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Cell dynamics and gene expression control in tissue homeostasis and development.

Rué P, Martinez Arias A - Mol. Syst. Biol. (2015)

Bottom Line: While some of the basic principles underlying these processes developing and maintaining these organs are known, much remains to be learnt from how cells encode the necessary information and use it to attain those complex but reproducible arrangements.We propose a framework, involving the existence of a transition state in which cells are more susceptible to signals that can affect their gene expression state and influence their cell fate decisions.This framework, which also applies to systems much more amenable to quantitative analysis like differentiating embryonic stem cells, links gene expression programmes with cell population dynamics.

View Article: PubMed Central - PubMed

Affiliation: Department of Genetics, University of Cambridge, Cambridge, UK.

No MeSH data available.


Related in: MedlinePlus

Vertebrate retinogenesis(A) During the development of the vertebrate retina, there is an initial phase where most of the divisions are symmetric proliferative leading to progenitor amplification. As development proceeds, proliferation slows down. When individual cells stop dividing, they differentiate and this leads to a link between the different cell types and the growth of the tissue (Livesey & Cepko, 2001). (B) Throughout retinal development, a reproducible sequence of overlapping temporal windows of specific fate adoption by differentiating cells is established. An early differentiating cell can become a retinal ganglion cell (RGC), a horizontal cell (HC), a rod photoreceptor (PR) or an amacrine cell (AC), whereas if it differentiates later, it can become a bipolar cell (BC), a Müller cell (MC) or a cone PR; that is, there appears to be an overlap between these windows of opportunities (adapted from Cepko et al, 1996). (C) Recent accurate single-cell tracing assays have unveiled complex lineage compositions in the zebrafish retina development. Three out of 60 clones from He et al (2012) are shown. Despite the observed high variability of clone compositions, there are some remarkable trends; for example, RGCs appear through asymmetric divisions, PRs through symmetric ones.
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fig03: Vertebrate retinogenesis(A) During the development of the vertebrate retina, there is an initial phase where most of the divisions are symmetric proliferative leading to progenitor amplification. As development proceeds, proliferation slows down. When individual cells stop dividing, they differentiate and this leads to a link between the different cell types and the growth of the tissue (Livesey & Cepko, 2001). (B) Throughout retinal development, a reproducible sequence of overlapping temporal windows of specific fate adoption by differentiating cells is established. An early differentiating cell can become a retinal ganglion cell (RGC), a horizontal cell (HC), a rod photoreceptor (PR) or an amacrine cell (AC), whereas if it differentiates later, it can become a bipolar cell (BC), a Müller cell (MC) or a cone PR; that is, there appears to be an overlap between these windows of opportunities (adapted from Cepko et al, 1996). (C) Recent accurate single-cell tracing assays have unveiled complex lineage compositions in the zebrafish retina development. Three out of 60 clones from He et al (2012) are shown. Despite the observed high variability of clone compositions, there are some remarkable trends; for example, RGCs appear through asymmetric divisions, PRs through symmetric ones.

Mentions: The retina is a structure with millions of cells structurally diversified into seven main functionally distinct cell types that are allocated in specific proportions and positions to generate a functioning organ (Masland & Raviola, 2000; Masland, 2001). The structure emerges over time during embryogenesis and continues growth after birth from a collection of retinal progenitor cells (RPG, P) which display two essential behaviours (Fig3A, Livesey & Cepko, 2001; Centanin et al, 2011; Centanin & Wittbrodt, 2014). The first one relates to the patterns of divisions which early on amplify the P compartment (P→PP, Fig3A and B) while towards the end of development lean towards terminally differentiating symmetric divisions (P→DD) (Livesey & Cepko, 2001; Rapaport et al, 2004) and in between exhibit a mixture of symmetric and asymmetric (P→PD) divisions, with the corresponding proportions varying over time. The second behaviour is a reproducible sequence of fates adopted by differentiating cells; although to date there is no way to reliably predict the fate of a specific cell when it divides, it is known that, at a given time, a cell always chooses among a restricted number of fates and that the repertoire of available fates changes with time (Cepko et al, 1996; Livesey & Cepko, 2001, Fig3B and C). These observations led to a model suggesting that as development proceeds, an intrinsically defined competence to obtain particular fates changes and this is what determines the fate of a differentiating cell. According to this model, a pattern of differentiating (DD) divisions is superimposed upon this shifting window of competence resulting in a loose but reproducible sequence of fates (Livesey & Cepko, 2001).


