M6A-modified lncRNA FAM83H-AS1 promotes colorectal cancer progression through PTBP1

Cancer Lett. 2024 Aug 28:598:217085. doi: 10.1016/j.canlet.2024.217085. Epub 2024 Jul 2.

Abstract

LncRNA plays a crucial role in cancer progression and targeting, but it has been difficult to identify the critical lncRNAs involved in colorectal cancer (CRC) progression. We identified FAM83H-AS1 as a tumor-promoting associated lncRNA using 21 pairs of stage IV CRC tissues and adjacent normal tissues. In vitro and in vivo experiments revealed that knockdown of FAM83H-AS1 in CRC cells inhibited tumor proliferation and metastasis, and vice versa. M6A modification is critical for FAM83H-AS1 RNA stability through the writer METTL3 and the readers IGF2BP2/IGFBP3. PTBP1-an RNA binding protein-is responsible for the FAM83H-AS1 function in CRC. T4 (1770-2440 nt) and T5 (2440-2743 nt) on exon 4 of FAM83H-AS1 provide a platform for PTBP1 RRM2 interactions. Our results demonstrated that m6A modification dysregulated the FAM83H-AS1 oncogenic role by phosphorylated PTBP1 on its RNA splicing effect. In patient-derived xenograft models, ASO-FAM83H-AS1 significantly suppressed the growth of gastrointestinal (GI) tumors, not only CRC but also GC and ESCC. The combination of ASO-FAM83H-AS1 and oxaliplatin/cisplatin significantly suppressed tumor growth compared with treatment with either agent alone. Notably, there was pathological complete response in all these three GI cancers. Our findings suggest that FAM83H-AS1 targeted therapy would benefit patients primarily receiving platinum-based therapy in GI cancers.

Keywords: CRC; FAM83H-AS1; PTBP1; RNA splicing; m6A modification.

MeSH terms

  • Adenosine / analogs & derivatives
  • Adenosine / metabolism
  • Animals
  • Cell Line, Tumor
  • Cell Movement
  • Cell Proliferation*
  • Colorectal Neoplasms* / genetics
  • Colorectal Neoplasms* / metabolism
  • Colorectal Neoplasms* / pathology
  • Disease Progression*
  • Female
  • Gene Expression Regulation, Neoplastic*
  • Heterogeneous-Nuclear Ribonucleoproteins* / genetics
  • Heterogeneous-Nuclear Ribonucleoproteins* / metabolism
  • Humans
  • Male
  • Methyltransferases* / genetics
  • Methyltransferases* / metabolism
  • Mice
  • Mice, Inbred BALB C
  • Mice, Nude
  • Polypyrimidine Tract-Binding Protein* / genetics
  • Polypyrimidine Tract-Binding Protein* / metabolism
  • RNA Stability
  • RNA, Long Noncoding* / genetics
  • RNA-Binding Proteins
  • Ribonucleoside Diphosphate Reductase
  • Xenograft Model Antitumor Assays

Substances

  • Polypyrimidine Tract-Binding Protein
  • RNA, Long Noncoding
  • PTBP1 protein, human
  • Heterogeneous-Nuclear Ribonucleoproteins
  • Methyltransferases
  • METTL3 protein, human
  • N-methyladenosine
  • Adenosine
  • IGF2BP2 protein, human
  • ribonucleotide reductase M2
  • Ribonucleoside Diphosphate Reductase
  • RNA-Binding Proteins