Epigenetic Modulation of Microglial Inflammatory Gene Loci in Helminth-Induced Immune Suppression: Implications for Immune Regulation in Neurocysticercosis

ASN Neuro. 2015 Jul 6;7(4):1759091415592126. doi: 10.1177/1759091415592126. Print 2015 Jul-Aug.

Abstract

In neurocysticercosis, parasite-induced immune suppressive effects are thought to play an important role in enabling site-specific inhibition of inflammatory responses to infections. It is axiomatic that microglia-mediated (M1 proinflammatory) response causes central nervous system inflammation; however, the mechanisms by which helminth parasites modulate microglia activation remain poorly understood. Here, we show that microglia display a diminished expression of M1-inflammatory mediators such as tumor necrosis factor-alpha (TNF-α), interleukin-6 (IL-6), and nitric oxide synthase 2 (NOS2) in murine neurocysticercosis. Microglia also exhibited a lack of myeloid cell maturation marker major histocompatibility complex (MHC)-II in these parasite-infected brains. Treatment of microglia with helminth soluble/secreted factors (HSFs) in vitro did not induce expression of M1-inflammatory signature molecule NOS2 as well as MHC-II in primary microglia. However, HSF treatment completely inhibited lipopolysaccharide-induced increase in expression of MHC-II, NOS2 and nitric oxide production in these cells. As epigenetic modulation of chromatin states that regulates recruitment of RNA polymerase II (Pol-II) is a key regulatory step in determining gene expression and functional outcome, we next evaluated whether HSF induced modulation of these phenomenon in microglia in vitro. Indeed, HSF downregulated Pol-II recruitment to the promoter region of TNF-α, IL-6, NOS2, MHC-II, and transcription factor CIITA (a regulator of MHC-II expression), by itself. Moreover, HSF suppressed the lipopolysaccharide-induced increase in Pol-II recruitment as well. In addition, HSF exposure reduced the positive histone marks H3K4Me3 and H3K9/14Ac at the promoter of TNF-α, IL-6, NOS2, MHC-II, and CIITA. These studies provide a novel mechanistic insight into helminth-mediated immune suppression in microglia via modulation of epigenetic processes.

Keywords: epigenetics; helminth; immune suppression; microglia; neurocysticercosis.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Animals, Newborn
  • Cells, Cultured
  • Central Nervous System / pathology*
  • Chromatin Immunoprecipitation
  • Cytokines / genetics
  • Cytokines / metabolism
  • Disease Models, Animal
  • Epigenesis, Genetic / drug effects
  • Epigenesis, Genetic / immunology*
  • Helminthiasis / immunology*
  • Helminthiasis / pathology*
  • Helminths / metabolism
  • Helminths / pathogenicity*
  • Histocompatibility Antigens Class II / genetics
  • Histocompatibility Antigens Class II / metabolism
  • Histones / genetics
  • Histones / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Microglia / drug effects
  • Microglia / metabolism*
  • Nitric Oxide Synthase Type II / genetics
  • Nitric Oxide Synthase Type II / metabolism
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism
  • Polysaccharides / pharmacology
  • RNA Polymerase II / genetics
  • RNA Polymerase II / metabolism
  • Trans-Activators / genetics
  • Trans-Activators / metabolism

Substances

  • Cytokines
  • Histocompatibility Antigens Class II
  • Histones
  • MHC class II transactivator protein
  • Nuclear Proteins
  • Polysaccharides
  • Trans-Activators
  • Nitric Oxide Synthase Type II
  • Nos2 protein, mouse
  • RNA Polymerase II