Ecdysone promotes growth of imaginal discs through the regulation of Thor in D. melanogaster

Animals have a determined species-specific body size that results from the combined action of hormones and signaling pathways regulating growth rate and duration. In Drosophila, the steroid hormone ecdysone controls developmental transitions, thereby regulating the duration of the growth period. Here we show that ecdysone promotes the growth of imaginal discs in mid-third instar larvae, since imaginal discs from larvae with reduced or no ecdysone synthesis are smaller than wild type due to smaller and fewer cells. We show that insulin-like peptides are produced and secreted normally in larvae with reduced ecdysone synthesis, and upstream components of insulin/insulin-like signaling are activated in their discs. Instead, ecdysone appears to regulate the growth of imaginal discs via Thor/4E-BP, a negative growth regulator downstream of the insulin/insulin-like growth factor/Tor pathways. Discs from larvae with reduced ecdysone synthesis have elevated levels of Thor, while mutations in Thor partially rescue their growth. The regulation of organ growth by ecdysone is evolutionarily conserved in hemimetabolous insects, as shown by our results obtained using Blattella germanica. In summary, our data provide new insights into the relationship between components of the insulin/insulin-like/Tor and ecdysone pathways in the control of organ growth.

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Main Authors: Herboso, Leire, Oliveira, Marisa, Talamillo, Ana, Pérez, Coralia, González, Monika, Martín Casacuberta, David A., Sutherland, James D., Shingleton, Alexander W., Mirth, Christen, Barrio, Rosa
Other Authors: Ministerio de Ciencia e Innovación (España)
Format: artículo biblioteca
Language:English
Published: Nature Publishing Group 2015-07-22
Online Access:http://hdl.handle.net/10261/151366
http://dx.doi.org/10.13039/501100004837
http://dx.doi.org/10.13039/501100005635
http://dx.doi.org/10.13039/501100001871
http://dx.doi.org/10.13039/100000001
http://dx.doi.org/10.13039/501100003086
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spelling dig-ibe-es-10261-1513662021-12-28T15:52:23Z Ecdysone promotes growth of imaginal discs through the regulation of Thor in D. melanogaster Herboso, Leire Oliveira, Marisa Talamillo, Ana Pérez, Coralia González, Monika Martín Casacuberta, David A. Sutherland, James D. Shingleton, Alexander W. Mirth, Christen Barrio, Rosa Ministerio de Ciencia e Innovación (España) Eusko Jaurlaritza Fundação Calouste Gulbenkian Fundação para a Ciência e a Tecnologia (Portugal) National Science Foundation (US) Animals have a determined species-specific body size that results from the combined action of hormones and signaling pathways regulating growth rate and duration. In Drosophila, the steroid hormone ecdysone controls developmental transitions, thereby regulating the duration of the growth period. Here we show that ecdysone promotes the growth of imaginal discs in mid-third instar larvae, since imaginal discs from larvae with reduced or no ecdysone synthesis are smaller than wild type due to smaller and fewer cells. We show that insulin-like peptides are produced and secreted normally in larvae with reduced ecdysone synthesis, and upstream components of insulin/insulin-like signaling are activated in their discs. Instead, ecdysone appears to regulate the growth of imaginal discs via Thor/4E-BP, a negative growth regulator downstream of the insulin/insulin-like growth factor/Tor pathways. Discs from larvae with reduced ecdysone synthesis have elevated levels of Thor, while mutations in Thor partially rescue their growth. The regulation of organ growth by ecdysone is evolutionarily conserved in hemimetabolous insects, as shown by our results obtained using Blattella germanica. In summary, our data provide new insights into the relationship between components of the insulin/insulin-like/Tor and ecdysone pathways in the control of organ growth. RB, DM and LH thank the Spanish Ministry of Science and Consolider program (BFU-2008-01884, BFU2011-25986, CSD2007-008-25120, BFU2009-10571 