Fat cells reactivate quiescent neuroblasts via TOR and glial insulin relays in Drosophila
Nerve progenitors hungry for action The availability of nutrients prompts quiescent neural stem cells (neuroblasts) in Drosophila larvae to begin to divide. A study of the mechanism linking diet to stem-cell behaviour has identified a relay mechanism regulating this nutritional checkpoint. Specific...
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| Published in | Nature (London) Vol. 471; no. 7339; pp. 508 - 512 |
|---|---|
| Main Authors | , , |
| Format | Journal Article |
| Language | English |
| Published |
London
Nature Publishing Group UK
24.03.2011
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Nerve progenitors hungry for action
The availability of nutrients prompts quiescent neural stem cells (neuroblasts) in
Drosophila
larvae to begin to divide. A study of the mechanism linking diet to stem-cell behaviour has identified a relay mechanism regulating this nutritional checkpoint. Specific insulin-like peptides produced within the brain by glia — non-neuronal cells with various physical and biochemical support roles — form a bridge from the amino-acid/TOR-dependent signal derived from the fat body to PI3K/TOR signalling in neuroblasts to induce exit from quiescence.
Little is known about how nutritional cues are detected by quiescent neural stem cells (neuroblasts in
Drosophila melanogaster
) and how these signals are relayed to reactivate their cell cycle to exit quiescence. This study uses an integrative physiology approach to identify the relay mechanism regulating this nutritional checkpoint in neural progenitors. It is found that specific insulin-like peptides produced within the brain by glia bridge the amino-acid/TOR-dependent signal derived from the fat body with PI3K/TOR signalling in neuroblasts to induce exit from quiescent.
Many stem, progenitor and cancer cells undergo periods of mitotic quiescence from which they can be reactivated
1
,
2
,
3
,
4
,
5
. The signals triggering entry into and exit from this reversible dormant state are not well understood. In the developing
Drosophila
central nervous system, multipotent self-renewing progenitors called neuroblasts
6
,
7
,
8
,
9
undergo quiescence in a stereotypical spatiotemporal pattern
10
. Entry into quiescence is regulated by Hox proteins and an internal neuroblast timer
11
,
12
,
13
. Exit from quiescence (reactivation) is subject to a nutritional checkpoint requiring dietary amino acids
14
. Organ co-cultures also implicate an unidentified signal from an adipose/hepatic-like tissue called the fat body
14
. Here we provide
in vivo
evidence that Slimfast amino-acid sensing and Target of rapamycin (TOR) signalling
15
activate a fat-body-derived signal (FDS) required for neuroblast reactivation. Downstream of this signal, Insulin-like receptor signalling and the Phosphatidylinositol 3-kinase (PI3K)/TOR network are required in neuroblasts for exit from quiescence. We demonstrate that nutritionally regulated glial cells provide the source of Insulin-like peptides (ILPs) relevant for timely neuroblast reactivation but not for overall larval growth. Conversely, ILPs secreted into the haemolymph by median neurosecretory cells systemically control organismal size
16
,
17
,
18
but do not reactivate neuroblasts.
Drosophila
thus contains two segregated ILP pools, one regulating proliferation within the central nervous system and the other controlling tissue growth systemically. Our findings support a model in which amino acids trigger the cell cycle re-entry of neural progenitors via a fat-body–glia–neuroblasts relay. This mechanism indicates that dietary nutrients and remote organs, as well as local niches, are key regulators of transitions in stem-cell behaviour. |
|---|---|
| AbstractList | Many stem, progenitor and cancer cells undergo periods of mitotic quiescence from which they can be reactivated (1-5). The signals triggering entry into and exit from this reversible dormant state are not well understood. In the developing Drosophila central nervous system, multipotent self-renewing progenitors called neuroblasts (6-9) undergo quiescence in a stereotypical spatiotemporal pattern (10). Entry into quiescence is regulated by Hox proteins and an internal neuroblast timer (11-13). Exit from quiescence (reactivation) is subject to a nutritional checkpoint requiring dietary amino acids (14). Organ co-cultures also implicate an unidentified signal from an adipose/ hepatic-like tissue called the fat body (14).Here weprovide in vivo evidence that Slimfast amino-acid sensing and Target of rapamycin (TOR) signalling (15) activate a fat-body-derived signal (FDS) required for neuroblast reactivation. Downstream of this signal, Insulin-like receptor signalling and the Phosphatidylinositol 3-kinase (PI3K)/TOR network are required in neuroblasts for exit from quiescence. We demonstrate that nutritionally regulated glial cells provide the source of Insulin-like peptides (ILPs) relevant for timely neuroblast reactivation but not for overall larval growth. Conversely, ILPs secreted into the haemolymph by median neurosecretory cells systemically control organismal size (16-18) but do not reactivate neuroblasts. Drosophila thus contains two segregated ILP pools, one regulating