implantation development and expand on the list of known developmental markers.

U2 - 10.1038/s41598-019-49817-3

DO - 10.1038/s41598-019-49817-3

M3 - Article

VL - 9

SP - 13356

JO - Scientific reports

JF - Scientific reports

SN - 2045-2322

IS - 1

ER -