Activated α2-macroglobulin binding to human prostate cancer cells triggers insulin-like responses

J Biol Chem. 2015 Apr 10;290(15):9571-87. doi: 10.1074/jbc.M114.617837. Epub 2015 Feb 26.

Abstract

Ligation of cell surface GRP78 by activated α2-macroglobulin (α2M*) promotes cell proliferation and suppresses apoptosis. α2M*-treated human prostate cancer cells exhibit a 2-3-fold increase in glucose uptake and lactate secretion, an effect similar to insulin treatment. In both α2M* and insulin-treated cells, the mRNA levels of SREBP1-c, SREBP2, fatty-acid synthase, acetyl-CoA carboxylase, ATP citrate lyase, and Glut-1 were significantly increased together with their protein levels, except for SREBP2. Pretreatment of cells with α2M* antagonist antibody directed against the carboxyl-terminal domain of GRP78 blocks these α2M*-mediated effects, and silencing GRP78 expression by RNAi inhibits up-regulation of ATP citrate lyase and fatty-acid synthase. α2M* induces a 2-3-fold increase in lipogenesis as determined by 6-[(14)C]glucose or 1-[(14)C]acetate incorporation into free cholesterol, cholesterol esters, triglycerides, free fatty acids, and phosphatidylcholine, which is blocked by inhibitors of fatty-acid synthase, PI 3-kinase, mTORC, or an antibody against the carboxyl-terminal domain of GRP78. We also assessed the incorporation of [(14)CH3]choline into phosphatidylcholine and observed similar effects. Lipogenesis is significantly affected by pretreatment of prostate cancer cells with fatostatin A, which blocks sterol regulatory element-binding protein proteolytic cleavage and activation. This study demonstrates that α2M* functions as a growth factor, leading to proliferation of prostate cancer cells by promoting insulin-like responses. An antibody against the carboxyl-terminal domain of GRP78 may have important applications in prostate cancer therapy.

Keywords: Aerobic Glycolysis; Antibody Directed Against the Carboxyl-terminal Domain of GRP78; Cell Surface GRP78; Glycolysis; Lipogenesis; Prostate Cancer; Signal Transduction; Warburg Effect; α-2-Macroglobulin and Metabolic Regulation.

MeSH terms

  • Antibodies, Neoplasm / immunology
  • Antibodies, Neoplasm / pharmacology
  • Blotting, Western
  • Cell Line, Tumor
  • Cell Proliferation / drug effects*
  • Cholesterol / metabolism
  • Endoplasmic Reticulum Chaperone BiP
  • Fatty Acid Synthase, Type I / genetics
  • Fatty Acid Synthase, Type I / metabolism
  • Gene Expression / drug effects
  • Glucose / metabolism*
  • Heat-Shock Proteins / genetics
  • Heat-Shock Proteins / immunology
  • Heat-Shock Proteins / metabolism
  • Humans
  • Hypoglycemic Agents / pharmacology
  • Insulin / pharmacology*
  • Lactates / metabolism
  • Lipid Metabolism / drug effects
  • Lipid Metabolism / genetics
  • Lipogenesis / drug effects
  • Lipogenesis / genetics
  • Male
  • Prostatic Neoplasms / genetics
  • Prostatic Neoplasms / metabolism
  • Prostatic Neoplasms / pathology
  • Protein Binding
  • Reverse Transcriptase Polymerase Chain Reaction
  • Sterol Regulatory Element Binding Protein 1 / genetics
  • Sterol Regulatory Element Binding Protein 1 / metabolism
  • alpha-Macroglobulins / metabolism
  • alpha-Macroglobulins / pharmacology*

Substances

  • Antibodies, Neoplasm
  • Endoplasmic Reticulum Chaperone BiP
  • HSPA5 protein, human
  • Heat-Shock Proteins
  • Hypoglycemic Agents
  • Insulin
  • Lactates
  • Sterol Regulatory Element Binding Protein 1
  • alpha-Macroglobulins
  • Cholesterol
  • FASN protein, human
  • Fatty Acid Synthase, Type I
  • Glucose