and BES-2009-016077). RB thanks the Departments of Education and Industry of the Basque Government (PI2012/42), and the Bizkaia County. CKM and MMO thank the Instituto Gulbenkian de Ciência/Fundação Calouste Gulbenkian and the Fundação Para a Ciência e a Tecnologia (SFRH/BD/51181/2010). AWS thanks the National Science Foundation (IOS-0919855 and IOS-1406547). Peer reviewed 2017-06-13T10:55:37Z 2017-06-13T10:55:37Z 2015-07-22 artículo http://purl.org/coar/resource_type/c_6501 Scientific Reports 5: 12383 (2015) 2045-2322 http://hdl.handle.net/10261/151366 10.1038/srep12383 2045-2322 http://dx.doi.org/10.13039/501100004837 http://dx.doi.org/10.13039/501100005635 http://dx.doi.org/10.13039/501100001871 http://dx.doi.org/10.13039/100000001 http://dx.doi.org/10.13039/501100003086 26198204 en Publisher's version http://dx.doi.org/10.1038/srep12383 Sí open Nature Publishing Group
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language English
description Animals have a determined species-specific body size that results from the combined action of hormones and signaling pathways regulating growth rate and duration. In Drosophila, the steroid hormone ecdysone controls developmental transitions, thereby regulating the duration of the growth period. Here we show that ecdysone promotes the growth of imaginal discs in mid-third instar larvae, since imaginal discs from larvae with reduced or no ecdysone synthesis are smaller than wild type due to smaller and fewer cells. We show that insulin-like peptides are produced and secreted normally in larvae with reduced ecdysone synthesis, and upstream components of insulin/insulin-like signaling are activated in their discs. Instead, ecdysone appears to regulate the growth of imaginal discs via Thor/4E-BP, a negative growth regulator downstream of the insulin/insulin-like growth factor/Tor pathways. Discs from larvae with reduced ecdysone synthesis have elevated levels of Thor, while mutations in Thor partially rescue their growth. The regulation of organ growth by ecdysone is evolutionarily conserved in hemimetabolous insects, as shown by our results obtained using Blattella germanica. In summary, our data provide new insights into the relationship between components of the insulin/insulin-like/Tor and ecdysone pathways in the control of organ growth.
author2 Ministerio de Ciencia e Innovación (España)
author_facet Ministerio de Ciencia e Innovación (España)
Herboso, Leire
Oliveira, Marisa
Talamillo, Ana
Pérez, Coralia
González, Monika
Martín Casacuberta, David A.
Sutherland, James D.
Shingleton, Alexander W.
Mirth, Christen
Barrio, Rosa
format artículo
author Herboso, Leire
Oliveira, Marisa
Talamillo, Ana
Pérez, Coralia
González, Monika
Martín Casacuberta, David A.
Sutherland, James D.
Shingleton, Alexander W.
Mirth, Christen
Barrio, Rosa
spellingShingle Herboso, Leire
Oliveira, Marisa
Talamillo, Ana
Pérez, Coralia
González, Monika
Martín Casacuberta, David A.
Sutherland, James D.
Shingleton, Alexander W.
Mirth, Christen
Barrio, Rosa
Ecdysone promotes growth of imaginal discs through the regulation of Thor in D. melanogaster
author_sort Herboso, Leire
title Ecdysone promotes growth of imaginal discs through the regulation of Thor in D. melanogaster
title_short Ecdysone promotes growth of imaginal discs through the regulation of Thor in D. melanogaster
title_full Ecdysone promotes growth of imaginal discs through the regulation of Thor in D. melanogaster
title_fullStr Ecdysone promotes growth of imaginal discs through the regulation of Thor in D. melanogaster
title_full_unstemmed Ecdysone promotes growth of imaginal discs through the regulation of Thor in D. melanogaster
title_sort ecdysone promotes growth of imaginal discs through the regulation of thor in d. melanogaster
publisher Nature Publishing Group
publishDate 2015-07-22
url http://hdl.handle.net/10261/151366
http://dx.doi.org/10.13039/501100004837
http://dx.doi.org/10.13039/501100005635
http://dx.doi.org/10.13039/501100001871
http://dx.doi.org/10.13039/100000001
http://dx.doi.org/10.13039/501100003086
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