Oncogenic RAS-induced downregulation of ATG12 is required for survival of malignant intestinal epithelial cells

Autophagy. 2018;14(1):134-151. doi: 10.1080/15548627.2017.1370171. Epub 2017 Dec 21.

Abstract

Activating mutations of RAS GTPase contribute to the progression of many cancers, including colorectal carcinoma. So far, attempts to develop treatments of mutant RAS-carrying cancers have been unsuccessful due to insufficient understanding of the salient mechanisms of RAS signaling. We found that RAS downregulates the protein ATG12 in colon cancer cells. ATG12 is a mediator of autophagy, a process of degradation and reutilization of cellular components. In addition, ATG12 can kill cells via autophagy-independent mechanisms. We established that RAS reduces ATG12 levels in cancer cells by accelerating its proteasomal degradation. We further observed that RAS-dependent ATG12 loss in these cells is mediated by protein kinases MAP2K/MEK and MAPK1/ERK2-MAPK3/ERK1, known effectors of RAS. We also demonstrated that the reversal of the effect of RAS on ATG12 achieved by the expression of exogenous ATG12 in cancer cells triggers both apoptotic and nonapoptotic signals and efficiently kills the cells. ATG12 is known to promote autophagy by forming covalent complexes with other autophagy mediators, such as ATG5. We found that the ability of ATG12 to kill oncogenic RAS-carrying malignant cells does not require covalent binding of ATG12 to other proteins. In summary, we have identified a novel mechanism by which oncogenic RAS promotes survival of malignant intestinal epithelial cells. This mechanism is driven by RAS-dependent loss of ATG12 in these cells.

Keywords: ATG12; RAS; apoptosis; autophagy; colorectal cancer.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis
  • Autophagy*
  • Autophagy-Related Protein 12 / metabolism*
  • Autophagy-Related Protein 5 / metabolism
  • Cell Line, Tumor
  • Cell Survival
  • Colorectal Neoplasms / metabolism*
  • Colorectal Neoplasms / pathology
  • Down-Regulation
  • Humans
  • Intestinal Mucosa / metabolism*
  • Intestinal Mucosa / pathology
  • MAP Kinase Kinase Kinases / metabolism
  • Mutation
  • Protein Binding
  • Proto-Oncogene Proteins p21(ras) / genetics
  • Proto-Oncogene Proteins p21(ras) / metabolism*
  • Signal Transduction

Substances

  • ATG12 protein, human
  • ATG5 protein, human
  • Autophagy-Related Protein 12
  • Autophagy-Related Protein 5
  • KRAS protein, human
  • MAP Kinase Kinase Kinases
  • Proto-Oncogene Proteins p21(ras)

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