Hypoxic regulation of RIOK3 is a major mechanism for cancer cell invasion and metastasis
Open accessAbstract
Hypoxia is a common feature of locally advanced breast cancers that is associated with increased metastasis and poorer survival. Stabilisation of hypoxia-inducible factor-1α (HIF1α) in tumours causes transcriptional changes in numerous genes that function at distinct stages of the metastatic cascade. We demonstrate that expression of RIOK3 (RIght Open reading frame kinase 3) was increased during hypoxic exposure in an HIF1α-dependent manner. RIOK3 was localised to distinct cytoplasmic aggregates in normoxic cells and underwent redistribution to the leading edge of the cell in hypoxia with a corresponding change in the organisation of the actin cytoskeleton. Depletion of RIOK3 expression caused MDA-MB-231 to become elongated and this morphological change was due to a loss of protraction at the trailing edge of the cell. This phenotypic change resulted in reduced cell migration in two-dimensional cultures and inhibition of cell invasion through three-dimensional extracellular matrix. Proteomic analysis identified interactions of RIOK3 with actin and several actin-binding factors including tropomyosins (TPM3 and TPM4) and tropomodulin 3. Depletion of RIOK3 in cells resulted in fewer and less organised actin filaments. Analysis of these filaments showed reduced association of TPM3, particularly during hypoxia, suggesting that RIOK3 regulates actin filament specialisation. RIOK3 depletion reduced the dissemination of MDA-MB-231 cells in both a zebrafish model of systemic metastasis and a mouse model of pulmonary metastasis. These findings demonstrate that RIOK3 is necessary for maintaining actin cytoskeletal organisation required for migration and invasion, biological processes that are necessary for hypoxia-driven metastasis.
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The RIOK3 kinase promotes re-organization of the actin cytoskeleton in a HIF-1α-dependent manner, which increases breast cancer cell migration and invasion/metastasis.
“The RIOK3 kinase promotes re-organization of the actin cytoskeleton in a HIF-1α-dependent manner, which has been shown to increase breast cancer cell migration and invasion/metastasis (Singleton et al., 2015).”
From Therapeutic targeting of hypoxia and hypoxia-inducible factors in cancer (2016) · cites this paper as Singleton et al., 2015
The Introduction says RIOK3 promotes actin-cytoskeleton reorganisation, increasing cell migration and invasion, and that its depletion reduces metastatic potential in vivo. The Results show that hypoxic up-regulation of RIOK3 is HIF1α-dependent. But the Discussion says RIOK3 is required for actin organisation in both normoxia and hypoxia, so the paper does not establish that RIOK3’s actin-organising action itself is HIF1α-dependent. (LLM, conf=0.84)
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- Authors
- Singleton, D. C., Rouhi, P., Zois, C. E., Haider, S., Li, J.-L., Kessler, B. M., Cao, Y., & Harris, A. L.
- Affiliations
- John Radcliffe Hospital (GB)
- Karolinska Institutet (SE)
- University of Oxford (GB)
- Linköping University (SE)
- Corresponding author
- Harris, A L
- Venue
- Oncogene
- Published
- 2014-12-08
- Volume
- 34
- Issue
- 36
- Pages
- 4713-4722
- ISSN
- 0950-9232 (ISSN-L)
- 1476-5594
- PMC
- PMC4430306
- OpenAlex
- W2007979842
- Cited by
- 52
- References
- 43
- Citations by year
- 2026: 4 · 2025: 2 · 2024: 4 · 2023: 4 · 2022: 12 · 2021: 6 · 2020: 4 · 2019: 3 · 2018: 2 · 2017: 6 · 2016: 4 · 2015: 1
- FWCI
- 1.18
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Oncogene (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- PEARL (University of Plymouth) (submittedVersion)
- PEARL (University of Plymouth) (submittedVersion, other-oa)
- Funders
- Breast Cancer Research Foundation
- Cancer Research UK (11359, 16466, A11359)
- National Institute for Health and Care Research (NF-SI-0611-10163)
- European Commission (222741)
- BC Cancer Agency
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mechanisms of cancer metastasis
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
- Keywords
- RIOK3, hypoxia, HIF-1α, breast cancer, tumor invasion, metastasis, cell migration, actin cytoskeleton, tropomyosin, actin-binding proteins, extracellular matrix, lung metastasis
- MeSH terms
- Animals, Breast Neoplasms, Cell Movement, Humans, Actin Cytoskeleton, Neoplasm Invasiveness, Neoplasm Metastasis, Tropomyosin, Zebrafish, Cell Hypoxia, Gene Expression Regulation, Neoplastic, Protein Serine-Threonine Kinases, Cell Line, Tumor, Mice, Hypoxia-Inducible Factor 1, alpha Subunit
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