Endoplasmic reticulum heat shock protein gp96 maintains liver homeostasis and promotes hepatocellular carcinogenesis

J Hepatol. 2015 Apr;62(4):879-88. doi: 10.1016/j.jhep.2014.11.010. Epub 2014 Nov 22.

Abstract

Background & aims: gp96, or grp94, is an endoplasmic reticulum (ER)-localized heat shock protein 90 paralog that acts as a protein chaperone and plays an important role for example in ER homeostasis, ER stress, Wnt and integrin signaling, and calcium homeostasis, which are vital processes in oncogenesis. However, the cancer-intrinsic function of gp96 remains controversial.

Methods: We studied the roles of gp96 in liver biology in mice via an Albumin promoter-driven Cre recombinase-mediated disruption of gp96 gene, hsp90b1. The impact of gp96 status on hepatic carcinogenesis in response to diethyl-nitrosoamine (DENA) was probed. The roles of gp96 on human hepatocellular carcinoma cells (HCC) were also examined pharmacologically with a targeted gp96 inhibitor.

Results: We demonstrated that gp96 maintains liver development and hepatocyte function in vivo, and its loss genetically promotes adaptive accumulation of long chain ceramides, accompanied by steatotic regeneration of residual gp96+ hepatocytes. The need for compensatory expansion of gp96+ cells in the gp96- background predisposes mice to develop carcinogen-induced hepatic hyperplasia and cancer from gp96+ but not gp96- hepatocytes. We also found that genetic and pharmacological inhibition of gp96 in human HCCs perturbed multiple growth signals, and attenuated proliferation and expansion.

Conclusions: gp96 is a pro-oncogenic chaperone and an attractive therapeutic target for HCC.

Keywords: Liver cancer; Molecular chaperone; gp96; grp94.

Publication types

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

MeSH terms

  • Alkylating Agents / pharmacology
  • Animals
  • Carcinogenesis* / drug effects
  • Carcinogenesis* / metabolism
  • Carcinoma, Hepatocellular / metabolism*
  • Cell Line, Tumor
  • Diethylnitrosamine / pharmacology
  • Endoplasmic Reticulum / metabolism
  • Heat-Shock Proteins / metabolism
  • Humans
  • Liver / metabolism*
  • Liver Neoplasms / metabolism*
  • Membrane Glycoproteins / metabolism*
  • Mice
  • Models, Animal
  • Molecular Chaperones / metabolism
  • Signal Transduction / drug effects

Substances

  • Alkylating Agents
  • Heat-Shock Proteins
  • Membrane Glycoproteins
  • Molecular Chaperones
  • endoplasmin
  • Diethylnitrosamine