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Am J Physiol Heart Circ Physiol (November 26, 2003). doi:10.1152/ajpheart.00811.2003
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Submitted on August 21, 2003
Accepted on November 19, 2003

HYPOTHERMIA AUGMENTS REACTIVE OXYGEN SPECIES DETECTED IN THE GUINEA PIG ISOLATED PERFUSED HEART

Amadou K S Camara1, Matthias L Riess2, Leo G Kevin1, Enis Novalija3, and David F Stowe4*

1 Department of Anesthesiology, Medical College of Wisconsin, Milwaukee, Wisconsin, USA
2 Department of Anesthesiology, Medical College of Wisconsin, Milwaukee, Wisconsin, USA; Department of Physiology, Medical College of Wisconsin, Milwaukee, Wisconsin, USA; Department of Anesthesiology and Intensive Care Medicine, University Hospital, Munster, Germany
3 Department of Anesthesiology, Medical College of Wisconsin, Milwaukee, Wisconsin, USA; Department of Physiology, Medical College of Wisconsin, Milwaukee, Wisconsin, USA
4 Department of Anesthesiology, Medical College of Wisconsin, Milwaukee, Wisconsin, USA; Research Services Veterans Affairs Medical Center, Veterans Affairs Medical Center, Milwaukee, Wisconsin, USA; Department of Biomedical Engineering, Marquette University, Milwaukee, Wisconsin, USA

* To whom correspondence should be addressed. E-mail: dfstowe{at}mcw.edu.

Hypothermic perfusion of the heart decreases oxidative phosphorylation and increases NADH. Because O2 and substrates remain available and respiration (electron transport system, ETS) may become impaired, we examined if reactive oxygen species (ROS) exist in excess during hypothermic perfusion. A fiberoptic probe was placed on the left ventricular free wall of isolated guinea pig hearts to record intracellular ROS, principally superoxide (O2.-), and an extracellular reactive nitrogen reactant, principally peroxynitrite (ONOO-), a product of nitric oxide (NO.) + O2.-. Hearts were loaded with dihydroethidium (DHE), which is oxidized by O2 .- to ethidium, or perfused with L-tyrosine, which is oxidized by ONOO- to dityrosine. Shifts in fluorescence were measured on-line; diTyr fluorescence was also measured in coronary effluent. To validate our methods and to examine the source and identity of ROS during cold perfusion, we examined effects of a superoxide dismutase mimetic Mn (III) tetrakis (4-benzoic acid) porphyrin chloride (MnTBAP), the NOS inhibitor L-NAME, and several agents that impair electron flux through the ETS; menadione, sodium azide (NaN3), and 2,3-butanedione monoxime (BDM). Drugs were given before or during cold perfusion. ROS measured by DHE was inversely proportional to temperature between 37°C and 3°C. We found that perfusion at 17°C increased DHE 3-fold vs. at 37°C; this was reversed by MnTBAP, but not by L-NAME or BDM, and was markedly augmented by menadione and NaN3. Perfusion at 17°C also increased myocardial and effluent diTyr (ONOO-) by 2-fold. L-NAME, MnTBAP, or BDM perfused at 37°C before cooling, or during 17°C perfusion abrogated, whereas menadione and NaN3 again enhanced the cold-induced increase in ROS. Our results suggest that hypothermia moderately enhances O2.- generation by mitochondria while O2.- dismutation is markedly slowed. Also the increase in O2.- during hypothermia reacts with available NO. to produce ONOO-, and drug-induced O2 .- dismutation eliminates the hypothermia-induced increase in O2.-.




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