The roles of jim lovell and uninflatable in different endopolyploid larval tissues of Drosophila melanogaster.

The larvae of Drosophila melanogaster grow rapidly through use of a highly truncated cell cycle in which mitosis is entirely eliminated. The Drosophila homolog of the protooncogene transcription factor Myc plays a major role in promoting this endopolyploid (EP) growth. We have previously determined...

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Main Authors: Fanli Zhou, Stephanie R Green, Michael Tsay, Safina Hsu, Rami Dibbs, Kathleen M Beckingham
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2020-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0237662
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spelling doaj-c7f74e73e2a84ad084d2966886c843272021-03-03T22:00:08ZengPublic Library of Science (PLoS)PLoS ONE1932-62032020-01-01158e023766210.1371/journal.pone.0237662The roles of jim lovell and uninflatable in different endopolyploid larval tissues of Drosophila melanogaster.Fanli ZhouStephanie R GreenMichael TsaySafina HsuRami DibbsKathleen M BeckinghamThe larvae of Drosophila melanogaster grow rapidly through use of a highly truncated cell cycle in which mitosis is entirely eliminated. The Drosophila homolog of the protooncogene transcription factor Myc plays a major role in promoting this endopolyploid (EP) growth. We have previously determined that the gene jim lovell (lov), which encodes a member of the BTB/POZ (Bric-a-brac, Tramtrack, Broad/Pox virus zinc finger) domain family of transcription factors, is also required for EP growth in one larval tissue, the trachea. Here we show that lov promotes EP growth in three further tissues indicating a fundamental role in this process. However, epistasis experiments revealed heterogeneity in lov's action in these tissues. Whereas in the tracheae and salivary glands lov acts downstream of Myc, in the fat body, reduced expression of lov does not impede the action of Myc, indicating an upstream action for the gene. We show here that lov's regulation of the gene uninflatable (uif) in the tracheae is a component of this difference. uif is required for tracheal EP growth downstream of Myc and lov but has no equivalent role in the fat body. Although Uif is a transmembrane component of the plasma membrane in the tracheae, its action downstream of Myc suggests an intracellular role for the protein in the tracheae. In addition to regulating uif expression in some tissues we also show that lov locates to the nucleolus, indicating it can function in both polymerase I and polymerase II transcriptional events. Our major finding is that tissue-specific mechanisms can interact with universal growth promotion by Myc to generate the individual endopolyploid organs of the larvae.https://doi.org/10.1371/journal.pone.0237662
collection DOAJ
language English
format Article
sources DOAJ
author Fanli Zhou
Stephanie R Green
Michael Tsay
Safina Hsu
Rami Dibbs
Kathleen M Beckingham
spellingShingle Fanli Zhou
Stephanie R Green
Michael Tsay
Safina Hsu
Rami Dibbs
Kathleen M Beckingham
The roles of jim lovell and uninflatable in different endopolyploid larval tissues of Drosophila melanogaster.
PLoS ONE
author_facet Fanli Zhou
Stephanie R Green
Michael Tsay
Safina Hsu
Rami Dibbs
Kathleen M Beckingham
author_sort Fanli Zhou
title The roles of jim lovell and uninflatable in different endopolyploid larval tissues of Drosophila melanogaster.
title_short The roles of jim lovell and uninflatable in different endopolyploid larval tissues of Drosophila melanogaster.
title_full The roles of jim lovell and uninflatable in different endopolyploid larval tissues of Drosophila melanogaster.
title_fullStr The roles of jim lovell and uninflatable in different endopolyploid larval tissues of Drosophila melanogaster.
title_full_unstemmed The roles of jim lovell and uninflatable in different endopolyploid larval tissues of Drosophila melanogaster.
title_sort roles of jim lovell and uninflatable in different endopolyploid larval tissues of drosophila melanogaster.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2020-01-01
description The larvae of Drosophila melanogaster grow rapidly through use of a highly truncated cell cycle in which mitosis is entirely eliminated. The Drosophila homolog of the protooncogene transcription factor Myc plays a major role in promoting this endopolyploid (EP) growth. We have previously determined that the gene jim lovell (lov), which encodes a member of the BTB/POZ (Bric-a-brac, Tramtrack, Broad/Pox virus zinc finger) domain family of transcription factors, is also required for EP growth in one larval tissue, the trachea. Here we show that lov promotes EP growth in three further tissues indicating a fundamental role in this process. However, epistasis experiments revealed heterogeneity in lov's action in these tissues. Whereas in the tracheae and salivary glands lov acts downstream of Myc, in the fat body, reduced expression of lov does not impede the action of Myc, indicating an upstream action for the gene. We show here that lov's regulation of the gene uninflatable (uif) in the tracheae is a component of this difference. uif is required for tracheal EP growth downstream of Myc and lov but has no equivalent role in the fat body. Although Uif is a transmembrane component of the plasma membrane in the tracheae, its action downstream of Myc suggests an intracellular role for the protein in the tracheae. In addition to regulating uif expression in some tissues we also show that lov locates to the nucleolus, indicating it can function in both polymerase I and polymerase II transcriptional events. Our major finding is that tissue-specific mechanisms can interact with universal growth promotion by Myc to generate the individual endopolyploid organs of the larvae.
url https://doi.org/10.1371/journal.pone.0237662
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