NF-κB inhibition by bortezomib permits IFN-γ-activated RIP1 kinase-dependent necrosis in renal cell carcinoma

Mol Cancer Ther. 2013 Aug;12(8):1568-78. doi: 10.1158/1535-7163.MCT-12-1010. Epub 2013 May 8.

Abstract

Advanced renal cell carcinoma (RCC) is an invariably fatal cancer. Currently, small-molecule inhibitors that target cell growth, angiogenesis, or nutrient-sensing pathways represent the primary pharmacologic interventions for this disease, but these inhibitors only delay tumor progression and are not curative. The cytokine IFN-γ showed the potential to provide lasting remission in several phase I/II trials for advanced RCCs, but subsequent trials, including a multicenter phase III study using IFN-γ as a monotherapy for RCCs, were less promising. Notably, these trials were designed to exploit the indirect immunomodulatory effects of IFN-γ, whereas its direct antitumor properties--including its ability to trigger programmed cell death in tumors-remain mostly untapped. Here, we show that the proteasome inhibitor bortezomib (PS-341, Velcade) sensitizes otherwise resistant RCC cells to direct necrotic death by IFN-γ. Mechanistically, we show that bortezomib functions, at least in part, by inhibiting prosurvival NF-κB signaling. In the absence of this signal, IFN-γ triggers programmed necrosis (or "necroptosis") dependent on the kinase RIP1. When taken together with the observation that NF-κB signaling is elevated in RCCs, these results provide rationale for the combined use of IFN-γ and bortezomib in the treatment of metastatic RCCs.

Publication types

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

MeSH terms

  • Antineoplastic Agents / pharmacology*
  • Apoptosis / drug effects
  • Boronic Acids / pharmacology*
  • Bortezomib
  • Carcinoma, Renal Cell / metabolism*
  • Cell Line, Tumor
  • Enzyme Activation / drug effects
  • Humans
  • I-kappa B Kinase / antagonists & inhibitors
  • Interferon-gamma / pharmacology*
  • Kidney Neoplasms / metabolism*
  • NF-kappa B / antagonists & inhibitors*
  • NF-kappa B / metabolism
  • Necrosis / drug therapy
  • Proteasome Inhibitors / pharmacology
  • Pyrazines / pharmacology*
  • Receptor-Interacting Protein Serine-Threonine Kinases / metabolism*

Substances

  • Antineoplastic Agents
  • Boronic Acids
  • NF-kappa B
  • Proteasome Inhibitors
  • Pyrazines
  • Bortezomib
  • Interferon-gamma
  • Receptor-Interacting Protein Serine-Threonine Kinases
  • I-kappa B Kinase