LncRNA PVT1 Facilitates the Growth and Metastasis of Colorectal Cancer by Sponging with MiR-3619-5p to Regulate TRIM29 Expression

Overview

Journal Cancer Rep (Hoboken)

Specialty Oncology

Date 2024 Jun 5

PMID 38837682

Authors

Zhenni Sun

Xutong Li

Yanyan Shi

Yasai Yao

Affiliations

Soon will be listed here.

Abstract

Background: Colorectal cancer (CRC) is the second most common cause of cancer-related death worldwide. Long noncoding RNA (lncRNA) is involved in many malignant tumors. This study aimed to clarify the role of the lncRNA plasmacytoma variant translocation 1 (PVT1) in CRC growth and metastasis.

Methods: Differentially expressed lncRNAs in CRC were analyzed using the Cancer Genome Atlas. Gene expression profiling interactive analysis and a comprehensive resource for lncRNAs from cancer arrays databases were used to analyze lncRNA PVT1 expression and CRC prognosis, respectively. Cell counting kit-8, wound healing, colony formation, Transwell, and immunofluorescence assays were used to evaluate CRC cell proliferation, migration, invasion, and epithelial-mesenchymal transition (EMT), respectively. Tumor growth and metastasis models were used to explore the PVT1 effect on the growth and metastasis of CRC in vivo.

Results: PVT1 was highly expressed in CRC, associated with a poor prognosis of CRC, and showed good diagnostic value. Transfection of sh-PVT1 or pcDNA3.1-PVT1 reduced or increased the proliferation, wound healing rate, colony formation, invasion, and EMT of CRC cells. PVT1 and miR-3619-5p were co-expressed in CRC cytoplasm, and PVT1 acted as a competitive endogenous RNA (ceRNA) by sponging miR-3619-5p to up-regulate tripartite motif containing 29 (TRIM29) expression. MiR-3619-5p overexpression and TRIM29 knockdown reduced proliferation, wound healing rate, invasion, and EMT of CRC cells. However, simultaneous PVT1 and miR-3619-5p overexpression or knockdown of miR-3619-5p and TRIM29 knockdown rescued the malignant phenotype of CRC cells.

Conclusions: We first clarified the ceRNA mechanism of PVT1 in CRC, which induced growth and metastasis by sponging with miR-3619-5p to regulate TRIM29.

Citing Articles

Long non‑coding RNA ABHD11‑AS1 inhibits colorectal cancer progression through interacting with EGFR to suppress the EGFR/ERK signaling pathway.

Tan S, Li S, Xia L, Jiang X, Ren Z, Peng Q Int J Oncol. 2025; 66(3).

PMID: 39950321 PMC: 11844336. DOI: 10.3892/ijo.2025.5726.

Deciphering the role of LOC124905135-related non-coding RNA cluster in human cancers: A comprehensive review.

Eftekhari Kenzerki M, Mohajeri Khorasani A, Zare I, Amirmahani F, Ghasemi Y, Hamblin M Heliyon. 2024; 10(22):e39931.

PMID: 39641053 PMC: 11617737. DOI: 10.1016/j.heliyon.2024.e39931.

References

Ren X, Cao D, Yang L, Li X, Zhang W, Xiao Y . High Expression of long non-coding RNA PVT1 predicts metastasis in Han and Uygur Patients with Gastric Cancer in Xinjiang, China. Sci Rep. 2019; 9(1):548. PMC: 6345741. DOI: 10.1038/s41598-018-36985-x. View

Han J, Zhao Z, Zhang N, Yang Y, Ma L, Feng L . Transcriptional dysregulation of TRIM29 promotes colorectal cancer carcinogenesis via pyruvate kinase-mediated glucose metabolism. Aging (Albany NY). 2021; 13(4):5034-5054. PMC: 7950264. DOI: 10.18632/aging.202414. View

Yang X, Cheng T, He Q, Lei Z, Chi J, Tang Z . LINC01133 as ceRNA inhibits gastric cancer progression by sponging miR-106a-3p to regulate APC expression and the Wnt/β-catenin pathway. Mol Cancer. 2018; 17(1):126. PMC: 6106894. DOI: 10.1186/s12943-018-0874-1. View

Fidler I . The pathogenesis of cancer metastasis: the 'seed and soil' hypothesis revisited. Nat Rev Cancer. 2003; 3(6):453-8. DOI: 10.1038/nrc1098. View

Zheng Z, Li Z, Zhou G, Lin L, Zhang L, Lv J . Long Noncoding RNA FAM225A Promotes Nasopharyngeal Carcinoma Tumorigenesis and Metastasis by Acting as ceRNA to Sponge miR-590-3p/miR-1275 and Upregulate ITGB3. Cancer Res. 2019; 79(18):4612-4626. DOI: 10.1158/0008-5472.CAN-19-0799. View

