TNFα and IL-17 cooperatively stimulate glucose metabolism and growth factor production in human colorectal cancer cells

Mol Cancer. 2013 Jul 17:12:78. doi: 10.1186/1476-4598-12-78.

Abstract

Background: Inflammation is a well-known etiological factor for colorectal cancer, but mechanisms underlying the linkage between inflammation and cancer are incompletely understood. We hypothesized that two pro-inflammatory cytokines, TNFα and IL-17, might play a role in promoting colorectal carcinogenesis. Aerobic glycolysis is a metabolic adaptation that promotes the survival/proliferation of cancer cells. Paracrine signaling between tumor cells and cancer-associated fibroblasts also plays a role in carcinogenesis.

Methods: The effect of TNFα and IL-17 on aerobic glycolysis and growth factor production in cultured human colorectal cancer cells was investigated. Glucose utilization and lactate production were quantified by measuring the disappearance of glucose and appearance of lactate in the culture medium. Glucose transporter and glycolytic enzyme expression levels were measured by immunoblotting.

Results: TNFα and IL-17 cooperatively stimulated glycolysis in HT-29, T84, Caco-2 and HCT116 colorectal cancer cells. Treatment of HT-29 cells with TNFα plus IL-17 also increased the expression of HIF-1α and c-myc, two factors know to induce the transcription of genes encoding components of the glycolytic pathway. To further investigate mechanisms for cytokine-stimulated glycolysis, the effects of TNFα and IL-17 on expression of six members and one regulator of the glycolytic pathway were investigated. TNFα and IL-17 cooperatively increased the expression of the glucose transporter SLC2A1 and hexokinase-2 but did not regulate expression of glucose transporter SLC2A3, enolase-1, pyruvate kinase M2, lactate dehydrogenase A, or 6-phoshofructo-2-kinase/fructose-2,6-bisphosphatase-3 (PFKFB3). Experiments with inhibitors indicated that HIF-1α played a role in induction of SLC2A1 and that the transcription factor NF-κB played a role in induction of hexokinase-2 by TNFα and IL-17. TNFα and IL-17 also synergistically stimulated production by HT-29 cells of a growth factor that simulated proliferation/survival of NIL8 fibroblastic cells. The activity of this factor was not specifically inhibited by the EGFR inhibitor AG1478, indicating that it is not an EGFR ligand.

Conclusions: Chronic inflammation is known to promote colorectal tumorigenesis. The pro-inflammatory cytokines TNFα and IL-17 may contribute to this effect by stimulating glycolysis and growth factor production in colorectal cancer cells.

MeSH terms

  • Cell Proliferation / drug effects
  • Cell Survival / drug effects
  • Colorectal Neoplasms / genetics
  • Colorectal Neoplasms / metabolism*
  • Gene Expression Regulation, Neoplastic / drug effects
  • Glucose / metabolism*
  • Glucose Transporter Type 1 / genetics
  • Glucose Transporter Type 1 / metabolism
  • Glycolysis / drug effects
  • HT29 Cells
  • Humans
  • Hypoxia-Inducible Factor 1, alpha Subunit / genetics
  • Hypoxia-Inducible Factor 1, alpha Subunit / metabolism
  • Interleukin-17 / pharmacology*
  • Lactic Acid / biosynthesis
  • Metabolic Networks and Pathways / drug effects*
  • Phosphorylation
  • Proto-Oncogene Proteins c-akt / metabolism
  • Proto-Oncogene Proteins c-myc / genetics
  • Proto-Oncogene Proteins c-myc / metabolism
  • Tumor Necrosis Factor-alpha / pharmacology*

Substances

  • Glucose Transporter Type 1
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Interleukin-17
  • Proto-Oncogene Proteins c-myc
  • Tumor Necrosis Factor-alpha
  • Lactic Acid
  • Proto-Oncogene Proteins c-akt
  • Glucose