Cited by 472TGF-β signaling in diseasesCancer Cells and MetastasisDevelopmental Biology and Gene Regulation

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TGF-β Promotes Heterogeneity and Drug Resistance in Squamous Cell Carcinoma

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Oshimori, Naoki, Oristian, Daniel, Fuchs, Elaine·2015·Cell

DOI 10.1016/j.cell.2015.01.043PMC PMC4509607

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Abstract

Subsets of long-lived, tumor-initiating stem cells often escape cancer therapies. However, sources and mechanisms that generate tumor heterogeneity and drug-resistant cell population are still unfolding. Here, we devise a functional reporter system to lineage trace and/or genetic ablate signaling in TGF-β-activated squamous cell carcinoma stem cells (SCC-SCs). Dissecting TGF-β's impact on malignant progression, we demonstrate that TGF-β concentrating near tumor-vasculature generates heterogeneity in TGF-β signaling at tumor-stroma interface and bestows slower-cycling properties to neighboring SCC-SCs. While non-responding progenies proliferate faster and accelerate tumor growth, TGF-β-responding progenies invade, aberrantly differentiate, and affect gene expression. Intriguingly, TGF-β-responding SCC-SCs show increased protection against anti-cancer drugs, but slower-cycling alone does not confer survival. Rather, TGF-β transcriptionally activates p21, which stabilizes NRF2, thereby markedly enhancing glutathione metabolism and diminishing effectiveness of anti-cancer therapeutics. Together, these findings establish a surprising non-genetic paradigm for TGF-β signaling in fueling heterogeneity in SCC-SCs, tumor characteristics, and drug resistance.

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Authors: Oshimori, N., Oristian, D., & Fuchs, E.
Affiliations: Rockefeller University (US)
Howard Hughes Medical Institute (US)
Corresponding author: Fuchs, Elaine
ORCID: Oshimori, Naoki
Fuchs, Elaine
Venue: Cell
Publisher: Elsevier BV
Published: 2015-02
Volume: 160
Issue: 5
Pages: 963-976
ISSN: 0092-8674 (ISSN-L)
DOI: 10.1016/j.cell.2015.01.043
PMC: PMC4509607
OpenAlex: W2120246444
Cited by: 471
References: 52
Citations by year: 2026: 18 · 2025: 25 · 2024: 35 · 2023: 46 · 2022: 40 · 2021: 60 · 2020: 51 · 2019: 52 · 2018: 41 · 2017: 42 · 2016: 46 · 2015: 13
FWCI: 20.54
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 390 d)
Locations: Cell (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: Howard Hughes Medical Institute
New York State Department of Health
National Institutes of Health
Weill Cornell Medical College
Japan Society for the Promotion of Science
National Cancer Institute (R00CA178197, K99CA178197)
National Institute of Arthritis and Musculoskeletal and Skin Diseases (R01AR031737)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › TGF-β signaling in diseases
Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
Keywords: TGF-beta signaling, squamous cell carcinoma, cancer stem cells, tumor heterogeneity, drug resistance, tumor-stroma interface, tumor vasculature, cell cycle, p21, Nrf2, glutathione metabolism, lineage tracing, malignant progression, tumor invasion, aberrant differentiation
MeSH terms: Animals, Carcinoma, Squamous Cell, Cisplatin, Female, Glutathione, Head and Neck Neoplasms, Humans, Mice, Nude, Neoplasm Transplantation, Skin Neoplasms, Tetradecanoylphorbol Acetate, Neoplastic Stem Cells, 9,10-Dimethyl-1,2-benzanthracene, Signal Transduction, Transforming Growth Factor beta, Drug Resistance, Neoplasm, Gene Expression Profiling, NF-E2-Related Factor 2, Mice, Heterografts

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TGF-β Promotes Heterogeneity and Drug Resistance in Squamous Cell Carcinoma

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