Four simple rules that are sufficient to generate the mammalian blastocyst

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Standard

Four simple rules that are sufficient to generate the mammalian blastocyst. / Nissen, Silas Boye; Perera Pérez, Marta; Martin Gonzalez, Javier; Morgani, Sophie Maria Christina; Jensen, Mogens Høgh; Sneppen, Kim; Brickman, Joshua Mark; Trusina, Ala.

I: PLOS Biology, Bind 15, Nr. 7, e2000737, 12.07.2017, s. 1-30.

Publikation: Bidrag til tidsskriftTidsskriftartikelForskningfagfællebedømt

Harvard

Nissen, SB, Perera Pérez, M, Martin Gonzalez, J, Morgani, SMC, Jensen, MH, Sneppen, K, Brickman, JM & Trusina, A 2017, 'Four simple rules that are sufficient to generate the mammalian blastocyst', PLOS Biology, bind 15, nr. 7, e2000737, s. 1-30. https://doi.org/10.1371/journal.pbio.2000737

APA

Nissen, S. B., Perera Pérez, M., Martin Gonzalez, J., Morgani, S. M. C., Jensen, M. H., Sneppen, K., Brickman, J. M., & Trusina, A. (2017). Four simple rules that are sufficient to generate the mammalian blastocyst. PLOS Biology, 15(7), 1-30. [e2000737]. https://doi.org/10.1371/journal.pbio.2000737

Vancouver

Nissen SB, Perera Pérez M, Martin Gonzalez J, Morgani SMC, Jensen MH, Sneppen K o.a. Four simple rules that are sufficient to generate the mammalian blastocyst. PLOS Biology. 2017 jul 12;15(7):1-30. e2000737. https://doi.org/10.1371/journal.pbio.2000737

Author

Nissen, Silas Boye ; Perera Pérez, Marta ; Martin Gonzalez, Javier ; Morgani, Sophie Maria Christina ; Jensen, Mogens Høgh ; Sneppen, Kim ; Brickman, Joshua Mark ; Trusina, Ala. / Four simple rules that are sufficient to generate the mammalian blastocyst. I: PLOS Biology. 2017 ; Bind 15, Nr. 7. s. 1-30.

Bibtex

@article{3ce49541b3204dfdaa5b146658a72a20,
title = "Four simple rules that are sufficient to generate the mammalian blastocyst",
abstract = "Early mammalian development is both highly regulative and self-organizing. It involves the interplay of cell position, predetermined gene regulatory networks, and environmental interactions to generate the physical arrangement of the blastocyst with precise timing. However, this process occurs in the absence of maternal information and in the presence of transcriptional stochasticity. How does the preimplantation embryo ensure robust, reproducible development in this context? It utilizes a versatile toolbox that includes complex intracellular networks coupled to cell—cell communication, segregation by differential adhesion, and apoptosis. Here, we ask whether a minimal set of developmental rules based on this toolbox is sufficient for successful blastocyst development, and to what extent these rules can explain mutant and experimental phenotypes. We implemented experimentally reported mechanisms for polarity, cell—cell signaling, adhesion, and apoptosis as a set of developmental rules in an agent-based in silico model of physically interacting cells. We find that this model quantitatively reproduces specific mutant phenotypes and provides an explanation for the emergence of heterogeneity without requiring any initial transcriptional variation. It also suggests that a fixed time point for the cells{\textquoteright} competence of fibroblast growth factor (FGF)/extracellular signal—regulated kinase (ERK) sets an embryonic clock that enables certain scaling phenomena, a concept that we evaluate quantitatively by manipulating embryos in vitro. Based on these observations, we conclude that the minimal set of rules enables the embryo to experiment with stochastic gene expression and could provide the robustness necessary for the evolutionary diversification of the preimplantation gene regulatory network.",
author = "Nissen, {Silas Boye} and {Perera P{\'e}rez}, Marta and {Martin Gonzalez}, Javier and Morgani, {Sophie Maria Christina} and Jensen, {Mogens H{\o}gh} and Kim Sneppen and Brickman, {Joshua Mark} and Ala Trusina",
year = "2017",
month = jul,
day = "12",
doi = "10.1371/journal.pbio.2000737",
language = "English",
volume = "15",
pages = "1--30",
journal = "P L o S Biology",
issn = "1544-9173",
publisher = "Public Library of Science",
number = "7",

