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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

Cell proliferation and differentiation(A) The generation of neuroblast lineages in Drosophila is an example of a determinate process consisting of reproducible sequences of asymmetric cell divisions with changing fates. The succession of different fates upon each asymmetric cell division is controlled by a precise genetic programme on the progenitor, relying on the sequential expression of Hunchback (Hb), Kruppel (Kr), Pdm and Cas (adapted from Kohwi & Doe, 2013). (B) Asymmetric cell division is an invariant mechanism of generating differentiated progeny from stem cells where one daughter cell differentiates (D, yellow) and the other remains a stem cell (SC, teal). In homeostatic lineages, invariant asymmetry leads to homogeneous cell lineages. (C) Transit-amplifying cells are progenitors derived from stem cells that retain a proliferative capacity for a few division rounds before differentiating. SC: stem cell; D: differentiated cell; P, P1,…,PN: progenitors.
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fig01: Cell proliferation and differentiation(A) The generation of neuroblast lineages in Drosophila is an example of a determinate process consisting of reproducible sequences of asymmetric cell divisions with changing fates. The succession of different fates upon each asymmetric cell division is controlled by a precise genetic programme on the progenitor, relying on the sequential expression of Hunchback (Hb), Kruppel (Kr), Pdm and Cas (adapted from Kohwi & Doe, 2013). (B) Asymmetric cell division is an invariant mechanism of generating differentiated progeny from stem cells where one daughter cell differentiates (D, yellow) and the other remains a stem cell (SC, teal). In homeostatic lineages, invariant asymmetry leads to homogeneous cell lineages. (C) Transit-amplifying cells are progenitors derived from stem cells that retain a proliferative capacity for a few division rounds before differentiating. SC: stem cell; D: differentiated cell; P, P1,…,PN: progenitors.

Mentions: There are three ways to coordinate cell division and cell identity/fate. The first one is exemplified by eutelic organisms like C. elegans, in which every division is associated with the generation of two different cells and this process is iterated over time (Sulston, 1976; Sulston & Horvitz, 1977). The number of divisions is exquisitely regulated, such that each tissue is the result of a defined lineage built from a sequence of asymmetric cell divisions, that is, each gives rise to two different cells, and underpinned by a hardwired genetic programme (Gönczy, 2008; Knoblich, 2008). This strategy can also be found in other systems like the embryonic central neural system (CNS) of insects (Kohwi & Doe, 2013) where each neuroblast sequentially divides asymmetrically to self-renew and generates a differentiating ganglion mother cell, which can further divide and generate two differentiated neural cells (Fig1A). The whole process is associated with a gene expression programme running on each neuroblast, which involves the sequential expression of Hunchback, Kruppel, Pdm and Cas. These highly deterministic systems are usually associated with small and fast-developing embryos and have little regulative capacity: when a cell is lost, it is not replenished. At the other extreme, there are situations in which a group of cells make copies of themselves over a period of time and are given specific identities as the tissue grows by virtue of global cues, for example the imaginal discs of Drosophila (Wartlick et al, 2011). In these cases, there is no recognizable pattern relating cellular proliferation and fate assignment. In between these two extremes, there is a collection of dynamic behaviours exemplified by systems of growth driven by stem/progenitor cells, which divide asymmetrically to generate a cell that remains undifferentiated and thus sustains a naive state, and another cell that differentiates (Fig1B). In some instances, in tissues with wear and tear, these same cell populations maintain tissue homeostasis and have received increased attention over the last few years (Pellettieri & Sánchez Alvarado, 2007; Simons & Clevers, 2011).


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

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

Cell proliferation and differentiation(A) The generation of neuroblast lineages in Drosophila is an example of a determinate process consisting of reproducible sequences of asymmetric cell divisions with changing fates. The succession of different fates upon each asymmetric cell division is controlled by a precise genetic programme on the progenitor, relying on the sequential expression of Hunchback (Hb), Kruppel (Kr), Pdm and Cas (adapted from Kohwi & Doe, 2013). (B) Asymmetric cell division is an invariant mechanism of generating differentiated progeny from stem cells where one daughter cell differentiates (D, yellow) and the other remains a stem cell (SC, teal). In homeostatic lineages, invariant asymmetry leads to homogeneous cell lineages. (C) Transit-amplifying cells are progenitors derived from stem cells that retain a proliferative capacity for a few division rounds before differentiating. SC: stem cell; D: differentiated cell; P, P1,…,PN: progenitors.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

fig01: Cell proliferation and differentiation(A) The generation of neuroblast lineages in Drosophila is an example of a determinate process consisting of reproducible sequences of asymmetric cell divisions with changing fates. The succession of different fates upon each asymmetric cell division is controlled by a precise genetic programme on the progenitor, relying on the sequential expression of Hunchback (Hb), Kruppel (Kr), Pdm and Cas (adapted from Kohwi & Doe, 2013). (B) Asymmetric cell division is an invariant mechanism of generating differentiated progeny from stem cells where one daughter cell differentiates (D, yellow) and the other remains a stem cell (SC, teal). In homeostatic lineages, invariant asymmetry leads to homogeneous cell lineages. (C) Transit-amplifying cells are progenitors derived from stem cells that retain a proliferative capacity for a few division rounds before differentiating. SC: stem cell; D: differentiated cell; P, P1,…,PN: progenitors.
Mentions: There are three ways to coordinate cell division and cell identity/fate. The first one is exemplified by eutelic organisms like C. elegans, in which every division is associated with the generation of two different cells and this process is iterated over time (Sulston, 1976; Sulston & Horvitz, 1977). The number of divisions is exquisitely regulated, such that each tissue is the result of a defined lineage built from a sequence of asymmetric cell divisions, that is, each gives rise to two different cells, and underpinned by a hardwired genetic programme (Gönczy, 2008; Knoblich, 2008). This strategy can also be found in other systems like the embryonic central neural system (CNS) of insects (Kohwi & Doe, 2013) where each neuroblast sequentially divides asymmetrically to self-renew and generates a differentiating ganglion mother cell, which can further divide and generate two differentiated neural cells (Fig1A). The whole process is associated with a gene expression programme running on each neuroblast, which involves the sequential expression of Hunchback, Kruppel, Pdm and Cas. These highly deterministic systems are usually associated with small and fast-developing embryos and have little regulative capacity: when a cell is lost, it is not replenished. At the other extreme, there are situations in which a group of cells make copies of themselves over a period of time and are given specific identities as the tissue grows by virtue of global cues, for example the imaginal discs of Drosophila (Wartlick et al, 2011). In these cases, there is no recognizable pattern relating cellular proliferation and fate assignment. In between these two extremes, there is a collection of dynamic behaviours exemplified by systems of growth driven by stem/progenitor cells, which divide asymmetrically to generate a cell that remains undifferentiated and thus sustains a naive state, and another cell that differentiates (Fig1B). In some instances, in tissues with wear and tear, these same cell populations maintain tissue homeostasis and have received increased attention over the last few years (Pellettieri & Sánchez Alvarado, 2007; Simons & Clevers, 2011).

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