Activation of APOBEC3 cytidine deaminases and endogenous retroviruses is integrated by MUC1-C in NSCLC cells

Abstract The APOBEC3 (A3) genes encoding cytidine deaminases evolved in mammals to restrict retroviral replication. The MUC1 gene appeared in mammals to protect barrier tissues from viral infections. There is no known involvement of the MUC1 encoded MUC1-C/M1C protein in the regulation of A3s. We fo...

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Main Authors: Naoki Haratake, Shinkichi Takamori, Hideko Isozaki, Keisuke Shigeta, Chie Kikutake, Hiroki Ozawa, Atrayee Bhattacharya, Ayako Nakashoji, Mikita Suyama, Tomoyoshi Takenaka, Tomoharu Yoshizumi, Atsushi Osoegawa, Aaron N. Hata, Donald Kufe
Format: Article
Language:English
Published: Nature Publishing Group 2025-08-01
Series:Cell Death Discovery
Online Access:https://doi.org/10.1038/s41420-025-02673-9
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author Naoki Haratake
Shinkichi Takamori
Hideko Isozaki
Keisuke Shigeta
Chie Kikutake
Hiroki Ozawa
Atrayee Bhattacharya
Ayako Nakashoji
Mikita Suyama
Tomoyoshi Takenaka
Tomoharu Yoshizumi
Atsushi Osoegawa
Aaron N. Hata
Donald Kufe
author_facet Naoki Haratake
Shinkichi Takamori
Hideko Isozaki
Keisuke Shigeta
Chie Kikutake
Hiroki Ozawa
Atrayee Bhattacharya
Ayako Nakashoji
Mikita Suyama
Tomoyoshi Takenaka
Tomoharu Yoshizumi
Atsushi Osoegawa
Aaron N. Hata
Donald Kufe
author_sort Naoki Haratake
collection DOAJ
description Abstract The APOBEC3 (A3) genes encoding cytidine deaminases evolved in mammals to restrict retroviral replication. The MUC1 gene appeared in mammals to protect barrier tissues from viral infections. There is no known involvement of the MUC1 encoded MUC1-C/M1C protein in the regulation of A3s. We found that induction of MUC1-C in NSCLC cells treated with EGFR inhibitors integrates activation of an inflammatory memory response with the type I interferon (IFN) STAT1/STAT2/IRF9 (U-ISGF3) pathway. In turn, MUC1-C drives expression of A3 genes by activating their U-ISGF3-stimulated response elements (ISREs). We also report that MUC1-C-mediated induction of type II IFN STAT1 homodimer (U-GAF) complexes and the gamma-associated signaling (GAS) pathway drives human endogenous retrovirus HERV-K102/K108 expression. Our results in NSCLC cell line and patient-derived models further demonstrate that MUC1-C activates A3 and HERV-K expression by a common MUC1-C→STAT1 auto-inductive pathway. These previously unrecognized findings demonstrate that a MUC1-C-driven inflammatory pathway coordinates activation of APOBEC3 and HERV-K expression.
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spelling doaj-art-e62311c0e7ae4926bc07209f285c49142025-08-20T04:01:46ZengNature Publishing GroupCell Death Discovery2058-77162025-08-0111111410.1038/s41420-025-02673-9Activation of APOBEC3 cytidine deaminases and endogenous retroviruses is integrated by MUC1-C in NSCLC cellsNaoki Haratake0Shinkichi Takamori1Hideko Isozaki2Keisuke Shigeta3Chie Kikutake4Hiroki Ozawa5Atrayee Bhattacharya6Ayako Nakashoji7Mikita Suyama8Tomoyoshi Takenaka9Tomoharu Yoshizumi10Atsushi Osoegawa11Aaron N. Hata12Donald Kufe13Department of Medical Oncology, Dana-Farber Cancer Institute, Harvard Medical SchoolDepartment of Medical Oncology, Dana-Farber Cancer Institute, Harvard Medical SchoolDepartment of Medicine, Massachusetts General Hospital, Harvard Medical SchoolDepartment of Medical Oncology, Dana-Farber Cancer Institute, Harvard Medical SchoolDivision of Bioinformatics, Medical Institute of Bioregulation, Kyushu UniversityDepartment of Medical Oncology, Dana-Farber Cancer Institute, Harvard Medical SchoolDepartment of Medical Oncology, Dana-Farber Cancer Institute, Harvard Medical SchoolDepartment of Medical Oncology, Dana-Farber Cancer Institute, Harvard Medical SchoolDivision of Bioinformatics, Medical Institute of Bioregulation, Kyushu UniversityDepartment of Surgery and Science, Graduate School of Medical Sciences, Kyushu UniversityDepartment of Surgery and Science, Graduate School of Medical Sciences, Kyushu UniversityDepartment of Thoracic and Breast Surgery, Oita University Faculty of MedicineDepartment of Medicine, Massachusetts General Hospital, Harvard Medical SchoolDepartment of Medical Oncology, Dana-Farber Cancer Institute, Harvard Medical SchoolAbstract The APOBEC3 (A3) genes encoding cytidine deaminases evolved in mammals to restrict retroviral replication. The MUC1 gene appeared in mammals to protect barrier tissues from viral infections. There is no known involvement of the MUC1 encoded MUC1-C/M1C protein in the regulation of A3s. We found that induction of MUC1-C in NSCLC cells treated with EGFR inhibitors integrates activation of an inflammatory memory response with the type I interferon (IFN) STAT1/STAT2/IRF9 (U-ISGF3) pathway. In turn, MUC1-C drives expression of A3 genes by activating their U-ISGF3-stimulated response elements (ISREs). We also report that MUC1-C-mediated induction of type II IFN STAT1 homodimer (U-GAF) complexes and the gamma-associated signaling (GAS) pathway drives human endogenous retrovirus HERV-K102/K108 expression. Our results in NSCLC cell line and patient-derived models further demonstrate that MUC1-C activates A3 and HERV-K expression by a common MUC1-C→STAT1 auto-inductive pathway. These previously unrecognized findings demonstrate that a MUC1-C-driven inflammatory pathway coordinates activation of APOBEC3 and HERV-K expression.https://doi.org/10.1038/s41420-025-02673-9
spellingShingle Naoki Haratake
Shinkichi Takamori
Hideko Isozaki
Keisuke Shigeta
Chie Kikutake
Hiroki Ozawa
Atrayee Bhattacharya
Ayako Nakashoji
Mikita Suyama
Tomoyoshi Takenaka
Tomoharu Yoshizumi
Atsushi Osoegawa
Aaron N. Hata
Donald Kufe
Activation of APOBEC3 cytidine deaminases and endogenous retroviruses is integrated by MUC1-C in NSCLC cells
Cell Death Discovery
title Activation of APOBEC3 cytidine deaminases and endogenous retroviruses is integrated by MUC1-C in NSCLC cells
title_full Activation of APOBEC3 cytidine deaminases and endogenous retroviruses is integrated by MUC1-C in NSCLC cells
title_fullStr Activation of APOBEC3 cytidine deaminases and endogenous retroviruses is integrated by MUC1-C in NSCLC cells
title_full_unstemmed Activation of APOBEC3 cytidine deaminases and endogenous retroviruses is integrated by MUC1-C in NSCLC cells
title_short Activation of APOBEC3 cytidine deaminases and endogenous retroviruses is integrated by MUC1-C in NSCLC cells
title_sort activation of apobec3 cytidine deaminases and endogenous retroviruses is integrated by muc1 c in nsclc cells
url https://doi.org/10.1038/s41420-025-02673-9
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