Microvesicles secreted by macrophages shuttle invasion-potentiating microRNAs into breast cancer cells
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BACKGROUND: Tumor-associated macrophages (TAMs) are alternatively activated cells induced by interleukin-4 (IL-4)-releasing CD4+ T cells. TAMs promote breast cancer invasion and metastasis; however, the mechanisms underlying these interactions between macrophages and tumor cells that lead to cancer metastasis remain elusive. Previous studies have found microRNAs (miRNAs) circulating in the peripheral blood and have identified microvesicles, or exosomes, as mediators of cell-cell communication. Therefore, one alternative mechanism for the promotion of breast cancer cell invasion by TAMs may be through macrophage-secreted exosomes, which would deliver invasion-potentiating miRNAs to breast cancer cells. RESULTS: We utilized a co-culture system with IL-4-activated macrophages and breast cancer cells to verify that miRNAs are transported from macrophages to breast cancer cells. The shuttling of fluorescently-labeled exogenous miRNAs from IL-4-activated macrophages to co-cultivated breast cancer cells without direct cell-cell contact was observed. miR-223, a miRNA specific for IL-4-activated macrophages, was detected within the exosomes released by macrophages and was significantly elevated in the co-cultivated SKBR3 and MDA-MB-231 cells. The invasiveness of the co-cultivated breast cancer cells decreased when the IL-4-activated macrophages were treated with a miR-223 antisense oligonucleotide (ASO) that would inhibit miR-223 expression. Furthermore, results from a functional assay revealed that miR-223 promoted the invasion of breast cancer cells via the Mef2c-β-catenin pathway. CONCLUSIONS: We conclude that macrophages regulate the invasiveness of breast cancer cells through exosome-mediated delivery of oncogenic miRNAs. Our data provide insight into the mechanisms underlying the metastasis-promoting interactions between macrophages and breast cancer cells.
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Secretion of miRNAs via exosomes is regulated by signaling molecules such as interleukin-4 and docosahexaenoic acid.
“Secretion of miRNAs via exosomes have also been reported to be regulated by signaling molecules, such as interleukin-4 (IL4) (132) and Docosahexaenoic acid (DHA) (133).”
From Overview of MicroRNA Biogenesis, Mechanisms of Actions, and Circulation (2018) · cites this paper as [132]
IL4-activated macrophages were found to secrete exosomes carrying oncogenic miRNAs to promote invasiveness of breast cancer cells.
“IL4-activated macrophages were found to secrete exosomes carrying oncogenic miRNAs to promote invasiveness of breast cancer cells (132).”
From Overview of MicroRNA Biogenesis, Mechanisms of Actions, and Circulation (2018) · cites this paper as [132]
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- Authors
- Yang, M., Chen, J., Su, F., Yu, B., Su, F., Lin, L., Liu, Y., Huang, J.-D., & Song, E.
- Affiliations
- Sun Yat-sen University (CN)
- University of Hong Kong (HK)
- Corresponding author
- Huang, Jian-Dong
- Song, Erwei
- Venue
- Molecular Cancer
- Published
- 2011-09-22
- Volume
- 10
- Issue
- 1
- Pages
- 117-117
- ISSN
- 1476-4598 (ISSN-L)
- PMC
- PMC3190352
- OpenAlex
- W2059266855
- Cited by
- 693
- References
- 48
- Citations by year
- 2026: 11 · 2025: 15 · 2024: 34 · 2023: 43 · 2022: 45 · 2021: 60 · 2020: 66 · 2019: 48 · 2018: 45 · 2017: 50 · 2016: 54 · 2015: 78 · 2014: 54 · 2013: 45 · 2012: 41
- FWCI
- 18.55
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Molecular Cancer (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- The HKU Scholars Hub (University of Hong Kong) (submittedVersion, cc-by-nc-nd)
- Funders
- National Natural Science Foundation of China (30972785, 2009CB521706, 2010CB912800, 30921140312, 30830110, KLB09001, 2011CB504203)
- Sun Yat-sen University (KLB09001, 2011CB504203, 2010CB912800)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
- Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
- Keywords
- tumor-associated macrophages, microvesicles, exosomes, microRNA, breast cancer invasion, miR-223, IL-4, metastasis, antisense oligonucleotides
- MeSH terms
- Breast Neoplasms, Cell Communication, Female, Humans, Macrophages, Neoplasm Invasiveness, Interleukin-4, Genes, Reporter, Myogenic Regulatory Factors, Coculture Techniques, Cell Culture Techniques, 3' Untranslated Regions, MADS Domain Proteins, RNA Interference, MicroRNAs, Cell Line, Tumor, Luciferases, Renilla, beta Catenin, Exosomes, MEF2 Transcription Factors
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