LncRNA PVT1 promotes gemcitabine resistance of pancreatic cancer via activating Wnt/β-catenin and autophagy pathway through modulating the miR-619-5p/Pygo2 and miR-619-5p/ATG14 axes
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Background: Pancreatic cancer is one of the most lethal malignancies and has an extremely poor diagnosis and prognosis. The development of resistance to gemcitabine is still a major challenge. The long noncoding RNA PVT1 was reported to be involved in carcinogenesis and chemoresistance; however, the mechanism by which PVT1 regulates the sensitivity of pancreatic cancer to gemcitabine remains poorly understood. Methods: The viability of pancreatic cancer cells was assessed by MTT assay in vitro and xenograft tumor formation assay in vivo. The expression levels of PVT1 and miR-619-5p were detected by quantitative real-time polymerase chain reaction (qRT-PCR). Western blotting analysis and qRT-PCR were performed to assess the protein and mRNA levels of Pygo2 and ATG14, respectively. Autophagy was explored via autophagic flux detection under confocal microscopy and autophagic vacuole investigation under transmission electron microscopy (TEM). The functional role and mechanism of PVT1 were further investigated by gain- and loss-of-function assays in vitro. Results: In the present study, we demonstrated that PVT1 was up-regulated in gemcitabine-resistant pancreatic cancer cell lines. Gain- and loss-of-function assays revealed that PVT1 impaired sensitivity to gemcitabine in vitro and in vivo. We further found that PVT1 up-regulated the expression of both Pygo2 and ATG14 and thus regulated Wnt/β-catenin signaling and autophagic activity to overcome gemcitabine resistance through sponging miR-619-5p. Moreover, we discovered three TCF/LEF binding elements (TBEs) in the promoter region of PVT1, and activation of Wnt/β-catenin signaling mediated by the up-regulation of Pygo2 increased PVT1 expression by direct binding to the TBE region. Furthermore, PVT1 was discovered to interact with ATG14, thus promoting assembly of the autophagy specific complex I (PtdIns3K-C1) and ATG14-dependent class III PtdIns3K activity. Conclusions: These data indicate that PVT1 plays a critical role in the sensitivity of pancreatic cancer to gemcitabine and highlight its potential as a valuable target for pancreatic cancer therapy.
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The PI3K/AKT pathway and increased activity of the Wnt/β-catenin pathway contribute to the mechanisms by which PDAC cells develop drug resistance.
“the PI3K/AKT pathway and increased activity of the Wnt/β‐catenin pathway contribute to the mechanisms by which PDAC cells develop drug resistance [49, 50]”
From Pyrvinium Pamoate Alone and With Gemcitabine Exhibits Anti‐Pancreatic Cancer Activity in <scp>2D</scp> and <scp>3D</scp> Cell Culture Models (2024) · cites this paper as [50]
The Discussion reports that activated Wnt/β-catenin signaling is associated with PVT1-induced gemcitabine resistance in pancreatic cancer. The Results also describe Wnt/β-catenin signaling as a mechanism of chemoresistance. Our copy does not support the PI3K/AKT part: its PIK3C3 findings concern an autophagy-related complex, not PI3K/AKT signaling. (LLM, conf=0.88)
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- Authors
- Zhou, C., Yi, C., Yi, Y., Qin, W., Yan, Y., Dong, X., Zhang, X., Huang, Y., Zhang, R., Wei, J., Ali, D. W., Michalak, M., Chen, X.-Z., & Tang, J.
- Affiliations
- Hubei University of Technology (CN)
- Nanjing Second Hospital (CN)
- University of Alberta (CA)
- Corresponding author
- Tang, Jingfeng
- ORCID
- Venue
- Molecular Cancer
- Published
- 2020-07-29
- Volume
- 19
- Issue
- 1
- Pages
- 118-118
- ISSN
- 1476-4598 (ISSN-L)
- PMC
- PMC7389684
- OpenAlex
- W3045960922
- Cited by
- 382
- References
- 59
- Citations by year
- 2026: 18 · 2025: 42 · 2024: 88 · 2023: 79 · 2022: 92 · 2021: 53 · 2020: 10
- FWCI
- 20.86
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Molecular Cancer (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Natural Science Foundation of China (31701228, 31871420, 31871176)
- Wuhan Science and Technology Project (2019020701011475)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer-related molecular mechanisms research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
- Health Sciences › Medicine › Oncology › Pancreatic and Hepatic Oncology Research
- Keywords
- long non-coding RNA, gemcitabine resistance, pancreatic cancer, Pygo2, ATG14, Wnt/β-catenin signaling, autophagy, chemoresistance
- MeSH terms
- Autophagy-Related Proteins, Gemcitabine, Animals, Autophagy, Binding Sites, Cell Survival, Deoxycytidine, Disease Models, Animal, Dose-Response Relationship, Drug, Humans, Pancreatic Neoplasms, Protein Binding, Gene Expression Regulation, Neoplastic, Drug Resistance, Neoplasm, Xenograft Model Antitumor Assays, Adaptor Proteins, Vesicular Transport, RNA Interference, MicroRNAs, Cell Line, Tumor, Intracellular Signaling Peptides and Proteins, Cell Proliferation, Mice, Wnt Signaling Pathway, RNA, Long Noncoding
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