FXYD3 functionally demarcates an ancestral breast cancer stem cell subpopulation with features of drug-tolerant persisters.


Journal

The Journal of clinical investigation
ISSN: 1558-8238
Titre abrégé: J Clin Invest
Pays: United States
ID NLM: 7802877

Informations de publication

Date de publication:
15 Nov 2023
Historique:
received: 08 11 2022
accepted: 21 09 2023
medline: 16 11 2023
pubmed: 15 11 2023
entrez: 15 11 2023
Statut: epublish

Résumé

The heterogeneity of cancer stem cells (CSCs) within tumors presents a challenge in therapeutic targeting. To decipher the cellular plasticity that fuels phenotypic heterogeneity, we undertook single-cell transcriptomics analysis in triple-negative breast cancer (TNBC) to identify subpopulations in CSCs. We found a subpopulation of CSCs with ancestral features that is marked by FXYD domain-containing ion transport regulator 3 (FXYD3), a component of the Na+/K+ pump. Accordingly, FXYD3+ CSCs evolve and proliferate, while displaying traits of alveolar progenitors that are normally induced during pregnancy. Clinically, FXYD3+ CSCs were persistent during neoadjuvant chemotherapy, hence linking them to drug-tolerant persisters (DTPs) and identifying them as crucial therapeutic targets. Importantly, FXYD3+ CSCs were sensitive to senolytic Na+/K+ pump inhibitors, such as cardiac glycosides. Together, our data indicate that FXYD3+ CSCs with ancestral features are drivers of plasticity and chemoresistance in TNBC. Targeting the Na+/K+ pump could be an effective strategy to eliminate CSCs with ancestral and DTP features that could improve TNBC prognosis.

Identifiants

pubmed: 37966117
pii: 166666
doi: 10.1172/JCI166666
pmc: PMC10645391
doi:
pii:

Substances chimiques

FXYD3 protein, human 0
Membrane Proteins 0
Neoplasm Proteins 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

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Auteurs

Mengjiao Li (M)

Division of Cancer Cell Biology, Cancer Research Institute, and.

Tatsunori Nishimura (T)

Division of Cancer Cell Biology, Cancer Research Institute, and.

Yasuto Takeuchi (Y)

Division of Cancer Cell Biology, Cancer Research Institute, and.
Institute for Frontier Science Initiative, Kanazawa University, Kanazawa City, Japan.

Tsunaki Hongu (T)

Division of Cancer Cell Biology, Cancer Research Institute, and.

Yuming Wang (Y)

Division of Cancer Cell Biology, Cancer Research Institute, and.

Daisuke Shiokawa (D)

Division of Cancer Differentiation, National Cancer Center Research Institute, Chuo-ku, Tokyo, Japan.

Kang Wang (K)

Department of Oncology-Pathology, Karolinska Institute, Karolinska University Hospital, Stockholm, Sweden.

Haruka Hirose (H)

Division of Systems Biology, Graduate School of Medicine, Nagoya University, Nagoya City, Japan.

Asako Sasahara (A)

Department of Breast and Endocrine Surgery, Graduate School of Medicine, The University of Tokyo, Bunkyo-ku, Tokyo, Japan.

Masao Yano (M)

Department of Surgery, Minami-machida Hospital, Machida City, Tokyo, Japan.

Satoko Ishikawa (S)

Department of Breast Oncology, Kanazawa University Hospital, Kanazawa City, Japan.

Masafumi Inokuchi (M)

Department of Breast Oncology, Kanazawa University Hospital, Kanazawa City, Japan.

Tetsuo Ota (T)

Department of Breast Oncology, Kanazawa University Hospital, Kanazawa City, Japan.

Masahiko Tanabe (M)

Department of Breast and Endocrine Surgery, Graduate School of Medicine, The University of Tokyo, Bunkyo-ku, Tokyo, Japan.

Kei-Ichiro Tada (KI)

Department of Breast and Endocrine Surgery, Nihon University, Itabashi-ku, Tokyo, Japan.

