Deciphering lineage specification during early embryogenesis in mouse gastruloids using multilayered proteomics

Suzan Stelloo; Maria Teresa Alejo-Vinogradova; Charlotte A G H van Gelder; Dick W Zijlmans; Marek J van Oostrom; Juan Manuel Valverde; Lieke A Lamers; Teja Rus; Paula Sobrevals Alcaraz; Tilman Schäfers; Cristina Furlan; Pascal W T C Jansen; Marijke P A Baltissen; Katharina F Sonnen; Boudewijn Burgering; Maarten A F M Altelaar; Harmjan R Vos; Michiel Vermeulen

doi:10.1016/j.stem.2024.04.017

Deciphering lineage specification during early embryogenesis in mouse gastruloids using multilayered proteomics

Suzan Stelloo, Maria Teresa Alejo-Vinogradova, Charlotte A G H van Gelder, Dick W Zijlmans, Marek J van Oostrom, Juan Manuel Valverde, Lieke A Lamers, Teja Rus, Paula Sobrevals Alcaraz, Tilman Schäfers, Cristina Furlan, Pascal W T C Jansen, Marijke P A Baltissen, Katharina F Sonnen, Boudewijn Burgering, Maarten A F M Altelaar, Harmjan R Vos, Michiel Vermeulen

Hubrecht Institute

Onderzoeksoutput: Bijdrage aan wetenschappelijk tijdschrift/periodieke uitgave › Artikel › Wetenschappelijk › peer review

1 Citaat (Scopus)

Samenvatting

Gastrulation is a critical stage in embryonic development during which the germ layers are established. Advances in sequencing technologies led to the identification of gene regulatory programs that control the emergence of the germ layers and their derivatives. However, proteome-based studies of early mammalian development are scarce. To overcome this, we utilized gastruloids and a multilayered mass spectrometry-based proteomics approach to investigate the global dynamics of (phospho) protein expression during gastruloid differentiation. Our findings revealed many proteins with temporal expression and unique expression profiles for each germ layer, which we also validated using single-cell proteomics technology. Additionally, we profiled enhancer interaction landscapes using P300 proximity labeling, which revealed numerous gastruloid-specific transcription factors and chromatin remodelers. Subsequent degron-based perturbations combined with single-cell RNA sequencing (scRNA-seq) identified a critical role for ZEB2 in mouse and human somitogenesis. Overall, this study provides a rich resource for developmental and synthetic biology communities endeavoring to understand mammalian embryogenesis.

Originele taal-2	Engels
Pagina's (van-tot)	1072-1090.e8
Tijdschrift	Cell Stem Cell
Volume	31
Nummer van het tijdschrift	7
DOI's	https://doi.org/10.1016/j.stem.2024.04.017
Status	Gepubliceerd - 05 jul. 2024

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10.1016/j.stem.2024.04.017

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Stelloo, S., Alejo-Vinogradova, M. T., van Gelder, C. A. G. H., Zijlmans, D. W., van Oostrom, M. J., Valverde, J. M., Lamers, L. A., Rus, T., Sobrevals Alcaraz, P., Schäfers, T., Furlan, C., Jansen, P. W. T. C., Baltissen, M. P. A., Sonnen, K. F., Burgering, B., Altelaar, M. A. F. M., Vos, H. R., & Vermeulen, M. (2024). Deciphering lineage specification during early embryogenesis in mouse gastruloids using multilayered proteomics. Cell Stem Cell, 31(7), 1072-1090.e8. https://doi.org/10.1016/j.stem.2024.04.017

@article{577937d7feaf4b05884d3c62cc7b5c9f,

title = "Deciphering lineage specification during early embryogenesis in mouse gastruloids using multilayered proteomics",

abstract = "Gastrulation is a critical stage in embryonic development during which the germ layers are established. Advances in sequencing technologies led to the identification of gene regulatory programs that control the emergence of the germ layers and their derivatives. However, proteome-based studies of early mammalian development are scarce. To overcome this, we utilized gastruloids and a multilayered mass spectrometry-based proteomics approach to investigate the global dynamics of (phospho) protein expression during gastruloid differentiation. Our findings revealed many proteins with temporal expression and unique expression profiles for each germ layer, which we also validated using single-cell proteomics technology. Additionally, we profiled enhancer interaction landscapes using P300 proximity labeling, which revealed numerous gastruloid-specific transcription factors and chromatin remodelers. Subsequent degron-based perturbations combined with single-cell RNA sequencing (scRNA-seq) identified a critical role for ZEB2 in mouse and human somitogenesis. Overall, this study provides a rich resource for developmental and synthetic biology communities endeavoring to understand mammalian embryogenesis.",

keywords = "Animals, Proteomics, Mice, Embryonic Development/genetics, Cell Lineage, Gene Expression Regulation, Developmental, Humans, Single-Cell Analysis, Cell Differentiation, Gastrula/metabolism, Gastrulation",