proliferation within the central nervous system and the other controlling tissue growth systemically. Our findings support a model in which amino acids trigger the cell cycle re-entry of neural progenitors via a fat-body-glia-neuroblasts relay. This mechanism indicates that dietary nutrients and remote organs, as well as local niches, are key regulators of transitions in stem-cell behaviour. Nerve progenitors hungry for action The availability of nutrients prompts quiescent neural stem cells (neuroblasts) in Drosophila larvae to begin to divide. A study of the mechanism linking diet to stem-cell behaviour has identified a relay mechanism regulating this nutritional checkpoint. Specific insulin-like peptides produced within the brain by glia — non-neuronal cells with various physical and biochemical support roles — form a bridge from the amino-acid/TOR-dependent signal derived from the fat body to PI3K/TOR signalling in neuroblasts to induce exit from quiescence. Little is known about how nutritional cues are detected by quiescent neural stem cells (neuroblasts in Drosophila melanogaster ) and how these signals are relayed to reactivate their cell cycle to exit quiescence. This study uses an integrative physiology approach to identify the relay mechanism regulating this nutritional checkpoint in neural progenitors. It is found that specific insulin-like peptides produced within the brain by glia bridge the amino-acid/TOR-dependent signal derived from the fat body with PI3K/TOR signalling in neuroblasts to induce exit from quiescent. Many stem, progenitor and cancer cells undergo periods of mitotic quiescence from which they can be reactivated 1 , 2 , 3 , 4 , 5 . The signals triggering entry into and exit from this reversible dormant state are not well understood. In the developing Drosophila central nervous system, multipotent self-renewing progenitors called neuroblasts 6 , 7 , 8 , 9 undergo quiescence in a stereotypical spatiotemporal pattern 10 . Entry into quiescence is regulated by Hox proteins and an internal neuroblast timer 11 , 12 , 13 . Exit from quiescence (reactivation) is subject to a nutritional checkpoint requiring dietary amino acids 14 . Organ co-cultures also implicate an unidentified signal from an adipose/hepatic-like tissue called the fat body 14 . Here we provide in vivo evidence that Slimfast amino-acid sensing and Target of rapamycin (TOR) signalling 15 activate a fat-body-derived signal (FDS) required for neuroblast reactivation. Downstream of this signal, Insulin-like receptor signalling and the Phosphatidylinositol 3-kinase (PI3K)/TOR network are required in neuroblasts for exit from quiescence. We demonstrate that nutritionally regulated glial cells provide the source of Insulin-like peptides (ILPs) relevant for timely neuroblast reactivation but not for overall larval growth. Conversely, ILPs secreted into the haemolymph by median neurosecretory cells systemically control organismal size 16 , 17 , 18 but do not reactivate neuroblasts. Drosophila thus contains two segregated ILP pools, one regulating proliferation within the central nervous system and the other controlling tissue growth systemically. Our findings support a model in which amino acids trigger the cell cycle re-entry of neural progenitors via a fat-body–glia–neuroblasts relay. This mechanism indicates that dietary nutrients and remote organs, as well as local niches, are key regulators of transitions in stem-cell behaviour. Many stem, progenitor and cancer cells undergo periods of mitotic quiescence from which they can be reactivated. The signals triggering entry into and exit from this reversible dormant state are not well understood. In the developing Drosophila central nervous system, multipotent self-renewing progenitors called neuroblasts undergo quiescence in a stereotypical spatiotemporal pattern. Entry into quiescence is regulated by Hox proteins and an internal neuroblast timer. Exit from quiescence (reactivation) is subject to a nutritional checkpoint requiring dietary amino acids. Organ co-cultures also implicate an unidentified signal from an adipose/hepatic-like tissue called the fat body. Here we provide in vivo evidence that Slimfast amino-acid sensing and Target of rapamycin (TOR) signalling activate a fat-body-derived signal (FDS) required for neuroblast reactivation. Downstream of this signal, Insulin-like receptor signalling and the Phosphatidylinositol 3-kinase (PI3K)/TOR network are required in neuroblasts for exit from quiescence. We demonstrate that nutritionally regulated glial cells provide the source of Insulin-like peptides (ILPs) relevant for timely neuroblast reactivation but not for overall larval growth. Conversely, ILPs secreted into the haemolymph by median neurosecretory cells systemically control organismal size but do not reactivate neuroblasts. Drosophila thus contains two segregated ILP pools, one regulating proliferation within the central nervous system and the other controlling tissue growth systemically. Our findings support a model in which amino acids trigger the cell cycle re-entry of neural progenitors via a fat-body-glia-neuroblasts relay. This mechanism indicates that dietary nutrients and remote organs, as well as local niches, are key regulators of transitions in stem-cell