Pathogenic Role of the Damage-Associated Molecular Patterns S100A8 and S100A9 in Coxsackievirus B3-Induced Myocarditis

Circ Heart Fail. 2017 Nov;10(11):e004125. doi: 10.1161/CIRCHEARTFAILURE.117.004125.

Abstract

Background: The alarmins S100A8 and S100A9 are damage-associated molecular patterns, which play a pivotal role in cardiovascular diseases, inflammation, and viral infections. We aimed to investigate their role in Coxsackievirus B3 (CVB3)-induced myocarditis.

Methods and results: S100A8 and S100A9 mRNA expression was 13.0-fold (P=0.012) and 5.1-fold (P=0.038) higher in endomyocardial biopsies from patients with CVB3-positive myocarditis compared with controls, respectively. Elimination of CVB3 led to a downregulation of these alarmins. CVB3-infected mice developed an impaired left ventricular function and displayed an increased left ventricular S100A8 and S100A9 protein expression versus controls. In contrast, CVB3-infected S100A9 knockout mice, which are also a complete knockout for S100A8 on protein level, showed an improved left ventricular function, which was associated with a reduced cardiac inflammatory and oxidative response, and lower CVB3 copy number compared with wild-type CVB3 mice. Exogenous application of S100A8 to S100A9 knockout CVB3 mice induced a severe myocarditis similar to wild-type CVB3 mice. In CVB3-infected HL-1 cells, S100A8 and S100A9 enhanced oxidative stress and CVB3 copy number compared with unstimulated infected cells. In CVB3-infected RAW macrophages, both alarmins increased MIP-2 (macrophage inflammatory protein-2) chemokine expression, which was reduced in CVB3 S100A8 knockdown versus scrambled siRNA CVB3 cells.

Conclusions: S100A8 and S100A9 aggravate CVB3-induced myocarditis and might serve as therapeutic targets in inflammatory cardiomyopathies.

Keywords: Coxsackievirus B3; RAGE; S100A8; S100A9; myocarditis.

MeSH terms

  • Adult
  • Animals
  • Calgranulin A / deficiency
  • Calgranulin A / genetics
  • Calgranulin A / metabolism*
  • Calgranulin B / genetics
  • Calgranulin B / metabolism*
  • Case-Control Studies
  • Chemokine CXCL2 / metabolism
  • Coxsackievirus Infections / diagnosis
  • Coxsackievirus Infections / genetics
  • Coxsackievirus Infections / metabolism*
  • Coxsackievirus Infections / virology
  • Disease Models, Animal
  • Enterovirus B, Human / genetics
  • Enterovirus B, Human / pathogenicity*
  • Female
  • Fibrosis
  • Host-Pathogen Interactions
  • Humans
  • Macrophages / metabolism
  • Macrophages / virology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Middle Aged
  • Myocarditis / diagnosis
  • Myocarditis / genetics
  • Myocarditis / metabolism*
  • Myocarditis / virology
  • Myocytes, Cardiac / metabolism*
  • Myocytes, Cardiac / pathology
  • Myocytes, Cardiac / virology
  • Neutrophil Infiltration
  • Oxidative Stress
  • RAW 264.7 Cells
  • RNA Interference
  • RNA, Messenger / genetics
  • Receptor for Advanced Glycation End Products / metabolism
  • Signal Transduction
  • Transfection
  • Ventricular Function, Left

Substances

  • Ager protein, mouse
  • Calgranulin A
  • Calgranulin B
  • Chemokine CXCL2
  • Cxcl2 protein, mouse
  • RNA, Messenger
  • Receptor for Advanced Glycation End Products
  • S100A9 protein, mouse
  • S100a8 protein, mouse