Original article
Specific inhibition of the mitochondrial permeability transition prevents
lethal reperfusion injury
Laurent Argaud
a,b
, Odile Gateau-Roesch
a
, Danina Muntean
a
, Lara Chalabreysse
a
,
Joseph Loufouat
a
, Dominique Robert
b
, Michel Ovize
a,
*
a
Inserm E 0226, Laboratoire de Physiologie Lyon-Nord, Faculté de Médecine Lyon-Nord, Université Claude Bernard Lyon I, 8, avenue Rockefeller,
69373 Lyon cedex 8, France
b
Département d’Urgence et de Réanimation Médicale, Hôpital Edouard Herriot, Hospices Civils de Lyon, 5, place d’Arsonval,
69437 Lyon cedex 3, France
Received 13 October 2004; received in revised form 25 November 2004; accepted 3 December 2004
Available online 26 January 2005
Abstract
The aim of the present study was to determine whether specific inhibition of mitochondrial permeability transition (MPT) by NIM811 at
the time of reperfusion following acute myocardial infarction may protect the heart. MPT pore opening appears to be a pivotal event in cell
death following acute myocardial infarction. Recently, MPT pore opening has been involved in ischemic preconditioning. In protocol 1, NZW
rabbits underwent either no intervention (sham) or 10 min of ischemia followed by 5 min of reperfusion, preceded (preconditioned, PC) or not
(control, C) by 5 min of ischemia and 5 min of reperfusion. Additional rabbits were treated by cyclosporin A (CsA) or its non-
immunosuppressive and more specific derivative (NIM811) (10 mg kg
–1
, IV bolus), either 10 min before ischemia or 1 min before reperfu-
sion. Hearts were excised and mitochondria isolated for further assessment of Ca
2+
-induced MPT. In protocol 2, animals were randomly
assigned into similar experimental groups and underwent 30 min of ischemia and 4 h of reperfusion. Infarct size was assessed by TTC
staining, and apoptosis by TUNEL assay. The Ca
2+
overload required to induce MPT pore opening was significantly higher in NIM811, CsA
and PC groups than in controls. Both necrotic and apoptotic cardiomyocyte death were significantly reduced by NIM811, CsA and PC. In both
protocols, administration of NIM811 at reperfusion provided full protection. These data indicate that specific inhibition of MPT pore opening
at reperfusion following acute myocardial infarction provides a powerful antinecrotic and antiapoptotic protection.
© 2005 Elsevier Ltd. All rights reserved.
Keywords: Preconditioning; Cyclosporin A; NIM811; Ischemia; Reperfusion
1. Introduction
There is no doubt that reperfusion limits irreversible injury
following a prolonged ischemic insult, and reperfusion strat-
egies have been extensively studied and developed in clinical
practice over the last two decades [1,2]. Reperfusion has also
been named a “double-edged sword”, since it is associated
with reversible functional alterations including myocardial
stunning, arrhythmias or no-reflow [3]. The existence of
another form of reperfusion, namely lethal reperfusion injury,
has been widely investigated and remains a matter of debate
[4,5]. Demonstration of the existence of lethal reperfusion
injury would imply reduction of infarct size following admin-
istration of a pharmacological agent at the time of reperfu-
sion. Recently, the demonstration that several peptide growth
factors as well as caspase inhibitors can attenuate myocardial
cell death when administered at the time of reflow, reacti-
vated the issue of lethal reperfusion injury and the hope for
the development of adjunctive treatments to thrombolysis or
coronary angioplasty during acute myocardial infarction
[6–9]. It has been recently demonstrated that brief episodes
of ischemia–reperfusion performed at the time of reflow
(named “postconditioning”) may similarly attenuate lethal
reperfusion injury, likewise the previously described con-
trolled reperfusion [10–12].
In the past 3 years, increasing research has been focused
on the role of mitochondrial permeability transition (MPT)
* Corresponding author. Tel.: +33-4-78-77-70-74; fax:
+33-4-78-77-71-75.
E-mail address: ovize@rockefeller.univ-lyon1.fr (M. Ovize).
Journal of Molecular and Cellular Cardiology 38 (2005) 367–374
www.elsevier.com/locate/yjmcc
0022-2828/$ - see front matter © 2005 Elsevier Ltd. All rights reserved.
doi:10.1016/j.yjmcc.2004.12.001