NF-κB signaling driven by oncogenic Ras contributes to tumorigenesis in a Drosophila carcinoma model.

Cancer-driving mutations synergize with inflammatory stress signaling pathways during carcinogenesis. Drosophila melanogaster tumor models are increasingly recognized as models to inform conserved molecular mechanisms of tumorigenesis with both local and systemic effects of cancer. Although initial...

Full description

Saved in:
Bibliographic Details
Main Authors: Caroline Dillard, José Teles-Reis, Ashish Jain, Marina Gonçalves Antunes, Paula Ruiz-Duran, Yanyan Qi, Roland Le Borgne, Heinrich Jasper, Tor Erik Rusten
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2025-04-01
Series:PLoS Biology
Online Access:https://doi.org/10.1371/journal.pbio.3002663
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849720848423845888
author Caroline Dillard
José Teles-Reis
Ashish Jain
Marina Gonçalves Antunes
Paula Ruiz-Duran
Yanyan Qi
Roland Le Borgne
Heinrich Jasper
Tor Erik Rusten
author_facet Caroline Dillard
José Teles-Reis
Ashish Jain
Marina Gonçalves Antunes
Paula Ruiz-Duran
Yanyan Qi
Roland Le Borgne
Heinrich Jasper
Tor Erik Rusten
author_sort Caroline Dillard
collection DOAJ
description Cancer-driving mutations synergize with inflammatory stress signaling pathways during carcinogenesis. Drosophila melanogaster tumor models are increasingly recognized as models to inform conserved molecular mechanisms of tumorigenesis with both local and systemic effects of cancer. Although initial discoveries of the Toll-NFκB signaling pathway in development and immunity were pioneered in Drosophila, limited information is available for its role in cancer progression. Using a well-studied cooperative RasV12-driven epithelial-derived tumor model, we here describe functions of Toll-NF-κB signaling in malignant RasV12, scrib- tumors. The extracellular Toll pathway components ModSP and PGRP-SA and intracellular signaling Kinase, Pelle/IRAK, are rate-limiting for tumor growth. The Toll pathway NFκB protein Dorsal as well as cactus/IκΒ show elevated expression in tumors with highest expression in invasive cell populations. Oncogenic RasV12, and not loss of scribble, confers increased expression and heterogenous distribution of two Dorsal isoforms, DorsalA and DorsalB, in different tumor cell populations. Mechanistic analyses demonstrates that Dorsal, in concert with the BTB-transcription factor Chinmo, drives growth and malignancy by suppressing differentiation, counteracting apoptosis, and promoting invasion of RasV12, scrib- tumors.
format Article
id doaj-art-0a87f6ba5c5a48fba3c2a1e349925aa5
institution DOAJ
issn 1544-9173
1545-7885
language English
publishDate 2025-04-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS Biology
spelling doaj-art-0a87f6ba5c5a48fba3c2a1e349925aa52025-08-20T03:11:51ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852025-04-01234e300266310.1371/journal.pbio.3002663NF-κB signaling driven by oncogenic Ras contributes to tumorigenesis in a Drosophila carcinoma model.Caroline DillardJosé Teles-ReisAshish JainMarina Gonçalves AntunesPaula Ruiz-DuranYanyan QiRoland Le BorgneHeinrich JasperTor Erik RustenCancer-driving mutations synergize with inflammatory stress signaling pathways during carcinogenesis. Drosophila melanogaster tumor models are increasingly recognized as models to inform conserved molecular mechanisms of tumorigenesis with both local and systemic effects of cancer. Although initial discoveries of the Toll-NFκB signaling pathway in development and immunity were pioneered in Drosophila, limited information is available for its role in cancer progression. Using a well-studied cooperative RasV12-driven epithelial-derived tumor model, we here describe functions of Toll-NF-κB signaling in malignant RasV12, scrib- tumors. The extracellular Toll pathway components ModSP and PGRP-SA and intracellular signaling Kinase, Pelle/IRAK, are rate-limiting for tumor growth. The Toll pathway NFκB protein Dorsal as well as cactus/IκΒ show elevated expression in tumors with highest expression in invasive cell populations. Oncogenic RasV12, and not loss of scribble, confers increased expression and heterogenous distribution of two Dorsal isoforms, DorsalA and DorsalB, in different tumor cell populations. Mechanistic analyses demonstrates that Dorsal, in concert with the BTB-transcription factor Chinmo, drives growth and malignancy by suppressing differentiation, counteracting apoptosis, and promoting invasion of RasV12, scrib- tumors.https://doi.org/10.1371/journal.pbio.3002663
spellingShingle Caroline Dillard
José Teles-Reis
Ashish Jain
Marina Gonçalves Antunes
Paula Ruiz-Duran
Yanyan Qi
Roland Le Borgne
Heinrich Jasper
Tor Erik Rusten
NF-κB signaling driven by oncogenic Ras contributes to tumorigenesis in a Drosophila carcinoma model.
PLoS Biology
title NF-κB signaling driven by oncogenic Ras contributes to tumorigenesis in a Drosophila carcinoma model.
title_full NF-κB signaling driven by oncogenic Ras contributes to tumorigenesis in a Drosophila carcinoma model.
title_fullStr NF-κB signaling driven by oncogenic Ras contributes to tumorigenesis in a Drosophila carcinoma model.
title_full_unstemmed NF-κB signaling driven by oncogenic Ras contributes to tumorigenesis in a Drosophila carcinoma model.
title_short NF-κB signaling driven by oncogenic Ras contributes to tumorigenesis in a Drosophila carcinoma model.
title_sort nf κb signaling driven by oncogenic ras contributes to tumorigenesis in a drosophila carcinoma model
url https://doi.org/10.1371/journal.pbio.3002663
work_keys_str_mv AT carolinedillard nfkbsignalingdrivenbyoncogenicrascontributestotumorigenesisinadrosophilacarcinomamodel
AT josetelesreis nfkbsignalingdrivenbyoncogenicrascontributestotumorigenesisinadrosophilacarcinomamodel
AT ashishjain nfkbsignalingdrivenbyoncogenicrascontributestotumorigenesisinadrosophilacarcinomamodel
AT marinagoncalvesantunes nfkbsignalingdrivenbyoncogenicrascontributestotumorigenesisinadrosophilacarcinomamodel
AT paularuizduran nfkbsignalingdrivenbyoncogenicrascontributestotumorigenesisinadrosophilacarcinomamodel
AT yanyanqi nfkbsignalingdrivenbyoncogenicrascontributestotumorigenesisinadrosophilacarcinomamodel
AT rolandleborgne nfkbsignalingdrivenbyoncogenicrascontributestotumorigenesisinadrosophilacarcinomamodel
AT heinrichjasper nfkbsignalingdrivenbyoncogenicrascontributestotumorigenesisinadrosophilacarcinomamodel
AT torerikrusten nfkbsignalingdrivenbyoncogenicrascontributestotumorigenesisinadrosophilacarcinomamodel