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Long non-coding RNA SNHG4 enhances RNF14 mRNA stability to promote the progression of colorectal cancer by recruiting TAF15 protein

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Abstract

SNHG4 is a lncRNA that was previously reported to promote colorectal cancer (CRC) progression via molecular sponge mechanism. Bioinformatic analysis suggested SNHG4 might scaffold TAF15 protein-RNF14 mRNA interaction. We aimed to investigate the mechanisms of potential SNHG4/TAF15/RNF14 axis in promoting CRC malignant phenotypes. Protein-RNA interaction was determined using RNA immunoprecipitation, pull-down and fluorescence in situ hybridization (FISH) combined immunofluorescence assays. Cell apoptosis rates were quantified using flow cytometry. CCK-8 and colony formation were adopted to determine cell proliferation. Wound healing and transwell assays were employed to assess cell migration and invasion, respectively. Xenograft tumor model was applied to assess the effects of SNHG4 on CRC tumorigenesis in vivo. SNHG4, TAF15 and RNF14 were up-regulated in CRC tissues. SNHG4 overexpression promoted cell proliferation, migration, invasion, and Wnt/β-catenin pathway activation in vitro, as well as tumor growth in vivo. The inhibited malignant phenotypes caused by SNHG4 knockdown were impeded by TAF15 or RNF14 overexpression. Mechanistically, SNHG4 recruited TAF15 protein and thus promoted the interaction between TAF15 protein and RNF14 mRNA, leading to the increased RNF14 mRNA stability. This in turn facilitated the Wnt/β-catenin signal transduction. SNHG4 enhanced RNF14 mRNA stability and activated the Wnt/β-catenin pathway to promote the progression of colorectal cancer by recruiting TAF15 protein.

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Data availability

All data generated or analyzed during this study are included in this article. The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Abbreviations

CRC:

Colorectal cancer

FISH:

Fluorescence in situ hybridization

lncRNAs:

Long non-coding RNAs

EMT:

Epithelial-mesenchymal transition

SNHG4:

Small nucleolar RNA host gene 4

TAF15:

TATA-box binding protein associated factor 15

TCF/LEF:

T-cell factor/lymphoid enhancer-binding factor

RNF:

Ring finger

DMEM:

Dulbecco’s Modified Eagle’s Medium

RL:

Right lower

RU:

Right upper

References

  1. Chen W et al (2016) Cancer statistics in China, 2015. CA Cancer J Clin 66:115–132

    Article  PubMed  Google Scholar 

  2. Cao W, Chen HD, Yu YW, Li N, Chen WQ (2021) Changing profiles of cancer burden worldwide and in China: a secondary analysis of the global cancer statistics 2020. Chin Med J (Engl) 134:783–791

    Article  PubMed  Google Scholar 

  3. Vu T, Datta PK (2017) Regulation of EMT in colorectal cancer: a culprit in metastasis. Cancers (Basel) 9:171

    Article  PubMed  Google Scholar 

  4. Pavlič A, Urh K, Štajer K, Boštjančič E, Zidar N (2021) Epithelial-Mesenchymal transition in colorectal carcinoma: comparison between primary tumor, lymph node and liver metastases. Front Oncol 11:1504

    Article  Google Scholar 

  5. Sugai T et al (2018) Analysis of the expression of cancer-associated fibroblast- and EMT-related proteins in submucosal invasive colorectal cancer. J Cancer 9:2702–2712

    Article  PubMed  PubMed Central  Google Scholar 

  6. Zhang Z et al (2020) Genomics and prognosis analysis of epithelial-mesenchymal transition in colorectal cancer patients. BMC Cancer 20:1–2

    Article  Google Scholar 

  7. Yang Y et al (2021) Comprehensive analysis of EMT-related genes and lncRNAs in the prognosis, immunity, and drug treatment of colorectal cancer. J Transl Med 19:1–21

