Identifying lysophosphatidic acid receptor subtype 1 (LPA1) as a novel factor to modulate microglial activation and their TNF-α production by activating ERK1/2

Biochim Biophys Acta Mol Cell Biol Lipids. 2018 Oct;1863(10):1237-1245. doi: 10.1016/j.bbalip.2018.07.015. Epub 2018 Jul 30.

Abstract

Microglia regulate immune responses in the brain, and their activation is key to the pathogenesis of diverse neurological diseases. Receptor-mediated lysophosphatidic acid (LPA) signaling has been known to regulate microglial biology, but it is still unclear which receptor subtypes guide the biology, particularly, microglial activation. Here, we investigated the pathogenic aspects of LPA receptor subtype 1 (LPA1) in microglial activation using a systemic lipopolysaccharide (LPS) administration-induced septic mouse model in vivo and LPS-stimulated rat primary microglia in vitro. LPA1 knockdown in the brain with its specific shRNA lentivirus attenuated the sepsis-induced microglia activation, morphological transformation, and proliferation. LPA1 knockdown also resulted in the downregulation of TNF-α, at both mRNA and protein levels in septic brains, but not IL-1β or IL-6. In rat primary microglia, genetic or pharmacological blockade of LPA1 attenuated gene upregulation and secretion of TNF-α in LPS-stimulated cells. In particular, the latter was associated with the suppressed TNF-α converting enzyme (TACE) activity. We reaffirmed these biological aspects using a BV2 microglial cell line in which LPA1 expression was negligible. LPA1 overexpression in BV2 cells led to significant increments in TNF-α production upon stimulation with LPS, whereas inhibiting LPA1 reversed the production. We further identified ERK1/2, but not p38 MAPK or Akt, as the underlying effector pathway after LPA1 activation in both septic brains and stimulated microglia. The current findings of the novel role of LPA1 in microglial activation along with its mechanistic aspects could be applied to understanding the pathogenesis of diverse neurological diseases that involve microglial activation.

Keywords: ERK1/2; LPA(1); Microglia; Septic brain; TACE; TNF-α.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • ADAM17 Protein / metabolism
  • Animals
  • Cells, Cultured
  • Disease Models, Animal
  • Gene Expression Regulation / drug effects
  • Gene Knockdown Techniques
  • Lipopolysaccharides / adverse effects*
  • MAP Kinase Signaling System
  • Male
  • Mice
  • Microglia / cytology
  • Microglia / drug effects
  • Microglia / immunology*
  • Rats
  • Receptors, Lysophosphatidic Acid / genetics*
  • Receptors, Lysophosphatidic Acid / metabolism
  • Sepsis / chemically induced
  • Sepsis / genetics
  • Sepsis / immunology*
  • Tumor Necrosis Factor-alpha / genetics*
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • Lipopolysaccharides
  • Receptors, Lysophosphatidic Acid
  • Tumor Necrosis Factor-alpha
  • ADAM17 Protein