Gene signature driving invasive mucinous adenocarcinoma of the lung

Abstract Though invasive mucinous adenocarcinoma of the lung (IMA) is pathologically distinctive, the molecular mechanism driving IMA is not well understood, which hampers efforts to identify therapeutic targets. Here, by analyzing gene expression profiles of human and mouse IMA, we identified a Muc...

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Main Authors: Minzhe Guo, Koichi Tomoshige, Michael Meister, Thomas Muley, Takuya Fukazawa, Tomoshi Tsuchiya, Rebekah Karns, Arne Warth, Iris M Fink‐Baldauf, Takeshi Nagayasu, Yoshio Naomoto, Yan Xu, Marcus A Mall, Yutaka Maeda
Format: Article
Language:English
Published: Springer Nature 2017-03-01
Series:EMBO Molecular Medicine
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Online Access:https://doi.org/10.15252/emmm.201606711
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author Minzhe Guo
Koichi Tomoshige
Michael Meister
Thomas Muley
Takuya Fukazawa
Tomoshi Tsuchiya
Rebekah Karns
Arne Warth
Iris M Fink‐Baldauf
Takeshi Nagayasu
Yoshio Naomoto
Yan Xu
Marcus A Mall
Yutaka Maeda
author_facet Minzhe Guo
Koichi Tomoshige
Michael Meister
Thomas Muley
Takuya Fukazawa
Tomoshi Tsuchiya
Rebekah Karns
Arne Warth
Iris M Fink‐Baldauf
Takeshi Nagayasu
Yoshio Naomoto
Yan Xu
Marcus A Mall
Yutaka Maeda
author_sort Minzhe Guo
collection DOAJ
description Abstract Though invasive mucinous adenocarcinoma of the lung (IMA) is pathologically distinctive, the molecular mechanism driving IMA is not well understood, which hampers efforts to identify therapeutic targets. Here, by analyzing gene expression profiles of human and mouse IMA, we identified a Mucinous Lung Tumor Signature of 143 genes, which was unexpectedly enriched in mucin‐producing gastrointestinal, pancreatic, and breast cancers. The signature genes included transcription factors FOXA3, SPDEF, HNF4A, mucins MUC5AC, MUC5B, MUC3, and an inhibitory immune checkpoint VTCN1/B7‐H4 (but not PD‐L1/B7‐H1). Importantly, induction of FOXA3 or SPDEF along with mutant KRAS in lung epithelium was sufficient to develop benign or malignant mucinous lung tumors, respectively, in transgenic mice. FOXA3 and SPDEF induced MUC5AC and MUC5B, while HNF4A induced MUC3 in human mucinous lung cancer cells harboring a KRAS mutation. ChIP‐seq combined with CRISPR/Cas9 determined that upstream enhancer regions of the mucin genes MUC5AC and MUC5B, which were bound by SPDEF, were required for the expression of the mucin genes. Here, we report the molecular signature and gene regulatory network driving mucinous lung tumors.