    Article  CAS  Google Scholar 

  8. Mo S et al (2021) Comprehensive transcriptomic analysis reveals prognostic value of an EMT-related gene signature in colorectal cancer. Front cell Dev Biol 9:1566

    Article  Google Scholar 

  9. Iyer MK et al (2015) The landscape of long noncoding RNAs in the human transcriptome. Nat Genet 47:199–208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Fang Y, Fullwood MJ (2016) Roles, functions, and mechanisms of long non-CODING RNAs in cancer. Genomics Proteomics Bioinform 14:42–54

    Article  Google Scholar 

  11. Yao RW, Wang Y, Chen LL (2019) Cellular functions of long noncoding RNAs. Nat Cell Biol 21:542–551

    Article  CAS  PubMed  Google Scholar 

  12. Peng WX, Koirala P, Mo YY (2017) LncRNA-mediated regulation of cell signaling in cancer. Oncogene 36:5661–5667

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Chi Y, Wang D, Wang J, Yu W, Yang J (2019) Long non-coding RNA in the Pathogenesis of Cancers. Cells 8:1015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Goodall GJ, Wickramasinghe VO (2021) RNA in cancer. Nat Rev Cancer 21:22–36

    Article  CAS  PubMed  Google Scholar 

  15. Jiao Y et al (2020) The prognostic value of lncRNA SNHG4 and its potential mechanism in liver cancer. Biosci Rep. https://doi.org/10.1042/BSR20190729

  16. Cheng XB et al (2021) Knockdown of lncRNA SNHG4 suppresses gastric cancer cell proliferation and metastasis by targeting miR-204-5p. Neoplasma 68:546–556

    Article  CAS  PubMed  Google Scholar 

  17. Wang S, Zhu W, Qiu J, Chen F (2021) lncRNA SNHG4 promotes cell proliferation, migration, invasion and the epithelial-mesenchymal transition process via sponging miR-204–5p in gastric cancer. Mol Med Rep 23:1–11

    Google Scholar 

  18. Zhou Z et al (2021) lncRNA SNHG4 modulates colorectal cancer cell cycle and cell proliferation through regulating miR-590–3p/CDK1 axis. Aging (Albany. NY). 13:9838–9858

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Wang X et al (2021) LncRNA SNHG14 promotes cell proliferation and invasion in colorectal cancer through modulating miR-519b-3p/DDX5 axis. J Cancer 12:4958–4970

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Kc W, Hy C (2011) Molecular mechanisms of long noncoding RNAs. Mol Cell 43:904–914

    Article  Google Scholar 

  21. Andric V et al (2021) A scaffold lncRNA shapes the mitosis to meiosis switch. Nat Commun 12:1–2

    Article  Google Scholar 

  22. Bertolotti A, Lutz Y, Heard DJ, Chambon P, Tora L (1996) hTAF(II)68, a novel RNA/ssDNA-binding protein with homology to the pro-oncoproteins TLS/FUS and EWS is associated with both TFIID and RNA polymerase II. EMBO J 15:5022

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Ruan X et al (2020) lncRNA LINC00665 Stabilized by TAF15 Impeded the Malignant Biological Behaviors of Glioma Cells via STAU1-Mediated mRNA Degradation. Mol Ther Nucleic Acids 20:823–840

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Ibrahim F et al (2013) Identification of in vivo, conserved, TAF15 RNA binding sites reveals the impact of TAF15 on the neuronal transcriptome. Cell Rep 3:301–308

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Ren P, Xing L, Hong X, Chang L, Zhang H (2020) LncRNA PITPNA-AS1 boosts the proliferation and migration of lung squamous cell carcinoma cells by recruiting TAF15 to stabilize HMGB3 mRNA. Cancer Med 9:7706–7716

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Pan Li, Li Yi, Jin Li, Li J, Aixiang Xu (2020) TRPM2-AS promotes cancer cell proliferation through control of TAF15. Int J Biochem Cell Biol 120:105683

