The hypoxia‐induced changes in miRNA‐mRNA in RNA ‐induced silencing complexes and HIF ‐2 induced miRNAs in human endothelial cells
Open accessAbstract
The cellular adaptive response to hypoxia relies on the expression of hypoxia‐inducible factors (HIFs), HIF‐1 and HIF‐2. HIFs regulate global gene expression changes during hypoxia that are necessary for restoring oxygen homeostasis and promoting cell survival. In the early stages of hypoxia, HIF‐1 is elevated, whereas at the later stages, HIF‐2 becomes the predominant form. What governs the transition between the two HIFs (the HIF switch) and the role of miRNAs in this regulation are not completely clear. Genome‐wide expression studies on the miRNA content of RNA‐induced silencing complexes (RISC) in HUVECs exposed to hypoxia compared to the global miRNA‐Seq analysis revealed very specific differences between these two populations. We analyzed the miRNA and mRNA composition of RISC at 2 h (mainly HIF‐1 driven), 8 h (HIF‐1 and HIF‐2 elevated), and 16 h (mainly HIF‐2 driven) in a gene ontology context. This allowed for determining the direct impact of the miRNAs in modulating the cellular signaling pathways involved in the hypoxic adaptive response. Our results indicate that the miRNA‐mRNA RISC components control the adaptive responses, and this does not always rely on the miRNA transcriptional elevations during hypoxia. Furthermore, we demonstrate that the hypoxic levels of the vast majority of HIF‐1‐dependent miRNAs (including miR‐210‐3p) are also HIF‐2 dependent and that HIF‐2 governs the expression of 11 specific miRNAs. In summary, the switch from HIF‐1 to HIF‐2 during hypoxia provides an important level of miRNA‐driven control in the adaptive pathways in endothelial cells.
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In most tissues, hypoxic signaling follows a characteristic temporal pattern in which HIF-1 drives the early response and is subsequently replaced or supplemented by HIF-2-and in some contexts HIF-3-during prolonged hypoxia.
“In most tissues, hypoxic signaling follows a characteristic temporal pattern in which HIF-1 drives the early response and is subsequently replaced or supplemented by HIF-2 - and in some contexts HIF-3 - during prolonged hypoxia”
From HIF inhibition: Current strategies and clinical challenges (2026) · cites this paper as [67]
The Introduction describes early HIF-1 activity being supported and then replaced by HIF-2, and the Results document that transition in human endothelial cells. The paper does not establish that this pattern occurs in most tissues, and the passages found do not address a role for HIF-3 during prolonged hypoxia. (LLM, conf=0.88)
Experimental — accuracy not yet measuredThe HIF switch supports long-term adaptation while limiting oxidative stress and metabolic imbalance.
“This “HIF switch” supports long-term adaptation while limiting oxidative stress and metabolic imbalance [60,67,74,75]”
From HIF inhibition: Current strategies and clinical challenges (2026) · cites this paper as [67]
The Results (‘Changing mRNA and miRNA content of RISC components during the HIF switch’; page not provided) link the HIF-1-to-HIF-2 transition during prolonged hypoxia to adaptive responses and tuning of cellular metabolism in endothelial cells. The paper does not establish that the switch limits oxidative stress or metabolic imbalance. (LLM, conf=0.84)
Experimental — accuracy not yet measuredIndirect or transient suppression of HIF-α accumulation often proves effective only in tightly controlled in vitro settings and rarely translates into sustained in vivo efficacy.
“More broadly, consideration of HIF isoform switching and dynamic hypoxic signaling suggests that indirect or transient suppression of HIF-α accumulation often proves effective only in tightly controlled in vitro settings [67,270,271,275]. These approaches rarely translate into sustained in vivo efficacy.”
From HIF inhibition: Current strategies and clinical challenges (2026) · cites this paper as [67]
The Introduction describes a transition from HIF-1 to HIF-2 signaling, and the Results report efficient HIF1A and EPAS1 silencing in cultured endothelial cells. The paper does not say that suppression is effective only under tightly controlled in vitro conditions or assess whether it produces sustained in vivo efficacy. (LLM, conf=0.82)
Experimental — accuracy not yet measured
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- [61]Bartoszewski R, Moszynska A, Serocki M, Cabaj A, Polten A, Ochocka R, Dell'Italia L, Bartoszewska S, Kroliczewski J, Dabrowski MD, and Collawn JF (2019) Primary endothelial cell-specific regulation of hypoxia-inducible factor (HIF)-1 and HIF-2 and their target gene expression profiles during hypoxia. Faseb Journal 33, 7929– 7941 30917010 PMC6593883
Cited by
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- Authors
- Moszyńska, A., Jaśkiewicz, M., Serocki, M., Cabaj, A., Crossman, D. K., Bartoszewska, S., Gebert, M., Dąbrowski, M., Collawn, J. F., & Bartoszewski, R.
- Affiliations
- Gdańsk Medical University (PL)
- Instytut Biologii Doświadczalnej im. Marcelego Nenckiego (PL)
- University of Alabama at Birmingham (US)
- Department of Biology and Pharmaceutical Botany Medical University of Gdansk Gdansk Poland
- ORCID
- Venue
- The FASEB Journal
- Publisher
- Wiley
- Published
- 2022-06-17
- Volume
- 36
- Issue
- 7
- Pages
- e22412-e22412
- ISSN
- 0892-6638 (ISSN-L)
- 1530-6860
- PMC
- PMC9220987
- OpenAlex
- W4283067167
- Cited by
- 53
- References
- 82
- Citations by year
- 2026: 14 · 2025: 8 · 2024: 20 · 2023: 9 · 2022: 2
- FWCI
- 4.31
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- The FASEB Journal (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health (NIH P30 DK072482)
- Narodowe Centrum Nauki (UMO‐2015/18/E/NZ3/00687)
- 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 › Angiogenesis and VEGF in Cancer
- Keywords
- hypoxia, HIF-1, HIF-2, microRNA, RNA-induced silencing complex, endothelial cells, miR-210-3p, miRNA-mRNA interactions, gene expression regulation
- MeSH terms
- Endothelial PAS Domain-Containing Protein 1, Hypoxia, Humans, RNA, Messenger, Cell Hypoxia, RNA-Induced Silencing Complex, MicroRNAs, Endothelial Cells, Basic Helix-Loop-Helix Proteins, Hypoxia-Inducible Factor 1, alpha Subunit
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