author = "Suzan Stelloo and Alejo-Vinogradova, {Maria Teresa} and {van Gelder}, {Charlotte A G H} and Zijlmans, {Dick W} and {van Oostrom}, {Marek J} and Valverde, {Juan Manuel} and Lamers, {Lieke A} and Teja Rus and {Sobrevals Alcaraz}, Paula and Tilman Sch{\"a}fers and Cristina Furlan and Jansen, {Pascal W T C} and Baltissen, {Marijke P A} and Sonnen, {Katharina F} and Boudewijn Burgering and Altelaar, {Maarten A F M} and Vos, {Harmjan R} and Michiel Vermeulen",

year = "2024",

month = jul,

day = "5",

doi = "10.1016/j.stem.2024.04.017",

language = "English",

volume = "31",

pages = "1072--1090.e8",

journal = "Cell Stem Cell",

issn = "1934-5909",

publisher = "Cell Press",

number = "7",

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Stelloo, S, Alejo-Vinogradova, MT, van Gelder, CAGH, Zijlmans, DW, van Oostrom, MJ, Valverde, JM, Lamers, LA, Rus, T, Sobrevals Alcaraz, P, Schäfers, T, Furlan, C, Jansen, PWTC, Baltissen, MPA, Sonnen, KF, Burgering, B, Altelaar, MAFM, Vos, HR & Vermeulen, M 2024, 'Deciphering lineage specification during early embryogenesis in mouse gastruloids using multilayered proteomics', Cell Stem Cell, vol. 31, nr. 7, blz. 1072-1090.e8. https://doi.org/10.1016/j.stem.2024.04.017

Deciphering lineage specification during early embryogenesis in mouse gastruloids using multilayered proteomics. / Stelloo, Suzan; Alejo-Vinogradova, Maria Teresa; van Gelder, Charlotte A G H et al.
In: Cell Stem Cell, Vol. 31, Nr. 7, 05.07.2024, blz. 1072-1090.e8.

Onderzoeksoutput: Bijdrage aan wetenschappelijk tijdschrift/periodieke uitgave › Artikel › Wetenschappelijk › peer review

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T1 - Deciphering lineage specification during early embryogenesis in mouse gastruloids using multilayered proteomics

AU - Stelloo, Suzan

AU - Alejo-Vinogradova, Maria Teresa

AU - van Gelder, Charlotte A G H

AU - Zijlmans, Dick W

AU - van Oostrom, Marek J

AU - Valverde, Juan Manuel

AU - Lamers, Lieke A

AU - Rus, Teja

AU - Sobrevals Alcaraz, Paula

AU - Schäfers, Tilman

AU - Furlan, Cristina

AU - Jansen, Pascal W T C

AU - Baltissen, Marijke P A

AU - Sonnen, Katharina F

AU - Burgering, Boudewijn

AU - Altelaar, Maarten A F M

AU - Vos, Harmjan R

AU - Vermeulen, Michiel

PY - 2024/7/5

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N2 - Gastrulation is a critical stage in embryonic development during which the germ layers are established. Advances in sequencing technologies led to the identification of gene regulatory programs that control the emergence of the germ layers and their derivatives. However, proteome-based studies of early mammalian development are scarce. To overcome this, we utilized gastruloids and a multilayered mass spectrometry-based proteomics approach to investigate the global dynamics of (phospho) protein expression during gastruloid differentiation. Our findings revealed many proteins with temporal expression and unique expression profiles for each germ layer, which we also validated using single-cell proteomics technology. Additionally, we profiled enhancer interaction landscapes using P300 proximity labeling, which revealed numerous gastruloid-specific transcription factors and chromatin remodelers. Subsequent degron-based perturbations combined with single-cell RNA sequencing (scRNA-seq) identified a critical role for ZEB2 in mouse and human somitogenesis. Overall, this study provides a rich resource for developmental and synthetic biology communities endeavoring to understand mammalian embryogenesis.

AB - Gastrulation is a critical stage in embryonic development during which the germ layers are established. Advances in sequencing technologies led to the identification of gene regulatory programs that control the emergence of the germ layers and their derivatives. However, proteome-based studies of early mammalian development are scarce. To overcome this, we utilized gastruloids and a multilayered mass spectrometry-based proteomics approach to investigate the global dynamics of (phospho) protein expression during gastruloid differentiation. Our findings revealed many proteins with temporal expression and unique expression profiles for each germ layer, which we also validated using single-cell proteomics technology. Additionally, we profiled enhancer interaction landscapes using P300 proximity labeling, which revealed numerous gastruloid-specific transcription factors and chromatin remodelers. Subsequent degron-based perturbations combined with single-cell RNA sequencing (scRNA-seq) identified a critical role for ZEB2 in mouse and human somitogenesis. Overall, this study provides a rich resource for developmental and synthetic biology communities endeavoring to understand mammalian embryogenesis.

KW - Animals

KW - Proteomics

KW - Mice

KW - Embryonic Development/genetics

KW - Cell Lineage

KW - Gene Expression Regulation, Developmental

KW - Humans

KW - Single-Cell Analysis

KW - Cell Differentiation

KW - Gastrula/metabolism

KW - Gastrulation

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DO - 10.1016/j.stem.2024.04.017

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SN - 1934-5909

VL - 31

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JF - Cell Stem Cell

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