METTL3-mediated m6A modification of HDGF mRNA promotes gastric cancer progression and has prognostic significance

Gut. 2020 Jul;69(7):1193-1205. doi: 10.1136/gutjnl-2019-319639. Epub 2019 Oct 3.

Abstract

Objective: N6-methyladenosine (m6A) RNA methylation and its associated methyltransferase METTL3 are involved in tumour initiation and progression via the regulation of RNA function. This study explored the biological function and clinical significance of METTL3 in gastric cancer (GC).

Design: The prognostic value of METTL3 expression was evaluated using tissue microarray and immunohistochemical staining analyses in a human GC cohort. The biological role and mechanism of METTL3 in GC tumour growth and liver metastasis were determined in vitro and in vivo.

Results: The level of m6A RNA was significantly increased in GC, and METTL3 was the main regulator involved in the abundant m6A RNA modification. METTL3 expression was significantly elevated in GC tissues and associated with poor prognosis. Multivariate Cox regression analysis revealed that METTL3 expression was an independent prognostic factor and effective predictor in human patients with GC. Moreover, METTL3 overexpression promoted GC proliferation and liver metastasis in vitro and in vivo. Mechanistically, P300-mediated H3K27 acetylation activation in the promoter of METTL3 induced METTL3 transcription, which stimulated m6A modification of HDGF mRNA, and the m6A reader IGF2BP3 then directly recognised and bound to the m6A site on HDGF mRNA and enhanced HDGF mRNA stability. Secreted HDGF promoted tumour angiogenesis, while nuclear HDGF activated GLUT4 and ENO2 expression, followed by an increase in glycolysis in GC cells, which was correlated with subsequent tumour growth and liver metastasis.

Conclusions: Elevated METTL3 expression promotes tumour angiogenesis and glycolysis in GC, indicating that METTL3 expression is a potential prognostic biomarker and therapeutic target for human GC.

Keywords: METTL3; angiogenesis; gastric cancer; glycolysis; m6A.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aged
  • Animals
  • Disease Progression
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Intercellular Signaling Peptides and Proteins / metabolism*
  • Male
  • Methyltransferases / metabolism*
  • Mice, Nude
  • Middle Aged
  • Neoplasm Transplantation
  • Prognosis
  • RNA, Messenger / metabolism*
  • Stomach Neoplasms / diagnosis*
  • Stomach Neoplasms / metabolism
  • Stomach Neoplasms / pathology

Substances

  • Intercellular Signaling Peptides and Proteins
  • RNA, Messenger
  • hepatoma-derived growth factor
  • Methyltransferases
  • METTL3 protein, human