Cell lineages and the logic of proliferative control.

It is widely accepted that the growth and regeneration of tissues and organs is tightly controlled. Although experimental studies are beginning to reveal molecular mechanisms underlying such control, there is still very little known about the control strategies themselves. Here, we consider how secr...

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Main Authors: Arthur D Lander, Kimberly K Gokoffski, Frederic Y M Wan, Qing Nie, Anne L Calof
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2009-01-01
Series:PLoS Biology
Online Access:https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.1000015&type=printable
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author Arthur D Lander
Kimberly K Gokoffski
Frederic Y M Wan
Qing Nie
Anne L Calof
author_facet Arthur D Lander
Kimberly K Gokoffski
Frederic Y M Wan
Qing Nie
Anne L Calof
author_sort Arthur D Lander
collection DOAJ
description It is widely accepted that the growth and regeneration of tissues and organs is tightly controlled. Although experimental studies are beginning to reveal molecular mechanisms underlying such control, there is still very little known about the control strategies themselves. Here, we consider how secreted negative feedback factors ("chalones") may be used to control the output of multistage cell lineages, as exemplified by the actions of GDF11 and activin in a self-renewing neural tissue, the mammalian olfactory epithelium (OE). We begin by specifying performance objectives-what, precisely, is being controlled, and to what degree-and go on to calculate how well different types of feedback configurations, feedback sensitivities, and tissue architectures achieve control. Ultimately, we show that many features of the OE-the number of feedback loops, the cellular processes targeted by feedback, even the location of progenitor cells within the tissue-fit with expectations for the best possible control. In so doing, we also show that certain distinctions that are commonly drawn among cells and molecules-such as whether a cell is a stem cell or transit-amplifying cell, or whether a molecule is a growth inhibitor or stimulator-may be the consequences of control, and not a reflection of intrinsic differences in cellular or molecular character.
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spelling doaj-art-d00df3baf72e4d36af02a215ea20cd6a2025-08-20T02:00:48ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852009-01-0171e1510.1371/journal.pbio.1000015Cell lineages and the logic of proliferative control.Arthur D LanderKimberly K GokoffskiFrederic Y M WanQing NieAnne L CalofIt is widely accepted that the growth and regeneration of tissues and organs is tightly controlled. Although experimental studies are beginning to reveal molecular mechanisms underlying such control, there is still very little known about the control strategies themselves. Here, we consider how secreted negative feedback factors ("chalones") may be used to control the output of multistage cell lineages, as exemplified by the actions of GDF11 and activin in a self-renewing neural tissue, the mammalian olfactory epithelium (OE). We begin by specifying performance objectives-what, precisely, is being controlled, and to what degree-and go on to calculate how well different types of feedback configurations, feedback sensitivities, and tissue architectures achieve control. Ultimately, we show that many features of the OE-the number of feedback loops, the cellular processes targeted by feedback, even the location of progenitor cells within the tissue-fit with expectations for the best possible control. In so doing, we also show that certain distinctions that are commonly drawn among cells and molecules-such as whether a cell is a stem cell or transit-amplifying cell, or whether a molecule is a growth inhibitor or stimulator-may be the consequences of control, and not a reflection of intrinsic differences in cellular or molecular character.https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.1000015&type=printable
spellingShingle Arthur D Lander
Kimberly K Gokoffski
Frederic Y M Wan
Qing Nie
Anne L Calof
Cell lineages and the logic of proliferative control.
PLoS Biology
title Cell lineages and the logic of proliferative control.
title_full Cell lineages and the logic of proliferative control.
title_fullStr Cell lineages and the logic of proliferative control.
title_full_unstemmed Cell lineages and the logic of proliferative control.
title_short Cell lineages and the logic of proliferative control.
title_sort cell lineages and the logic of proliferative control
url https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.1000015&type=printable
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AT fredericymwan celllineagesandthelogicofproliferativecontrol
AT qingnie celllineagesandthelogicofproliferativecontrol
AT annelcalof celllineagesandthelogicofproliferativecontrol