Proinflammatory cytokine IL-1 beta promotes tumor growth of Lewis lung carcinoma by induction of angiogenic factors: in vivo analysis of tumor-stromal interaction

J Immunol. 2002 Jul 1;169(1):469-75. doi: 10.4049/jimmunol.169.1.469.

Abstract

Inflammatory conditions are associated with tumor development. IL-1beta is a multifunctional and proinflammatory cytokine that affects nearly all types of cells. To investigate the role of IL-1beta in tumor growth in vivo, we transduced the retroviral vector coding human IL-1beta gene into mouse Lewis lung carcinoma (LLC) cells and subsequently inoculated the transformant (LLC/IL-1beta) to syngeneic C57BL/6 mice. Tumors derived from LLC/IL-1beta grew faster (240%, day 18, vs null-vector control LLC/neo; p < 0.01) and showed more abundant vasculature (250%, vs LLC/neo; p < 0.05), whereas LLC/IL-1beta cells, LLC/neo cells, and wild-type LLC cells did not show any significant difference in the growth rate in vitro. As compared with LLC/neo cells, LLC/IL-1beta cells secreted 2-fold the amount of vascular endothelial growth factor and >10-fold the amount of macrophage-inflammatory protein-2 (CXCL2), one of whose main functions is angiogenesis. Although LLC/IL-1beta itself did not secrete hepatocyte growth factor (HGF), the tumor derived from LLC/IL-1beta cells also contained a >4-fold higher concentration of HGF, another angiogenic factor. In situ hybridization of HGF mRNA in LLC/IL-1beta tumor sections demonstrated that stromal fibroblasts and infiltrating cells overexpressed HGF mRNA. Moreover, when cultured in the presence of HGF in vitro, LLC/IL-1beta cells secreted even larger amounts of vascular endothelial growth factor and macrophage-inflammatory protein-2. The antiangiogenic agent TNP-470 and anti-CXCR2 Ab inhibited the tumor growth of LLC/IL-1beta cells in vivo. These results indicated that secreting IL-1beta into the tumor milieu induces several angiogenic factors from tumor and stromal cells and thus promotes tumor growth through hyperneovascularization.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Angiogenesis Inducing Agents / biosynthesis*
  • Angiogenesis Inhibitors / pharmacology
  • Animals
  • Antibodies / pharmacology
  • Carcinoma, Lewis Lung / blood supply
  • Carcinoma, Lewis Lung / immunology*
  • Carcinoma, Lewis Lung / metabolism
  • Carcinoma, Lewis Lung / pathology*
  • Cell Communication / genetics
  • Cell Communication / immunology
  • Cell Division / immunology
  • Chemokine CXCL2
  • Chemokines / biosynthesis
  • Chemokines / metabolism
  • Cyclohexanes
  • Endothelial Growth Factors / biosynthesis
  • Endothelial Growth Factors / metabolism
  • Gene Transfer Techniques
  • Hepatocyte Growth Factor / biosynthesis
  • Hepatocyte Growth Factor / genetics
  • Humans
  • Immunohistochemistry
  • Inflammation / immunology
  • Interleukin-1 / biosynthesis
  • Interleukin-1 / genetics
  • Interleukin-1 / physiology*
  • Lymphokines / biosynthesis
  • Lymphokines / metabolism
  • Male
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Mice, Nude
  • O-(Chloroacetylcarbamoyl)fumagillol
  • Receptors, Interleukin-8B / immunology
  • Sesquiterpenes / pharmacology
  • Species Specificity
  • Stromal Cells / immunology
  • Stromal Cells / metabolism
  • Stromal Cells / pathology
  • Tumor Cells, Cultured
  • Up-Regulation / genetics
  • Up-Regulation / immunology
  • Vascular Endothelial Growth Factor A
  • Vascular Endothelial Growth Factors

Substances

  • Angiogenesis Inducing Agents
  • Angiogenesis Inhibitors
  • Antibodies
  • Chemokine CXCL2
  • Chemokines
  • Cxcl2 protein, mouse
  • Cyclohexanes
  • Endothelial Growth Factors
  • Interleukin-1
  • Lymphokines
  • Receptors, Interleukin-8B
  • Sesquiterpenes
  • Vascular Endothelial Growth Factor A
  • Vascular Endothelial Growth Factors
  • Hepatocyte Growth Factor
  • O-(Chloroacetylcarbamoyl)fumagillol