Early neutrophil infiltration is critical for inflammation-sensitized hypoxic-ischemic brain injury in newborns

J Cereb Blood Flow Metab. 2020 Nov;40(11):2188-2200. doi: 10.1177/0271678X19891839. Epub 2019 Dec 16.

Abstract

Neutrophils are the most abundant leukocytes and usually the first immune cell-type recruited to a site of infection or tissue damage. In asphyxiated neonates, elevated peripheral neutrophil counts are associated with poorer neurological outcomes. Induced neutropenia provides brain protection in animal models of neonatal hypoxic-ischemic (HI) injury, but the anti-neutrophil serum used in past studies heavily cross-reacts with monocytes, thus complicating the interpretation of results. Here we examined neutrophil influx and extravasation, and used a specific anti-Ly6G antibody for induced neutropenia against lipopolysaccharide (LPS)-pretreated HI injury in murine neonates, a model for inflammation-sensitized hypoxic-ischemic encephalopathy (HIE). As early as 6 h after the LPS/HI insult, the mRNAs for neutrophil-recruiting and mitogenic chemokines ascended in the ipsilateral hemisphere, coinciding with immuno-detection of neutrophils. However, neutrophils mainly resided within blood vessels, exhibiting signs for neutrophil extracellular traps (NETs), before 48 h post-LPS/HI. Prophylactic anti-Ly6G treatment blocked the brain infiltration of neutrophils, but not monocytes or lymphocytes, and markedly decreased LPS/HI-induced pro-inflammatory cytokines, matrix metalloproteinase 9 (MMP-9), and brain tissue loss. In contrast, anti-Ly6G treatment at 4 h post-LPS/HI failed to prevent the influx of neutrophils and brain damage. Together, these results suggest important pathological functions for early-arriving neutrophils in inflammation-sensitized HIE.

Keywords: Hypoxic-ischemic encephalopathy; anti-Ly6G; lipopolysaccharide; matrix metalloproteinases; neutrophil extracellular trap.

Publication types

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

MeSH terms

  • Animals
  • Animals, Newborn
  • Antigens, Ly / immunology
  • Biomarkers
  • Brain Injuries / etiology
  • Brain Injuries / metabolism
  • Brain Injuries / pathology
  • Chemotaxis, Leukocyte / genetics
  • Chemotaxis, Leukocyte / immunology
  • Cytokines / metabolism
  • Disease Models, Animal
  • Disease Susceptibility
  • Extracellular Traps / immunology
  • Extracellular Traps / metabolism
  • Fluorescent Antibody Technique
  • Hypoxia-Ischemia, Brain / etiology*
  • Hypoxia-Ischemia, Brain / metabolism
  • Hypoxia-Ischemia, Brain / pathology*
  • Immunohistochemistry
  • Inflammation / complications*
  • Inflammation / pathology*
  • Lipopolysaccharides / adverse effects
  • Lipopolysaccharides / immunology
  • Matrix Metalloproteinases / metabolism
  • Mice
  • Neutrophil Infiltration*
  • Neutrophils / immunology
  • Neutrophils / metabolism
  • Neutrophils / pathology*

Substances

  • Antigens, Ly
  • Biomarkers
  • Cytokines
  • Lipopolysaccharides
  • Ly6G antigen, mouse
  • Matrix Metalloproteinases