behaviour. Many stem, progenitor and cancer cells undergo periods of mitotic quiescence from which they can be reactivated. The signals triggering entry into and exit from this reversible dormant state are not well understood. In the developing Drosophila central nervous system, multipotent self-renewing progenitors called neuroblasts undergo quiescence in a stereotypical spatiotemporal pattern. Entry into quiescence is regulated by Hox proteins and an internal neuroblast timer. Exit from quiescence (reactivation) is subject to a nutritional checkpoint requiring dietary amino acids. Organ co-cultures also implicate an unidentified signal from an adipose/hepatic-like tissue called the fat body. Here we provide in vivo evidence that Slimfast amino-acid sensing and Target of rapamycin (TOR) signalling activate a fat-body-derived signal (FDS) required for neuroblast reactivation. Downstream of this signal, Insulin-like receptor signalling and the Phosphatidylinositol 3-kinase (PI3K)/TOR network are required in neuroblasts for exit from quiescence. We demonstrate that nutritionally regulated glial cells provide the source of Insulin-like peptides (ILPs) relevant for timely neuroblast reactivation but not for overall larval growth. Conversely, ILPs secreted into the haemolymph by median neurosecretory cells systemically control organismal size but do not reactivate neuroblasts. Drosophila thus contains two segregated ILP pools, one regulating proliferation within the central nervous system and the other controlling tissue growth systemically. Our findings support a model in which amino acids trigger the cell cycle re-entry of neural progenitors via a fat-body-glia-neuroblasts relay. This mechanism indicates that dietary nutrients and remote organs, as well as local niches, are key regulators of transitions in stem-cell behaviour.Many stem, progenitor and cancer cells undergo periods of mitotic quiescence from which they can be reactivated. The signals triggering entry into and exit from this reversible dormant state are not well understood. In the developing Drosophila central nervous system, multipotent self-renewing progenitors called neuroblasts undergo quiescence in a stereotypical spatiotemporal pattern. Entry into quiescence is regulated by Hox proteins and an internal neuroblast timer. Exit from quiescence (reactivation) is subject to a nutritional checkpoint requiring dietary amino acids. Organ co-cultures also implicate an unidentified signal from an adipose/hepatic-like tissue called the fat body. Here we provide in vivo evidence that Slimfast amino-acid sensing and Target of rapamycin (TOR) signalling activate a fat-body-derived signal (FDS) required for neuroblast reactivation. Downstream of this signal, Insulin-like receptor signalling and the Phosphatidylinositol 3-kinase (PI3K)/TOR network are required in neuroblasts for exit from quiescence. We demonstrate that nutritionally regulated glial cells provide the source of Insulin-like peptides (ILPs) relevant for timely neuroblast reactivation but not for overall larval growth. Conversely, ILPs secreted into the haemolymph by median neurosecretory cells systemically control organismal size but do not reactivate neuroblasts. Drosophila thus contains two segregated ILP pools, one regulating proliferation within the central nervous system and the other controlling tissue growth systemically. Our findings support a model in which amino acids trigger the cell cycle re-entry of neural progenitors via a fat-body-glia-neuroblasts relay. This mechanism indicates that dietary nutrients and remote organs, as well as local niches, are key regulators of transitions in stem-cell behaviour. Many stem, progenitor and cancer cells undergo periods of mitotic quiescence from which they can be reactivated. The signals triggering entry into and exit from this reversible dormant state are not well understood. In the developing Drosophila central nervous system, multipotent self-renewing progenitors called neuroblasts undergo quiescence in a stereotypical spatiotemporal pattern. Entry into quiescence is regulated by Hox proteins and an internal neuroblast timer. Exit from quiescence (reactivation) is subject to a nutritional checkpoint requiring dietary amino acids. Organ co-cultures also implicate an unidentified signal from an adipose/hepatic-like tissue called the fat body. Here we provide in vivo evidence that Slimfast amino-acid sensing and Target of rapamycin (TOR) signalling activate a fat-body-derived signal (FDS) required for neuroblast reactivation. Downstream of this signal, Insulin-like receptor signalling and the Phosphatidylinositol 3-kinase (PI3K)/TOR network are required in neuroblasts for exit from quiescence. We demonstrate that nutritionally regulated glial cells provide the source of Insulin-like peptides (ILPs) relevant for timely neuroblast reactivation but not for overall larval growth. Conversely, ILPs secreted into the haemolymph by median neurosecretory cells systemically control organismal size but do not reactivate neuroblasts. Drosophila thus contains two segregated ILP pools, one regulating proliferation within the central nervous system and the other controlling tissue growth systemically. Our findings support a model in which amino acids trigger the cell