Sun Z, Yang S, Zhou Q, Wang G, Song J, Li Z . Emerging role of exosome-derived long non-coding RNAs in tumor microenvironment. Mol Cancer. 2018; 17(1):82. PMC: 5909226. DOI: 10.1186/s12943-018-0831-z. View

Li J, Liu S, Zhou H, Qu L, Yang J . starBase v2.0: decoding miRNA-ceRNA, miRNA-ncRNA and protein-RNA interaction networks from large-scale CLIP-Seq data. Nucleic Acids Res. 2013; 42(Database issue):D92-7. PMC: 3964941. DOI: 10.1093/nar/gkt1248. View

Christofi T, Baritaki S, Falzone L, Libra M, Zaravinos A . Current Perspectives in Cancer Immunotherapy. Cancers (Basel). 2019; 11(10). PMC: 6826426. DOI: 10.3390/cancers11101472. View

Wu H, Wei M, Jiang X, Tan J, Xu W, Fan X . lncRNA PVT1 Promotes Tumorigenesis of Colorectal Cancer by Stabilizing miR-16-5p and Interacting with the VEGFA/VEGFR1/AKT Axis. Mol Ther Nucleic Acids. 2020; 20:438-450. PMC: 7139143. DOI: 10.1016/j.omtn.2020.03.006. View

10.

Sun Q, Hao Q, Prasanth K . Nuclear Long Noncoding RNAs: Key Regulators of Gene Expression. Trends Genet. 2017; 34(2):142-157. PMC: 6002860. DOI: 10.1016/j.tig.2017.11.005. View

11.

Shigeyasu K, Toden S, Ozawa T, Matsuyama T, Nagasaka T, Ishikawa T . The PVT1 lncRNA is a novel epigenetic enhancer of MYC, and a promising risk-stratification biomarker in colorectal cancer. Mol Cancer. 2020; 19(1):155. PMC: 7643275. DOI: 10.1186/s12943-020-01277-4. View

12.

Wang H, Huo X, Yang X, He J, Cheng L, Wang N . STAT3-mediated upregulation of lncRNA HOXD-AS1 as a ceRNA facilitates liver cancer metastasis by regulating SOX4. Mol Cancer. 2017; 16(1):136. PMC: 5558651. DOI: 10.1186/s12943-017-0680-1. View

13.

Gharib E, Anaraki F, Baghdar K, Ghavidel P, Sadeghi H, Nasrabadi P . Investigating the diagnostic performance of HOTTIP, PVT1, and UCA1 long noncoding RNAs as a predictive panel for the screening of colorectal cancer patients with lymph node metastasis. J Cell Biochem. 2019; 120(9):14780-14790. DOI: 10.1002/jcb.28739. View

14.

Tang Z, Li C, Kang B, Gao G, Li C, Zhang Z . GEPIA: a web server for cancer and normal gene expression profiling and interactive analyses. Nucleic Acids Res. 2017; 45(W1):W98-W102. PMC: 5570223. DOI: 10.1093/nar/gkx247. View

15.

Xu W, Xu B, Yao Y, Yu X, Cao H, Zhang J . RNA interference against TRIM29 inhibits migration and invasion of colorectal cancer cells. Oncol Rep. 2016; 36(3):1411-8. DOI: 10.3892/or.2016.4941. View

16.

Tay Y, Rinn J, Pandolfi P . The multilayered complexity of ceRNA crosstalk and competition. Nature. 2014; 505(7483):344-52. PMC: 4113481. DOI: 10.1038/nature12986. View

17.

Aiello N, Kang Y . Context-dependent EMT programs in cancer metastasis. J Exp Med. 2019; 216(5):1016-1026. PMC: 6504222. DOI: 10.1084/jem.20181827. View

18.

Liu X, Bi L, Wang Q, Wen M, Li C, Ren Y . miR-1204 targets VDR to promotes epithelial-mesenchymal transition and metastasis in breast cancer. Oncogene. 2018; 37(25):3426-3439. DOI: 10.1038/s41388-018-0215-2. View

19.

Pastushenko I, Blanpain C . EMT Transition States during Tumor Progression and Metastasis. Trends Cell Biol. 2018; 29(3):212-226. DOI: 10.1016/j.tcb.2018.12.001. View

20.

Tragante V, Moore J, Asselbergs F . The ENCODE project and perspectives on pathways. Genet Epidemiol. 2014; 38(4):275-80. DOI: 10.1002/gepi.21802. View