Staphylococcal alpha-toxin provokes neutrophil-dependent cardiac dysfunction: role of ICAM-1 and cys-leukotrienes

Am J Physiol Heart Circ Physiol. 2002 Mar;282(3):H1157-65. doi: 10.1152/ajpheart.00165.2001.

Abstract

The role of polymorphonuclear neutrophils (PMN) in septic myocardial dysfunction is presently unknown. Staphylococcus aureus infections are frequently associated with septic sequelae. Therefore, we perfused isolated rat hearts with low doses of alpha-toxin, the major staphylococcal exotoxin, followed by application of human PMN, N-formyl-methionyl-leucyl-phenylalanine, and arachidonic acid. In contrast to sham-perfused hearts (no alpha-toxin), a rise in coronary perfusion pressure (CPP) and a reduction of contractile function were noted, and cardiac expression of intercellular adhesion molecule (ICAM)-1 was detected by immunohistochemical methods and real-time PCR. Histological analysis and myeloperoxidase activity indicated cardiac PMN accumulation in alpha-toxin-challenged hearts. Major quantities of cysteinyl (cys)-leukotrienes (LT), LTB4, and 5-hydroxyeicosatetraenoic acid (5-HETE) were found in the perfusate of alpha-toxin-exposed hearts. With an anti-ICAM-1 antibody, neutrophil accumulation, leukotriene (LT) synthesis, coronary vasoconstriction, and the accompanying cardiodepression were suppressed. Similarly, the lipoxygenase inhibitor MK-886 blocked LT synthesis and maintained cardiac function. We conclude that low-dose alpha-toxin provokes coronary endothelial ICAM-1 expression and neutrophil accumulation, with subsequent synthesis of cys-LTs, LTB4, and 5-HETE under conditions of appropriate stimulation. This response is linked with coronary vasoconstriction and contractile dysfunction, with cys-LT synthesis and maldistribution of perfusion offered as likely underlying mechanisms.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Arachidonic Acid / pharmacology
  • Bacterial Toxins / toxicity*
  • Exotoxins / toxicity*
  • Heart / drug effects*
  • Heart / physiopathology
  • Hemolysin Proteins / toxicity*
  • Humans
  • Hydrazones
  • In Vitro Techniques
  • Intercellular Adhesion Molecule-1 / genetics*
  • Leukotrienes / metabolism*
  • Myocardium / pathology
  • N-Formylmethionine Leucyl-Phenylalanine / pharmacology
  • Neutrophils / drug effects
  • Neutrophils / physiology*
  • Oligonucleotide Probes
  • Perfusion
  • Rats
  • Thiophenes

Substances

  • Bacterial Toxins
  • Exotoxins
  • Hemolysin Proteins
  • Hydrazones
  • Leukotrienes
  • Oligonucleotide Probes
  • Thiophenes
  • staphylococcal alpha-toxin
  • 2-thiophenaldehyde 2-pyridylhydrazone
  • Intercellular Adhesion Molecule-1
  • Arachidonic Acid
  • N-Formylmethionine Leucyl-Phenylalanine