cycle re-entry of neural progenitors via a fat-body-glia-neuroblasts relay. This mechanism indicates that dietary nutrients and remote organs, as well as local niches, are key regulators of transitions in stem-cell behaviour. [PUBLICATION ABSTRACT] Many stem, progenitor and cancer cells undergo periods of mitotic quiescence from which they can be reactivated 1 - 5 . The signals triggering entry into and exit from this reversible dormant state are not well understood. In the developing Drosophila central nervous system (CNS), multipotent self-renewing progenitors called neuroblasts 6 - 9 undergo quiescence in a stereotypical spatiotemporal pattern 10 . Entry into quiescence is regulated by Hox proteins and an internal neuroblast timer 11 - 13 . Exit from quiescence (reactivation) is subject to a nutritional checkpoint requiring dietary amino acids 14 . Organ co-cultures also implicate an unidentified signal from an adipose/hepatic-like tissue called fat body 14 . Here, we provide in vivo evidence that Slimfast amino-acid sensing and Target-of-Rapamycin (TOR) signalling 15 activate a fat-body derived signal (FDS) required for neuroblast reactivation. Downstream of the FDS, Insulin-like receptor (InR) signalling and the Phosphatidylinositol 3-Kinase (PI3K)/TOR network are required in neuroblasts for exit from quiescence. We demonstrate that nutritionally regulated glial cells provide the source of Insulin-like Peptides (Ilps) relevant for timely neuroblast reactivation but not for overall larval growth. Conversely, Ilps secreted into the hemolymph by median neurosecretory cells (mNSCs) systemically control organismal size 16 - 18 but do not reactivate neuroblasts. Drosophila thus contains two segregated Ilp pools, one regulating proliferation within the CNS and the other controlling tissue growth systemically. Together, our findings support a model in which amino acids trigger the cell cycle re-entry of neural progenitors via a fat body→glia→neuroblasts relay. This mechanism highlights that dietary nutrients and remote organs, as well as local niches, are key regulators of transitions in stem-cell behaviour. |
| Audience | Academic |
| Author | Gould, Alex P. Yee, Lih Ling Sousa-Nunes, Rita |
| Author_xml | – sequence: 1 givenname: Rita surname: Sousa-Nunes fullname: Sousa-Nunes, Rita organization: Division of Developmental Neurobiology, Medical Research Council National Institute for Medical Research, The Ridgeway, Mill Hill – sequence: 2 givenname: Lih Ling surname: Yee fullname: Yee, Lih Ling organization: Division of Developmental Neurobiology, Medical Research Council National Institute for Medical Research, The Ridgeway, Mill Hill – sequence: 3 givenname: Alex P. surname: Gould fullname: Gould, Alex P. email: agould@nimr.mrc.ac.uk organization: Division of Developmental Neurobiology, Medical Research Council National Institute for Medical Research, The Ridgeway, Mill Hill |
| BackLink | http://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=23947205$$DView record in Pascal Francis https://www.ncbi.nlm.nih.gov/pubmed/21346761$$D View this record in MEDLINE/PubMed |
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| Snippet | Nerve progenitors hungry for action
The availability of nutrients prompts quiescent neural stem cells (neuroblasts) in
Drosophila
larvae to begin to divide. A... Many stem, progenitor and cancer cells undergo periods of mitotic quiescence from which they can be reactivated. The signals triggering entry into and exit... Many stem, progenitor and cancer cells undergo periods of mitotic quiescence from which they can be reactivated (1-5). The signals triggering entry into and... Many stem, progenitor and cancer cells undergo periods of mitotic quiescence from which they can be reactivated 1 - 5 . The signals triggering entry into and... |
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| SubjectTerms | 631/136/532/2182 631/378/2571 631/80/86 Adipocytes - drug effects Adipocytes - metabolism Amino acids Amino Acids - pharmacology Animals Biological and medical sciences Cells Cellular signal transduction Central nervous system Central Nervous System - cytology Central Nervous System - drug effects Central Nervous System - metabolism Diet Drosophila Drosophila melanogaster - cytology Drosophila melanogaster - drug effects Drosophila melanogaster - growth & development Drosophila melanogaster - metabolism Drosophila Proteins - metabolism Fat Body - cytology Fat Body - drug effects Fat Body - metabolism Fundamental and applied biological sciences. Psychology Gene expression Genetic aspects Humanities and Social Sciences Insects Insulin - metabolism Kinases Larva - cytology Larva - drug effects Larva - metabolism Larval development letter multidisciplinary Neural Stem Cells - cytology Neural Stem Cells - drug effects Neural Stem Cells - metabolism Neuroglia - drug effects Neuroglia - metabolism Peptides Phosphatidylinositol 3-Kinases - metabolism Physiological aspects Sample variance Science Science (multidisciplinary) Signal Transduction - drug effects TOR Serine-Threonine Kinases - metabolism Vertebrates: nervous system and sense organs |
| Title | Fat cells reactivate quiescent neuroblasts via TOR and glial insulin relays in Drosophila |
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