STING-mediated type-I interferons contribute to the neuroinflammatory process and detrimental effects following traumatic brain injury

J Neuroinflammation. 2018 Nov 21;15(1):323. doi: 10.1186/s12974-018-1354-7.

Abstract

Background: Traumatic brain injury (TBI) represents a major cause of disability and death worldwide with sustained neuroinflammation and autophagy dysfunction contributing to the cellular damage. Stimulator of interferon genes (STING)-induced type-I interferon (IFN) signalling is known to be essential in mounting the innate immune response against infections and cell injury in the periphery, but its role in the CNS remains unclear. We previously identified the type-I IFN pathway as a key mediator of neuroinflammation and neuronal cell death in TBI. However, the modulation of the type-I IFN and neuroinflammatory responses by STING and its contribution to autophagy and neuronal cell death after TBI has not been explored.

Methods: C57BL/6J wild-type (WT) and STING-/- mice (8-10-week-old males) were subjected to controlled cortical impact (CCI) surgery and brains analysed by QPCR, Western blot and immunohistochemical analyses at 2 h or 24 h. STING expression was also analysed by QPCR in post-mortem human brain samples.

Results: A significant upregulation in STING expression was identified in late trauma human brain samples that was confirmed in wild-type mice at 2 h and 24 h after CCI. This correlated with an elevated pro-inflammatory cytokine profile with increased TNF-α, IL-6, IL-1β and type-I IFN (IFN-α and IFN-β) levels. This expression was suppressed in the STING-/- mice with a smaller lesion volume in the knockout animals at 24 h post CCI. Wild-type mice also displayed increased levels of autophagy markers, LC3-II, p62 and LAMP2 after TBI; however, STING-/- mice showed reduced LAMP2 expression suggesting a role for STING in driving dysfunctional autophagy after TBI.

Conclusion: Our data implicates a detrimental role for STING in mediating the TBI-induced neuroinflammatory response and autophagy dysfunction, potentially identifying a new therapeutic target for reducing cellular damage in TBI.

Keywords: Autophagy; Neuroinflammation; STING; Traumatic brain injury; Type-I interferon.

MeSH terms

  • Animals
  • Autophagy / genetics
  • Brain / metabolism*
  • Brain / pathology
  • Brain Injuries, Traumatic / complications*
  • Brain Injuries, Traumatic / pathology
  • Calcium-Binding Proteins / metabolism
  • Cytokines / genetics
  • Cytokines / metabolism
  • Disease Models, Animal
  • Encephalitis / etiology*
  • Encephalitis / metabolism*
  • Functional Laterality
  • Gene Expression Regulation / genetics*
  • Glial Fibrillary Acidic Protein / metabolism
  • Hepatocyte Nuclear Factor 3-alpha / metabolism
  • Humans
  • Lysosomal-Associated Membrane Protein 2 / genetics
  • Lysosomal-Associated Membrane Protein 2 / metabolism
  • Male
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Microfilament Proteins / metabolism
  • Nerve Tissue Proteins / metabolism

Substances

  • Aif1 protein, mouse
  • Calcium-Binding Proteins
  • Cytokines
  • Foxa1 protein, mouse
  • Glial Fibrillary Acidic Protein
  • Hepatocyte Nuclear Factor 3-alpha
  • Lysosomal-Associated Membrane Protein 2
  • Membrane Proteins
  • Microfilament Proteins
  • Nerve Tissue Proteins
  • Sting1 protein, mouse