LncRNA NEAT1 knockdown attenuates autophagy to elevate 5-FU sensitivity in colorectal cancer via targeting miR-34a

Cancer Med. 2020 Feb;9(3):1079-1091. doi: 10.1002/cam4.2746. Epub 2019 Dec 5.

Abstract

Backgrounds: Colorectal carcinoma (CRC) is a common malignant tumor. Increasing evidences indicated that CRC showed a resistance to 5-fluorouracil (5-FU) and further resulted in a poor prognosis. In this study, we aim to investigate the effect of long noncoding RNA nuclear paraspeckle assembly transcript 1 (LncRNA NEAT1) on cell viability, sensitivity to 5-FU, and autophagy of CRC cell lines.

Methods: MTT (3-(4,5-dimethyl-2-thiazolyl)-2,5-diphenyl-2-Htetrazolium bromide) was used to detect cell viability, immunofluorescent staining was used to detect autophagy puncta, and luciferase reporter system was used to determine binding ability between miR-34a and NEAT1 or putative targets. Additionally, indicated mRNAs and protein expressions were determined by qRT-PCR or western blotting, respectively.

Results: We found that NEAT1 expression was increased in CRC tissues and cells, which showed a negative correlation with miR-34a expression. In addition, NEAT1 knockdown noticeably inhibited the proliferation of CRC cells and enhanced 5-FU sensitivity. It revealed that NEAT1 knockdown suppressed the LC3 puncta and the expressions of Beclin-1, ULK1, and ratio of LC3II/I. Overexpression of miR-34a showed similar trends with NEAT1 knockdown. miR-34a was validated to target the putative binding sites in 3'-UTR of HMGB1, ATG9A, and ATG4B, which are involved in the activation of autophagy. Inhibition of miR-34a or overexpression of HMGB1 could effectively reverse elevated 5-FU sensitivity upon NEAT1 knockdown. In addition, 3-MA reversed NEAT1 overexpression-induced resistance in HT29 cells.

Conclusion: These findings indicate that LncRNA NEAT1 could target miR-34a and promote autophagy to facilitate 5-FU chemoresistance in CRC.

Keywords: HMGB1; LncRNA NEAT1; autophagy; colorectal carcinoma; miR-34a.

Publication types

  • Observational Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • 3' Untranslated Regions / genetics
  • Apoptosis / genetics
  • Autophagy / drug effects
  • Autophagy / genetics*
  • Autophagy-Related Proteins / genetics
  • Cell Proliferation / drug effects
  • Cell Proliferation / genetics
  • Cell Survival / drug effects
  • Cell Survival / genetics
  • Colorectal Neoplasms / drug therapy*
  • Colorectal Neoplasms / genetics
  • Colorectal Neoplasms / pathology
  • Colorectal Neoplasms / surgery
  • Cysteine Endopeptidases / genetics
  • Drug Resistance, Neoplasm / genetics*
  • Fluorouracil / pharmacology*
  • Fluorouracil / therapeutic use
  • Gene Expression Regulation, Neoplastic
  • Gene Knockdown Techniques
  • HMGB1 Protein / genetics
  • HT29 Cells
  • Humans
  • Membrane Proteins / genetics
  • MicroRNAs / metabolism*
  • RNA, Long Noncoding / genetics
  • RNA, Long Noncoding / metabolism*
  • Up-Regulation
  • Vesicular Transport Proteins / genetics

Substances

  • 3' Untranslated Regions
  • ATG9A protein, human
  • Autophagy-Related Proteins
  • HMGB1 Protein
  • HMGB1 protein, human
  • MIRN34 microRNA, human
  • Membrane Proteins
  • MicroRNAs
  • NEAT1 long non-coding RNA, human
  • RNA, Long Noncoding
  • Vesicular Transport Proteins
  • ATG4B protein, human
  • Cysteine Endopeptidases
  • Fluorouracil