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spelling doaj-art-0d624d3b6a504f8eae00181f7c7fcdae2025-08-20T04:02:56ZengSpringer NatureEMBO Molecular Medicine1757-46761757-46842017-03-019446248110.15252/emmm.201606711Gene signature driving invasive mucinous adenocarcinoma of the lungMinzhe Guo0Koichi Tomoshige1Michael Meister2Thomas Muley3Takuya Fukazawa4Tomoshi Tsuchiya5Rebekah Karns6Arne Warth7Iris M Fink‐Baldauf8Takeshi Nagayasu9Yoshio Naomoto10Yan Xu11Marcus A Mall12Yutaka Maeda13Perinatal Institute, Divisions of Neonatology, Perinatal and Pulmonary Biology, Cincinnati Children's Hospital Medical Center and the University of Cincinnati College of MedicinePerinatal Institute, Divisions of Neonatology, Perinatal and Pulmonary Biology, Cincinnati Children's Hospital Medical Center and the University of Cincinnati College of MedicineTranslational Research Unit, Thoraxklinik at University Hospital Heidelberg, Translational Lung Research Center Heidelberg (TLRC), Member of the German Center for Lung Research (DZL)Translational Research Unit, Thoraxklinik at University Hospital Heidelberg, Translational Lung Research Center Heidelberg (TLRC), Member of the German Center for Lung Research (DZL)Department of General Surgery, Kawasaki Medical SchoolDepartment of Surgical Oncology, Nagasaki University Graduate School of Biomedical SciencesDivision of Biomedical Informatics, Cincinnati Children's Hospital Medical Center and the University of Cincinnati College of MedicineInstitute of Pathology, Translational Lung Research Center Heidelberg (TLRC), Member of the German Center for Lung Research (DZL), University of HeidelbergPerinatal Institute, Divisions of Neonatology, Perinatal and Pulmonary Biology, Cincinnati Children's Hospital Medical Center and the University of Cincinnati College of MedicineDepartment of Surgical Oncology, Nagasaki University Graduate School of Biomedical SciencesDepartment of General Surgery, Kawasaki Medical SchoolPerinatal Institute, Divisions of Neonatology, Perinatal and Pulmonary Biology, Cincinnati Children's Hospital Medical Center and the University of Cincinnati College of MedicineDepartment of Translational Pulmonology, Translational Lung Research Center Heidelberg (TLRC), Member of the German Center for Lung Research (DZL), University of HeidelbergPerinatal Institute, Divisions of Neonatology, Perinatal and Pulmonary Biology, Cincinnati Children's Hospital Medical Center and the University of Cincinnati College of MedicineAbstract Though invasive mucinous adenocarcinoma of the lung (IMA) is pathologically distinctive, the molecular mechanism driving IMA is not well understood, which hampers efforts to identify therapeutic targets. Here, by analyzing gene expression profiles of human and mouse IMA, we identified a Mucinous Lung Tumor Signature of 143 genes, which was unexpectedly enriched in mucin‐producing gastrointestinal, pancreatic, and breast cancers. The signature genes included transcription factors FOXA3, SPDEF, HNF4A, mucins MUC5AC, MUC5B, MUC3, and an inhibitory immune checkpoint VTCN1/B7‐H4 (but not PD‐L1/B7‐H1). Importantly, induction of FOXA3 or SPDEF along with mutant KRAS in lung epithelium was sufficient to develop benign or malignant mucinous lung tumors, respectively, in transgenic mice. FOXA3 and SPDEF induced MUC5AC and MUC5B, while HNF4A induced MUC3 in human mucinous lung cancer cells harboring a KRAS mutation. ChIP‐seq combined with CRISPR/Cas9 determined that upstream enhancer regions of the mucin genes MUC5AC and MUC5B, which were bound by SPDEF, were required for the expression of the mucin genes. Here, we report the molecular signature and gene regulatory network driving mucinous lung tumors.https://doi.org/10.15252/emmm.201606711FOXA3IMAMUC5AC/5BSPDEFVTCN1
spellingShingle Minzhe Guo
Koichi Tomoshige
Michael Meister
Thomas Muley
Takuya Fukazawa
Tomoshi Tsuchiya
Rebekah Karns
Arne Warth
Iris M Fink‐Baldauf
Takeshi Nagayasu
Yoshio Naomoto
Yan Xu
Marcus A Mall
Yutaka Maeda
Gene signature driving invasive mucinous adenocarcinoma of the lung
EMBO Molecular Medicine
FOXA3
IMA
MUC5AC/5B
SPDEF
VTCN1
title Gene signature driving invasive mucinous adenocarcinoma of the lung
title_full Gene signature driving invasive mucinous adenocarcinoma of the lung
title_fullStr Gene signature driving invasive mucinous adenocarcinoma of the lung
title_full_unstemmed Gene signature driving invasive mucinous adenocarcinoma of the lung
title_short Gene signature driving invasive mucinous adenocarcinoma of the lung
title_sort gene signature driving invasive mucinous adenocarcinoma of the lung
topic FOXA3
IMA
MUC5AC/5B
SPDEF
VTCN1
url https://doi.org/10.15252/emmm.201606711
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