    Article  CAS  PubMed  Google Scholar 

  27. Lin Y et al (2020) RNAInter in 2020: RNA interactome repository with increased coverage and annotation. Nucleic Acids Res 48:D189–D197

    Article  CAS  PubMed  Google Scholar 

  28. Schatoff EM, Leach BI, Dow LE (2017) Wnt signaling and colorectal cancer. Curr Colorectal Cancer Rep 13:101

    Article  PubMed  PubMed Central  Google Scholar 

  29. Cheng X, Xu X, Chen D, Zhao F, Wang W (2019) Therapeutic potential of targeting the Wnt/β-catenin signaling pathway in colorectal cancer. Biomed Pharmacother 110:473–481

    Article  CAS  PubMed  Google Scholar 

  30. Sebio A, Kahn M, Lenz HJ (2014) The potential of targeting Wnt/β-catenin in colon cancer. Expert Opin Ther Targets 18:611–615

    Article  CAS  PubMed  Google Scholar 

  31. Zhao H et al (2022) Wnt signaling in colorectal cancer: pathogenic role and therapeutic target. Mol Cancer 21:1–34

    Article  Google Scholar 

  32. Hao HX et al (2012) ZNRF3 promotes Wnt receptor turnover in an R-spondin-sensitive manner. Nature 485:195–202

    Article  CAS  PubMed  Google Scholar 

  33. Thomas JJ et al (2016) RNF4-dependent oncogene activation by protein stabilization. Cell Rep 16:3388–3400

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Wu B et al (2013) Ring finger protein 14 is a new regulator of TCF/β-catenin-mediated transcription and colon cancer cell survival. EMBO Rep 14:347–355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Chandrashekar DS et al (2017) UALCAN: a portal for facilitating tumor subgroup gene expression and survival analyses. Neoplasia 19:649–658

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Tang Z et al (2017) GEPIA: a web server for cancer and normal gene expression profiling and interactive analyses. Nucleic Acids Res 45:W98–W102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Tetsu O, McCormick F (1999) Beta-catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 398:422–426

    Article  CAS  PubMed  Google Scholar 

  38. He TC et al (1998) Identification of c-MYC as a target of the APC pathway. Science 281:1509–1512

    Article  CAS  PubMed  Google Scholar 

  39. Wu B, Crampton SP, Hughes CCW (2007) Wnt signaling induces MMP expression and regulates T cell transmigration. Immunity 26:227

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Jamora C, DasGupta R, Kocieniewski P, Fuchs E (2003) Links between signal transduction, transcription and adhesion in epithelial bud development. Nature 422:317–322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Loh C-Y et al (2019) The E-Cadherin and N-Cadherin Switch in epithelial-to-mesenchymal transition: signaling, therapeutic implications, and challenges. Cells 8:1118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

Not applicable.

Funding

This work was supported by Guangxi Research Foundation for Science &Technology Base and Talent Special (no. AD20238005).

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Authors

Contributions

LL: Conceptualization; Writing-original draft; Methodology; Formal analysis; Supervision; Validation; Visualization; BH: Data curation; Resources; LY: Investigation; Software; LZ: Funding acquisition; Project administration; Writing-review & editing.

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Correspondence to Lv Lv.

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The authors declare that they have no conflict of interest.

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The approval for patient recruitment, specimen collection and tissue processing has been acquired from the clinical research ethics committee in Affiliated Hospital of Guilin Medical University. The animal research ethics committee of Affiliated Hospital of Guilin Medical University approved all the animal experiment procedures.

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Lv, L., Huang, B., Yi, L. et al. Long non-coding RNA SNHG4 enhances RNF14 mRNA stability to promote the progression of colorectal cancer by recruiting TAF15 protein. Apoptosis 28, 414–431 (2023). https://doi.org/10.1007/s10495-022-01781-6

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  • DOI: https://doi.org/10.1007/s10495-022-01781-6

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