}

RIS

TY - JOUR

T1 - Four simple rules that are sufficient to generate the mammalian blastocyst

AU - Nissen, Silas Boye

AU - Perera Pérez, Marta

AU - Martin Gonzalez, Javier

AU - Morgani, Sophie Maria Christina

AU - Jensen, Mogens Høgh

AU - Sneppen, Kim

AU - Brickman, Joshua Mark

AU - Trusina, Ala

PY - 2017/7/12

Y1 - 2017/7/12

N2 - Early mammalian development is both highly regulative and self-organizing. It involves the interplay of cell position, predetermined gene regulatory networks, and environmental interactions to generate the physical arrangement of the blastocyst with precise timing. However, this process occurs in the absence of maternal information and in the presence of transcriptional stochasticity. How does the preimplantation embryo ensure robust, reproducible development in this context? It utilizes a versatile toolbox that includes complex intracellular networks coupled to cell—cell communication, segregation by differential adhesion, and apoptosis. Here, we ask whether a minimal set of developmental rules based on this toolbox is sufficient for successful blastocyst development, and to what extent these rules can explain mutant and experimental phenotypes. We implemented experimentally reported mechanisms for polarity, cell—cell signaling, adhesion, and apoptosis as a set of developmental rules in an agent-based in silico model of physically interacting cells. We find that this model quantitatively reproduces specific mutant phenotypes and provides an explanation for the emergence of heterogeneity without requiring any initial transcriptional variation. It also suggests that a fixed time point for the cells’ competence of fibroblast growth factor (FGF)/extracellular signal—regulated kinase (ERK) sets an embryonic clock that enables certain scaling phenomena, a concept that we evaluate quantitatively by manipulating embryos in vitro. Based on these observations, we conclude that the minimal set of rules enables the embryo to experiment with stochastic gene expression and could provide the robustness necessary for the evolutionary diversification of the preimplantation gene regulatory network.

AB - Early mammalian development is both highly regulative and self-organizing. It involves the interplay of cell position, predetermined gene regulatory networks, and environmental interactions to generate the physical arrangement of the blastocyst with precise timing. However, this process occurs in the absence of maternal information and in the presence of transcriptional stochasticity. How does the preimplantation embryo ensure robust, reproducible development in this context? It utilizes a versatile toolbox that includes complex intracellular networks coupled to cell—cell communication, segregation by differential adhesion, and apoptosis. Here, we ask whether a minimal set of developmental rules based on this toolbox is sufficient for successful blastocyst development, and to what extent these rules can explain mutant and experimental phenotypes. We implemented experimentally reported mechanisms for polarity, cell—cell signaling, adhesion, and apoptosis as a set of developmental rules in an agent-based in silico model of physically interacting cells. We find that this model quantitatively reproduces specific mutant phenotypes and provides an explanation for the emergence of heterogeneity without requiring any initial transcriptional variation. It also suggests that a fixed time point for the cells’ competence of fibroblast growth factor (FGF)/extracellular signal—regulated kinase (ERK) sets an embryonic clock that enables certain scaling phenomena, a concept that we evaluate quantitatively by manipulating embryos in vitro. Based on these observations, we conclude that the minimal set of rules enables the embryo to experiment with stochastic gene expression and could provide the robustness necessary for the evolutionary diversification of the preimplantation gene regulatory network.

U2 - 10.1371/journal.pbio.2000737

DO - 10.1371/journal.pbio.2000737

M3 - Journal article

C2 - 28700688

VL - 15

SP - 1

EP - 30

JO - P L o S Biology

JF - P L o S Biology

SN - 1544-9173

IS - 7

M1 - e2000737

ER -

ID: 180817665