The Cardioprotective Effects of Late-Phase Remote Preconditioning of Trauma Depends on Neurogenic Pathways and the Activation of PKC and NF-κB (But Not iNOS) in Mice

J Cardiovasc Pharmacol Ther. 2016 May;21(3):310-9. doi: 10.1177/1074248415609435. Epub 2015 Oct 7.

Abstract

Background: A superficial abdominal surgical incision elicits cardioprotection against cardiac ischemia-reperfusion (I/R) injury in mice. This process, called remote preconditioning of trauma (RPCT), has both an early and a late phase. Previous investigations have demonstrated that early RPCT reduces cardiac infarct size by 80% to 85%. We evaluated the cardioprotective and molecular mechanisms of late-phase RPCT in a murine I/R injury model.

Methods: Wild-type mice, bradykinin (BK) 2 receptor knockout mice, 3M transgenic mice (nuclear factor κB [NF-κb] repressor inhibitor of nuclear factor of kappa light polypeptide gene enhancer in B-cells inhibitor alpha [IκBα((S32A, S36A, Y42F))]), and inducible nitric oxide synthase (iNOS) knockout mice were analyzed using a previously established I/R injury model. A noninvasive abdominal surgical incision was made 24 hours prior to I/R injury and the infarct size was determined at 24 hours post-I/R injury.

Results: The results indicated that a strong cardioprotective effect occurred during late-phase RPCT (58.42% ± 1.89% sham vs 29.41% ± 4.00% late RPCT, mean area of the infarct divided by the mean area of the risk region; P ≤ .05; n = 10). Furthermore, pharmacological intervention revealed the involvement of neurogenic signaling in the beneficial effects of late RPCT via sensory and sympathetic thoracic nerves. Pharmacological experiments in transgenic mice-implicated BK receptors, β-adrenergic receptors, protein kinase C, and NF-κB but not iNOS signaling in the cardioprotective effects of late RPCT.

Conclusion: Late RPCT significantly decreased myocardial infarct size via neurogenic transmission and various other signaling pathways. This protective mechanism differentiates late and early RPCT. This study describes a new cardiac I/R injury prevention method and refines the concept of RPCT.

Keywords: cardioprotection; mechanism; myocardial ischemia reperfusion injury; remote nonischemic preconditioning; signal transduction.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Abdomen / surgery*
  • Animals
  • Apoptosis
  • Disease Models, Animal
  • Enzyme Activation
  • Female
  • Genetic Predisposition to Disease
  • Male
  • Mice, Knockout
  • Myocardial Infarction / enzymology
  • Myocardial Infarction / pathology
  • Myocardial Infarction / prevention & control*
  • Myocardial Reperfusion Injury / enzymology
  • Myocardial Reperfusion Injury / pathology
  • Myocardial Reperfusion Injury / physiopathology
  • Myocardial Reperfusion Injury / prevention & control*
  • Myocardium / enzymology*
  • Myocardium / pathology
  • NF-KappaB Inhibitor alpha / genetics
  • NF-KappaB Inhibitor alpha / metabolism
  • NF-kappa B / metabolism*
  • Nitric Oxide Synthase Type II / deficiency
  • Nitric Oxide Synthase Type II / genetics
  • Nitric Oxide Synthase Type II / metabolism*
  • Phenotype
  • Protein Kinase C / metabolism*
  • Receptor, Bradykinin B2 / deficiency
  • Receptor, Bradykinin B2 / genetics
  • Receptors, Adrenergic, beta / metabolism
  • Sensory Receptor Cells / metabolism
  • Synaptic Transmission*
  • Thoracic Nerves / metabolism
  • Thoracic Nerves / physiopathology
  • Time Factors

Substances

  • NF-kappa B
  • Nfkbia protein, mouse
  • Receptor, Bradykinin B2
  • Receptors, Adrenergic, beta
  • NF-KappaB Inhibitor alpha
  • Nitric Oxide Synthase Type II
  • Nos2 protein, mouse
  • Protein Kinase C