Tetsu Akiyama (T)

Laboratory of Molecular and Genetic Information, Institute for Quantitative Biosciences, The University of Tokyo, Bunkyo-ku, Tokyo, Japan.

Xi Cheng (X)

Department of Oncology, Shanghai Medical College, Fudan University, Shanghai, China.

Chia-Chi Liu (CC)

North Shore Heart Research Group, Kolling Institute, University of Sydney, Sydney, New South Wales, Australia.

Toshinari Yamashita (T)

Department of Breast and Endocrine Surgery, Kanagawa Cancer Center, Yokohama City, Kanagawa, Japan.

Sumio Sugano (S)

Tokyo Medical and Dental University, Bunkyo-ku, Tokyo, Japan.

Yutaro Uchida (Y)

Department of Systems Biomedicine, Tokyo Medical and Dental University, Bunkyo-ku, Tokyo, Japan.

Tomoki Chiba (T)

Department of Systems Biomedicine, Tokyo Medical and Dental University, Bunkyo-ku, Tokyo, Japan.

Hiroshi Asahara (H)

Department of Systems Biomedicine, Tokyo Medical and Dental University, Bunkyo-ku, Tokyo, Japan.

Masahiro Nakagawa (M)

Department of Pathology and Tumor Biology, Graduate School of Medicine, Kyoto University, Sakyo-ku, Kyoto, Japan.

Shinya Sato (S)

Molecular Pathology and Genetics Division, Kanagawa Cancer Center Research Institute, Yokohama City, Kanagawa, Japan.

Yohei Miyagi (Y)

Molecular Pathology and Genetics Division, Kanagawa Cancer Center Research Institute, Yokohama City, Kanagawa, Japan.

Teppei Shimamura (T)

Division of Systems Biology, Graduate School of Medicine, Nagoya University, Nagoya City, Japan.

Luis Augusto E Nagai (LAE)

Laboratory of Computational Genomics, Institute for Quantitative Biosciences.

Akinori Kanai (A)

Department of Computational Biology and Medical Sciences, Graduate School of Frontier Biosciences.

Manami Katoh (M)

Department of Cardiovascular Medicine, Graduate School of Medicine.
Genome Science Division, Research Center for Advanced Science and Technology.

Seitaro Nomura (S)

Department of Cardiovascular Medicine, Graduate School of Medicine.
Genome Science Division, Research Center for Advanced Science and Technology.
Department of Frontier Cardiovascular Science, Graduate School of Medicine, and.

Ryuichiro Nakato (R)

Laboratory of Computational Genomics, Institute for Quantitative Biosciences.

Yutaka Suzuki (Y)

Department of Computational Biology and Medical Sciences, Graduate School of Frontier Biosciences.

Arinobu Tojo (A)

Tokyo Medical and Dental University, Bunkyo-ku, Tokyo, Japan.
Institute of Medical Science, The University of Tokyo, Tokyo, Japan.

Dominic C Voon (DC)

Institute for Frontier Science Initiative, Kanazawa University, Kanazawa City, Japan.
Inflammation and Epithelial Plasticity Unit, Cancer Research Institute, Kanazawa University, Kanazawa City, Japan.

Seishi Ogawa (S)

Department of Pathology and Tumor Biology, Graduate School of Medicine, Kyoto University, Sakyo-ku, Kyoto, Japan.

Koji Okamoto (K)

Division of Cancer Differentiation, National Cancer Center Research Institute, Chuo-ku, Tokyo, Japan.
Advanced Comprehensive Research Organization, Teikyo University, Itabashi-ku, Tokyo, Japan.

Theodoros Foukakis (T)

Department of Oncology-Pathology, Karolinska Institute, Karolinska University Hospital, Stockholm, Sweden.

Noriko Gotoh (N)

Division of Cancer Cell Biology, Cancer Research Institute, and.
Institute for Frontier Science Initiative, Kanazawa University, Kanazawa City, Japan.

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