mTORC1 Inactivation Promotes Colitis-Induced Colorectal Cancer but Protects from APC Loss-Dependent Tumorigenesis

Cell Metab. 2018 Jan 9;27(1):118-135.e8. doi: 10.1016/j.cmet.2017.11.006. Epub 2017 Dec 21.

Abstract

Dietary habits that can induce inflammatory bowel disease (IBD) are major colorectal cancer (CRC) risk factors, but mechanisms linking nutrients, IBD, and CRC are unknown. Using human data and mouse models, we show that mTORC1 inactivation-induced chromosomal instability impairs intestinal crypt proliferation and regeneration, CDK4/6 dependently. This triggers interleukin (IL)-6-associated reparative inflammation, inducing crypt hyper-proliferation, wound healing, and CRC. Blocking IL-6 signaling or reactivating mTORC1 reduces inflammation-induced CRC, so mTORC1 activation suppresses tumorigenesis in IBD. Conversely, mTORC1 inactivation is beneficial in APC loss-dependent CRC. Thus, IL-6 blockers or protein-rich-diet-linked mTORC1 activation may prevent IBD-associated CRC. However, abolishing mTORC1 can mitigate CRC in predisposed patients with APC mutations. Our work reveals mTORC1 oncogenic and tumor-suppressive roles in intestinal epithelium and avenues to optimized and personalized therapeutic regimens for CRC.

Keywords: APC; DNA damage; IL-6; MCRS1; chromosomal instability; colorectal cancer; dNTPs; inflammatory bowel disease; mTORC1; regeneration.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenoma / pathology
  • Adenomatous Polyposis Coli Protein / deficiency*
  • Adenomatous Polyposis Coli Protein / metabolism
  • Carcinogenesis / metabolism
  • Carcinogenesis / pathology*
  • Cell Proliferation
  • Chromosomal Instability
  • Colitis / complications*
  • Colorectal Neoplasms / etiology*
  • DNA Damage
  • Female
  • HCT116 Cells
  • Homeostasis
  • Humans
  • Inflammation / pathology
  • Inflammatory Bowel Diseases / metabolism
  • Inflammatory Bowel Diseases / pathology
  • Interleukin-6 / metabolism
  • Intestines / pathology
  • Male
  • Mechanistic Target of Rapamycin Complex 1 / metabolism*
  • Nuclear Proteins / metabolism
  • RNA-Binding Proteins / metabolism
  • Regeneration
  • Signal Transduction
  • Tumor Suppressor Protein p53 / metabolism

Substances

  • Adenomatous Polyposis Coli Protein
  • Interleukin-6
  • MCRS1 protein, human
  • Mcrs1 protein, mouse
  • Nuclear Proteins
  • RNA-Binding Proteins
  • Tumor Suppressor Protein p53
  • Mechanistic Target of Rapamycin Complex 1