Nitric oxide, a mediator of inflammation, suppresses tumorigenesis

Cancer Res. 2004 Oct 1;64(19):6849-53. doi: 10.1158/0008-5472.CAN-04-2201.

Abstract

Inflammation influences the development of cancer. The nitric oxide synthase (NOS2) is induced by inflammatory cytokines, e.g., tumor necrosis factor alpha and interleukin 1beta, and produces nitric oxide (NO*), a critical mediator of the inflammatory response. Because p53 governs NO* production by transcriptionally transrepressing NOS2, we used a genetic strategy to determine whether NO* and p53 cooperatively regulate tumorigenesis. Lymphomas developed more rapidly in p53-/-NOS2-/- or p53-/-NOS2+/- mice than in p53-/-NOS2+/+ mice that were cross-bred into a >95% C57BL6 background and maintained in a pathogen-free condition. Likewise, sarcomas and lymphomas developed faster in p53+/-NOS2-/- or p53+/-NOS2+/- than in p53+/-NOS2+/+ mice. When compared with the double knockout mice, p53-/-NOS2+/+ mice showed a higher apoptotic index and a decreased proliferation index with an increased expression of death receptor ligands, CD95-L and tumor necrosis factor-related apoptosis-inducing ligand, and the cell cycle checkpoint protein, p21(waf1), in the spleen and thymus before tumor development. Furthermore, mice deficient in both p53 and NOS2 produced a high level of anti-inflammatory interleukin 10 when compared with p53-deficient mice. These studies provide genetic and mechanistic evidence that NO* can suppress tumorigenesis.

Publication types

  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • Apoptosis / physiology
  • Apoptosis Regulatory Proteins
  • Cyclin-Dependent Kinase Inhibitor p21
  • Cyclins / biosynthesis
  • Disease Models, Animal
  • Fas Ligand Protein
  • Female
  • Inbreeding
  • Inflammation Mediators / metabolism*
  • Interleukin-10 / biosynthesis
  • Ki-67 Antigen / biosynthesis
  • Lymphoma, T-Cell / enzymology
  • Lymphoma, T-Cell / metabolism*
  • Lymphoma, T-Cell / pathology
  • Male
  • Membrane Glycoproteins / biosynthesis
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Nitric Oxide / metabolism*
  • Nitric Oxide Synthase / deficiency
  • Nitric Oxide Synthase / genetics
  • Nitric Oxide Synthase / metabolism
  • Nitric Oxide Synthase Type II
  • Sarcoma, Experimental / enzymology
  • Sarcoma, Experimental / metabolism*
  • Sarcoma, Experimental / pathology
  • TNF-Related Apoptosis-Inducing Ligand
  • Tumor Necrosis Factor-alpha / biosynthesis
  • Tumor Suppressor Protein p53 / deficiency
  • Tumor Suppressor Protein p53 / genetics

Substances

  • Apoptosis Regulatory Proteins
  • Cdkn1a protein, mouse
  • Cyclin-Dependent Kinase Inhibitor p21
  • Cyclins
  • Fas Ligand Protein
  • Fasl protein, mouse
  • Inflammation Mediators
  • Ki-67 Antigen
  • Membrane Glycoproteins
  • TNF-Related Apoptosis-Inducing Ligand
  • Tnfsf10 protein, mouse
  • Tumor Necrosis Factor-alpha
  • Tumor Suppressor Protein p53
  • Interleukin-10
  • Nitric Oxide
  • Nitric Oxide Synthase
  • Nitric Oxide Synthase Type II
  • Nos2 protein, mouse