The Ascidia Ciona robusta Provides Novel Insights on the Evolution of the AP-1 Transcriptional Complex

The Activator Protein-1 transcription factor family (AP-1) transcriptional complex is historically defined as an early response group of transcription factors formed by dimeric complexes of the Jun, Fos, Atf, and Maf bZIP proteins that control cell proliferation and differentiation by regulating gen...

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Main Authors: Pina Marotta, Federica Salatiello, Luca Ambrosino, Federica Berruto, Maria Luisa Chiusano, Annamaria Locascio
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-08-01
Series:Frontiers in Cell and Developmental Biology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fcell.2021.709696/full
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author Pina Marotta
Pina Marotta
Federica Salatiello
Luca Ambrosino
Federica Berruto
Maria Luisa Chiusano
Maria Luisa Chiusano
Annamaria Locascio
author_facet Pina Marotta
Pina Marotta
Federica Salatiello
Luca Ambrosino
Federica Berruto
Maria Luisa Chiusano
Maria Luisa Chiusano
Annamaria Locascio
author_sort Pina Marotta
collection DOAJ
description The Activator Protein-1 transcription factor family (AP-1) transcriptional complex is historically defined as an early response group of transcription factors formed by dimeric complexes of the Jun, Fos, Atf, and Maf bZIP proteins that control cell proliferation and differentiation by regulating gene expression. It has been greatly investigated in many model organisms across metazoan evolution. Nevertheless, its complexity and variability of action made its multiple functions difficult to be defined. Here, we place the foundations for understanding the complexity of AP-1 transcriptional members in tunicates. We investigated the gene members of this family in the ascidian Ciona robusta and identified single copies of Jun, Fos, Atf3, Atf2/7, and Maf bZIP-related factors that could have a role in the formation of the AP-1 complex. We highlight that mesenchyme is a common cellular population where all these factors are expressed during embryonic development, and that, moreover, Fos shows a wider pattern of expression including also notochord and neural cells. By ectopic expression in transgenic embryos of Jun and Fos genes alone or in combination, we investigated the phenotypic alterations induced by these factors and highlighted a degree of functional conservation of the AP-1 complex between Ciona and vertebrates. The lack of gene redundancy and the first pieces of evidence of conserved functions in the control of cell movements and structural organization exerted by these factors open the way for using Ciona as a helpful model system to uncover the multiple potentialities of this highly complex family of bZIP transcription factors.
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spelling doaj.art-3ed3636ede6f4e4f8e91c4014a85510e2022-12-21T19:13:39ZengFrontiers Media S.A.Frontiers in Cell and Developmental Biology2296-634X2021-08-01910.3389/fcell.2021.709696709696The Ascidia Ciona robusta Provides Novel Insights on the Evolution of the AP-1 Transcriptional ComplexPina Marotta0Pina Marotta1Federica Salatiello2Luca Ambrosino3Federica Berruto4Maria Luisa Chiusano5Maria Luisa Chiusano6Annamaria Locascio7Stazione Zoologica Anton Dohrn, Department of Integrative Marine Ecology, Naples, ItalyStazione Zoologica Anton Dohrn, Department of Research Infrastructures for Marine Biological Resources, Naples, ItalyStazione Zoologica Anton Dohrn, Department of Biology and Evolution of Marine Organisms, Naples, ItalyStazione Zoologica Anton Dohrn, Department of Research Infrastructures for Marine Biological Resources, Naples, ItalyStazione Zoologica Anton Dohrn, Department of Biology and Evolution of Marine Organisms, Naples, ItalyStazione Zoologica Anton Dohrn, Department of Research Infrastructures for Marine Biological Resources, Naples, ItalyDepartment of Agriculture, Università degli Studi di Napoli Federico II, Portici, ItalyStazione Zoologica Anton Dohrn, Department of Biology and Evolution of Marine Organisms, Naples, ItalyThe Activator Protein-1 transcription factor family (AP-1) transcriptional complex is historically defined as an early response group of transcription factors formed by dimeric complexes of the Jun, Fos, Atf, and Maf bZIP proteins that control cell proliferation and differentiation by regulating gene expression. It has been greatly investigated in many model organisms across metazoan evolution. Nevertheless, its complexity and variability of action made its multiple functions difficult to be defined. Here, we place the foundations for understanding the complexity of AP-1 transcriptional members in tunicates. We investigated the gene members of this family in the ascidian Ciona robusta and identified single copies of Jun, Fos, Atf3, Atf2/7, and Maf bZIP-related factors that could have a role in the formation of the AP-1 complex. We highlight that mesenchyme is a common cellular population where all these factors are expressed during embryonic development, and that, moreover, Fos shows a wider pattern of expression including also notochord and neural cells. By ectopic expression in transgenic embryos of Jun and Fos genes alone or in combination, we investigated the phenotypic alterations induced by these factors and highlighted a degree of functional conservation of the AP-1 complex between Ciona and vertebrates. The lack of gene redundancy and the first pieces of evidence of conserved functions in the control of cell movements and structural organization exerted by these factors open the way for using Ciona as a helpful model system to uncover the multiple potentialities of this highly complex family of bZIP transcription factors.https://www.frontiersin.org/articles/10.3389/fcell.2021.709696/fullJunFosbZIP proteinmesenchymetranscription factornotochord
spellingShingle Pina Marotta
Pina Marotta
Federica Salatiello
Luca Ambrosino
Federica Berruto
Maria Luisa Chiusano
Maria Luisa Chiusano
Annamaria Locascio
The Ascidia Ciona robusta Provides Novel Insights on the Evolution of the AP-1 Transcriptional Complex
Frontiers in Cell and Developmental Biology
Jun
Fos
bZIP protein
mesenchyme
transcription factor
notochord
title The Ascidia Ciona robusta Provides Novel Insights on the Evolution of the AP-1 Transcriptional Complex
title_full The Ascidia Ciona robusta Provides Novel Insights on the Evolution of the AP-1 Transcriptional Complex
title_fullStr The Ascidia Ciona robusta Provides Novel Insights on the Evolution of the AP-1 Transcriptional Complex
title_full_unstemmed The Ascidia Ciona robusta Provides Novel Insights on the Evolution of the AP-1 Transcriptional Complex
title_short The Ascidia Ciona robusta Provides Novel Insights on the Evolution of the AP-1 Transcriptional Complex
title_sort ascidia ciona robusta provides novel insights on the evolution of the ap 1 transcriptional complex
topic Jun
Fos
bZIP protein
mesenchyme
transcription factor
notochord
url https://www.frontiersin.org/articles/10.3389/fcell.2021.709696/full
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