Glycogen accumulation and phase separation drives liver tumor initiation

Cell. 2021 Oct 28;184(22):5559-5576.e19. doi: 10.1016/j.cell.2021.10.001. Epub 2021 Oct 21.

Abstract

Glucose consumption is generally increased in tumor cells to support tumor growth. Interestingly, we report that glycogen accumulation is a key initiating oncogenic event during liver malignant transformation. We found that glucose-6-phosphatase (G6PC) catalyzing the last step of glycogenolysis is frequently downregulated to augment glucose storage in pre-malignant cells. Accumulated glycogen undergoes liquid-liquid phase separation, which results in the assembly of the Laforin-Mst1/2 complex and consequently sequesters Hippo kinases Mst1/2 in glycogen liquid droplets to relieve their inhibition on Yap. Moreover, G6PC or another glycogenolysis enzyme-liver glycogen phosphorylase (PYGL) deficiency in both human and mice results in glycogen storage disease along with liver enlargement and tumorigenesis in a Yap-dependent manner. Consistently, elimination of glycogen accumulation abrogates liver growth and cancer incidence, whereas increasing glycogen storage accelerates tumorigenesis. Thus, we concluded that cancer-initiating cells adapt a glycogen storing mode, which blocks Hippo signaling through glycogen phase separation to augment tumor incidence.

Keywords: Hippo signaling; Mst1; Mst2; cancer initiation; glycogen storage; liver cancer; phase separation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Aged
  • Aged, 80 and over
  • Animals
  • Carcinogenesis / metabolism*
  • Carcinogenesis / pathology*
  • Cell Line
  • Disease Models, Animal
  • Down-Regulation / genetics
  • Female
  • Gene Expression Regulation, Neoplastic
  • Glucose-6-Phosphatase / metabolism
  • Glycogen / metabolism*
  • Glycogen Phosphorylase / metabolism
  • Hepatocyte Growth Factor / metabolism
  • Hippo Signaling Pathway
  • Humans
  • Liver / metabolism
  • Liver / pathology
  • Liver Neoplasms / genetics
  • Liver Neoplasms / metabolism*
  • Liver Neoplasms / pathology*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Middle Aged
  • Neoplasm Staging
  • Phase Transition
  • Precancerous Conditions / metabolism
  • Precancerous Conditions / pathology
  • Protein Tyrosine Phosphatases, Non-Receptor / metabolism
  • Proto-Oncogene Proteins / metabolism
  • Serine-Threonine Kinase 3 / metabolism
  • YAP-Signaling Proteins / metabolism

Substances

  • Proto-Oncogene Proteins
  • YAP-Signaling Proteins
  • Yap1 protein, mouse
  • macrophage stimulating protein
  • Hepatocyte Growth Factor
  • Glycogen
  • Glycogen Phosphorylase
  • Serine-Threonine Kinase 3
  • Stk3 protein, mouse
  • Epm2a protein, mouse
  • Protein Tyrosine Phosphatases, Non-Receptor
  • Glucose-6-Phosphatase