Breast-cancer-secreted miR-122 reprograms glucose metabolism in premetastatic niche to promote metastasis
Open accessAbstract
Reprogrammed glucose metabolism as a result of increased glycolysis and glucose uptake is a hallmark of cancer. Here we show that cancer cells can suppress glucose uptake by non-tumour cells in the premetastatic niche, by secreting vesicles that carry high levels of the miR-122 microRNA. High miR-122 levels in the circulation have been associated with metastasis in breast cancer patients, and we show that cancer-cell-secreted miR-122 facilitates metastasis by increasing nutrient availability in the premetastatic niche. Mechanistically, cancer-cell-derived miR-122 suppresses glucose uptake by niche cells in vitro and in vivo by downregulating the glycolytic enzyme pyruvate kinase. In vivo inhibition of miR-122 restores glucose uptake in distant organs, including brain and lungs, and decreases the incidence of metastasis. These results demonstrate that, by modifying glucose utilization by recipient premetastatic niche cells, cancer-derived extracellular miR-122 is able to reprogram systemic energy metabolism to facilitate disease progression.
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miR-122 downregulates the glycolytic enzyme pyruvate kinase and restores glucose uptake by lungs and brain and lessens disease progression.
“Mechanistically, miR-122 downregulate the glycolytic enzyme pyruvate kinase and restores glucose uptake by lungs and brain and lessen disease progression [177].”
From Tumor microenvironment complexity and therapeutic implications at a glance (2020) · cites this paper as [177]
The Results section confirms that miR-122 downregulates pyruvate kinase, but reports that miR-122 reduces glucose uptake by niche cells and promotes metastasis—the opposite of the claimed effects. In “Systemic miR-122 intervention,” inhibiting miR-122 reduced the incidence of brain and lung metastasis and alleviated suppressed glucose uptake in the brain; restoration of uptake in the lungs was not significant. (LLM, conf=0.91)
Checked by a reasoning model — may be wrong.
Experimental — accuracy not yet measuredBreast cancer cells secrete miR-122-enriched vesicles to suppress glucose uptake by niche cells in vitro and in vivo.
“To increase nutrient availability, breast cancer cells secrete miR-122 -enriched vesicles to suppress glucose uptake by niche cells in vitro and in vivo.”
From Tumor microenvironment complexity and therapeutic implications at a glance (2020) · cites this paper as [177]
Experimental — accuracy not yet measuredCancer cells can systemically reprogram energy metabolism by recipient premetastatic niche cells to promote metastasis.
“Another interesting role of the exosome as mediators of cancer cell interaction with non-malignant cells is the observation that cancer cells can systemically reprogram energy metabolism by recipient premetastatic niche cells to promote metastasis.”
From Tumor microenvironment complexity and therapeutic implications at a glance (2020) · cites this paper as [177]
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Extracellular Vesicles in Brain Tumors and Neurodegenerative Diseases
Ciregia, F., Urbani, A., & Palmisano, G. (2017) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2017.00276 · Cited by 110 · see citing works
MicroRNA-122 in human cancers: from mechanistic to clinical perspectives
Faramin Lashkarian, M., Hashemipour, N., Niaraki, N., Soghala, S., Moradi, A., Sarhangi, S., Hatami, M., Aghaei-Zarch, F., Khosravifar, M., Mohammadzadeh, A., et al. (2023) · Cancer Cell International · doi:10.1186/s12935-023-02868-z · Cited by 105 · see citing works
Molecular alterations of cancer cell and tumour microenvironment in metastatic gastric cancer
Li, W., Ng, J. M.-K., Wong, C. C., Ng, E. K. W., & Yu, J. (2018) · Oncogene · doi:10.1038/s41388-018-0341-x · Cited by 87 · see citing works
Mazumdar, A., Urdinez, J., Boro, A., Arlt, M. J. E., Egli, F. E., Niederöst, B., Jaeger, P. K., Moschini, G., Muff, R., Fuchs, B., et al. (2020) · Cancers · doi:10.3390/cancers12113457 · Cited by 40 · see citing works
The emerging regulatory roles of non-coding RNAs associated with glucose metabolism in breast cancer
Kansara, S., Singh, A., Badal, A. K., Rani, R., Baligar, P., Garg, M., & Pandey, A. K. (2023) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2023.06.007 · Cited by 32 · see citing works
Metabolic reprogramming: The driving force behind cancer drug resistance
El-Sehrawy, A. A. M. A., Hsu, C.-Y., Alkhathami, A. G., Chandra, M., Basunduwah, T. S., Malathi, H., Senapati, J. N., Gautam, A., Kadhem, M., & Yasin, H. A. (2025) · Seminars in Oncology · doi:10.1016/j.seminoncol.2025.152392 · Cited by 11 · see citing works
Self-citation
- Authors
- Fong, M. Y., Zhou, W., Liu, L., Alontaga, A. Y., Chandra, M., Ashby, J., Chow, A., O’Connor, S. T. F., Li, S., Chin, A. R., Somlo, G., Palomares, M., Li, Z., Tremblay, J. R., Tsuyada, A., Sun, G., Reid, M. A., Wu, X., Swiderski, P., Ren, X., Shi, Y., Kong, M., Zhong, W., Chen, Y., & Wang, S. E.
- Affiliations
- City Of Hope National Medical Center (US)
- University of California, Riverside (US)
- Tianjin Medical University Cancer Institute and Hospital (CN)
- Corresponding author
- Wang, Shizhen Emily
- ORCID
- Venue
- Nature Cell Biology
- Published
- 2015-01-26
- Volume
- 17
- Issue
- 2
- Pages
- 183-194
- ISSN
- 1465-7392 (ISSN-L)
- 1476-4679
- PMC
- PMC4380143
- OpenAlex
- W1975355918
- Cited by
- 1,118
- References
- 74
- Citations by year
- 2026: 47 · 2025: 75 · 2024: 90 · 2023: 115 · 2022: 119 · 2021: 154 · 2020: 138 · 2019: 98 · 2018: 106 · 2017: 88 · 2016: 58 · 2015: 28
- FWCI
- 30.84
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Cell Biology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- National Cancer Institute (P30CA-33572, R01CA166020, R01CA163586, P30CA033572)
- National Institute of General Medical Sciences (R01GM086171, R01GM102538)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
- Keywords
- breast cancer, miR-122, extracellular vesicles, pre-metastatic niche, glucose metabolism, glucose uptake, pyruvate kinase, cancer-associated fibroblasts, tumor microenvironment, metastasis, circulating microRNAs
- MeSH terms
- Astrocytes, Base Sequence, Breast Neoplasms, Bromodeoxyuridine, Female, Fibroblasts, Glucose, Humans, Luciferases, Lung, Molecular Sequence Data, Neoplasm Metastasis, Pyruvate Kinase, Down-Regulation, MicroRNAs, Cell Line, Tumor, Cell Proliferation, Exosomes
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