A Circle RNA Regulatory Axis Promotes Lung Squamous Metastasis via CDR1-Mediated Regulation of Golgi Trafficking

Cancer Res. 2020 Nov 15;80(22):4972-4985. doi: 10.1158/0008-5472.CAN-20-1162. Epub 2020 Sep 25.

Abstract

Lung squamous carcinoma (LUSC) is a highly metastatic disease with a poor prognosis. Using an integrated screening approach, we found that miR-671-5p reduces LUSC metastasis by inhibiting a circular RNA (circRNA), CDR1as. Although the putative function of circRNA is through miRNA sponging, we found that miR-671-5p more potently silenced an axis of CDR1as and its antisense transcript, cerebellar degeneration related protein 1 (CDR1). Silencing of CDR1as or CDR1 significantly inhibited LUSC metastases and CDR1 was sufficient to promote migration and metastases. CDR1, which directly interacted with adaptor protein 1 (AP1) complex subunits and coatomer protein I (COPI) proteins, no longer promoted migration upon blockade of Golgi trafficking. Therapeutic inhibition of the CDR1as/CDR1 axis with miR-671-5p mimics reduced metastasis in vivo. This report demonstrates a novel role for CDR1 in promoting metastasis and Golgi trafficking. These findings reveal an miRNA/circRNA axis that regulates LUSC metastases through a previously unstudied protein, CDR1. SIGNIFICANCE: This study shows that circRNA, CDR1as, promotes lung squamous migration, metastasis, and Golgi trafficking through its complimentary transcript, CDR1.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Protein Complex 1 / metabolism
  • Animals
  • Autoantigens / genetics
  • Autoantigens / metabolism*
  • Carcinoma, Squamous Cell / metabolism
  • Carcinoma, Squamous Cell / mortality
  • Carcinoma, Squamous Cell / secondary*
  • Cell Line, Tumor
  • Cell Movement / physiology
  • Coat Protein Complex I / metabolism
  • Endoplasmic Reticulum / metabolism
  • Female
  • Golgi Apparatus / metabolism*
  • Humans
  • Hyaluronic Acid / therapeutic use
  • Lung Neoplasms / metabolism
  • Lung Neoplasms / mortality
  • Lung Neoplasms / pathology*
  • Mice
  • Mice, Nude
  • MicroRNAs / metabolism
  • Nanoparticles / therapeutic use
  • Neoplasm Metastasis
  • Neoplasm Proteins / genetics
  • Neoplasm Proteins / metabolism
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism*
  • RNA, Circular / antagonists & inhibitors*
  • RNA, Long Noncoding / metabolism*

Substances

  • Adaptor Protein Complex 1
  • Autoantigens
  • CDR1 protein, human
  • Coat Protein Complex I
  • MIRN671 microRNA, human
  • MicroRNAs
  • Neoplasm Proteins
  • Nerve Tissue Proteins
  • RNA, Circular
  • RNA, Long Noncoding
  • long non-coding RNA CDR1AS, human
  • Hyaluronic Acid