Cell dynamics and gene expression control in tissue homeostasis and development.

Rué P, Martinez Arias A - Mol. Syst. Biol. (2015)

Vertebrate retinogenesis(A) During the development of the vertebrate retina, there is an initial phase where most of the divisions are symmetric proliferative leading to progenitor amplification. As development proceeds, proliferation slows down. When individual cells stop dividing, they differentiate and this leads to a link between the different cell types and the growth of the tissue (Livesey & Cepko, 2001). (B) Throughout retinal development, a reproducible sequence of overlapping temporal windows of specific fate adoption by differentiating cells is established. An early differentiating cell can become a retinal ganglion cell (RGC), a horizontal cell (HC), a rod photoreceptor (PR) or an amacrine cell (AC), whereas if it differentiates later, it can become a bipolar cell (BC), a Müller cell (MC) or a cone PR; that is, there appears to be an overlap between these windows of opportunities (adapted from Cepko et al, 1996). (C) Recent accurate single-cell tracing assays have unveiled complex lineage compositions in the zebrafish retina development. Three out of 60 clones from He et al (2012) are shown. Despite the observed high variability of clone compositions, there are some remarkable trends; for example, RGCs appear through asymmetric divisions, PRs through symmetric ones.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4358661&req=5

fig03: Vertebrate retinogenesis(A) During the development of the vertebrate retina, there is an initial phase where most of the divisions are symmetric proliferative leading to progenitor amplification. As development proceeds, proliferation slows down. When individual cells stop dividing, they differentiate and this leads to a link between the different cell types and the growth of the tissue (Livesey & Cepko, 2001). (B) Throughout retinal development, a reproducible sequence of overlapping temporal windows of specific fate adoption by differentiating cells is established. An early differentiating cell can become a retinal ganglion cell (RGC), a horizontal cell (HC), a rod photoreceptor (PR) or an amacrine cell (AC), whereas if it differentiates later, it can become a bipolar cell (BC), a Müller cell (MC) or a cone PR; that is, there appears to be an overlap between these windows of opportunities (adapted from Cepko et al, 1996). (C) Recent accurate single-cell tracing assays have unveiled complex lineage compositions in the zebrafish retina development. Three out of 60 clones from He et al (2012) are shown. Despite the observed high variability of clone compositions, there are some remarkable trends; for example, RGCs appear through asymmetric divisions, PRs through symmetric ones.
Mentions: The retina is a structure with millions of cells structurally diversified into seven main functionally distinct cell types that are allocated in specific proportions and positions to generate a functioning organ (Masland & Raviola, 2000; Masland, 2001). The structure emerges over time during embryogenesis and continues growth after birth from a collection of retinal progenitor cells (RPG, P) which display two essential behaviours (Fig3A, Livesey & Cepko, 2001; Centanin et al, 2011; Centanin & Wittbrodt, 2014). The first one relates to the patterns of divisions which early on amplify the P compartment (P→PP, Fig3A and B) while towards the end of development lean towards terminally differentiating symmetric divisions (P→DD) (Livesey & Cepko, 2001; Rapaport et al, 2004) and in between exhibit a mixture of symmetric and asymmetric (P→PD) divisions, with the corresponding proportions varying over time. The second behaviour is a reproducible sequence of fates adopted by differentiating cells; although to date there is no way to reliably predict the fate of a specific cell when it divides, it is known that, at a given time, a cell always chooses among a restricted number of fates and that the repertoire of available fates changes with time (Cepko et al, 1996; Livesey & Cepko, 2001, Fig3B and C). These observations led to a model suggesting that as development proceeds, an intrinsically defined competence to obtain particular fates changes and this is what determines the fate of a differentiating cell. According to this model, a pattern of differentiating (DD) divisions is superimposed upon this shifting window of competence resulting in a loose but reproducible sequence of fates (Livesey & Cepko, 2001).

Bottom Line: While some of the basic principles underlying these processes developing and maintaining these organs are known, much remains to be learnt from how cells encode the necessary information and use it to attain those complex but reproducible arrangements.We propose a framework, involving the existence of a transition state in which cells are more susceptible to signals that can affect their gene expression state and influence their cell fate decisions.This framework, which also applies to systems much more amenable to quantitative analysis like differentiating embryonic stem cells, links gene expression programmes with cell population dynamics.

View Article: PubMed Central - PubMed

Affiliation: Department of Genetics, University of Cambridge, Cambridge, UK.

No MeSH data available.


Related in: MedlinePlus