Tumor-secreted factors induce IL-1β maturation via the glucose-mediated synergistic axis of mTOR and NF-κB pathways in mouse macrophages

PLoS One. 2018 Dec 26;13(12):e0209653. doi: 10.1371/journal.pone.0209653. eCollection 2018.

Abstract

Macrophages are one of the major cell types that produce IL-1β. IL-1β maturation occurs via inflammasome activation, and mature IL-1β is then released from the cell. Secreted IL-1β mediates inflammatory reactions in various pathological environments, such as those in infectious, autoimmune, and cancerous diseases. Although the mechanism of IL-1β production has been discovered in infectious and autoimmune diseases, its production mechanism in the tumor microenvironment is unclear. Therefore, the mechanism of IL-1β production in macrophages in the tumor microenvironment was investigated in this study. First, bone marrow-derived macrophages obtained from C57BL/6 mice were treated with B16F10 tumor-conditioned media (TCM) in vitro. TCM increased the levels of IL-1β via glucose-mediated activation of the inflammasome. Moreover, TCM enhanced the activation of both NF-κB and mTOR pathways in a glucose-dependent manner. In particular, the expression levels of mTORC1 component proteins were dependent on the TCM-induced activation of NF-κB signaling. In addition, TCM affected ASC-ASC interactions through increasing intracellular reactive oxygen species levels. Finally, glucose inhibition by inoculation with 2-deoxy-D-glucose in vivo decreased the IL-1β levels in both the blood and tumor region of B16F10-bearing C57BL/6 mice relative to those in PBS-injected tumor-bearing mice. These results suggest that glucose supplied from blood vessels might be important for IL-1β production in tumor-associated macrophages via the integrated signals of the NF-κB and mTOR pathways in the tumor microenvironment.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Blood Vessels / metabolism
  • Bone Marrow Cells / drug effects
  • Culture Media, Conditioned / pharmacology
  • Glucose / antagonists & inhibitors
  • Glucose / metabolism
  • Humans
  • Inflammasomes / drug effects
  • Inflammasomes / genetics
  • Inflammation / genetics*
  • Inflammation / pathology
  • Interleukin-1beta / genetics*
  • Macrophages / drug effects
  • Melanoma, Experimental / genetics*
  • Melanoma, Experimental / metabolism
  • Melanoma, Experimental / pathology
  • Mice
  • NF-kappa B / genetics
  • Reactive Oxygen Species / metabolism
  • Signal Transduction / drug effects
  • TOR Serine-Threonine Kinases / genetics*
  • Tumor Microenvironment / drug effects

Substances

  • Culture Media, Conditioned
  • Inflammasomes
  • Interleukin-1beta
  • NF-kappa B
  • Reactive Oxygen Species
  • mTOR protein, mouse
  • TOR Serine-Threonine Kinases
  • Glucose

Grants and funding

This research was supported by a grant from the Korea Health Technology R&D Project through the Korea Health Industry Development Institute (KHIDI), which is funded by the Ministry of Health & Welfare of the Republic of Korea (HI15C0450), and the Basic Science Research Program through the National Research Foundation of Korea (NRF), which is funded by the Ministry of Science, ICT and Future Planning of the Republic of Korea (2014M2B2A9030381, 2015M2B2A6028602, and 2018R1D1A1B07049097) to Y-JJ. Funding was also provided by a research grant from Kangwon National University in 2016 to Y-JJ.