Materials and methods chemic samples were then collected, followed by two Results

156 J 21 depletion can also lead to an increase in intracellular Ca Penthrane. Body temperature was controlled at 378C with with activation of calcium-dependent enzymes, including a rectal probe and an abdominal heating pad. One femoral phospholipases and proteases. Endogenous inhibitors and artery was cannulated for measurement of arterial blood activators of proteases, which are phosphoproteins, are pressure and to obtain arterial blood samples for pH and present in cells and a change in their phosphorylation blood gas measurements. Cerebral ischemia was induced status during ATP depletion could enhance the activity of by coagulating the vertebral arteries via the alar foramina nonlysosomal proteases. and traction on loops placed around the carotid arteries. A challenge to the acidotic hypothesis of ischemic injury The dorsal surfaces of both cerebral hemispheres were arose from the observation that at the pH typically exposed and, after reflection of the dura mater, oval generated in ischemic brain, NMDA receptor-mediated cortical windows suspended in flexible mounting brackets currents were almost entirely abolished [38,39]. In that were gently placed on both cortices. The dorsal surface of NMDA-activated receptors are considered to be amongst the head around the windows was covered with a stabiliz- the primary mediators of excitotoxic ischemic injury [8], ing gel of 3 agar in artificial cerebrospinal fluid aCSF. 1 1 these findings suggested that acidosis could actually limit The aCSF contained: Na , 155.8 mEq l; K , 2.95 mEq l; 21 21 2 the extent of excitotoxic injury. Mild acidosis was sub- Ca , 2.5 mEq l; Mg , 1.85 mEq l; Cl , 141.13 mEq l; 2 sequently shown to protect hippocampal and cortical HCO , 22 mEq l; urea, 40.2 mg dl which had been 3 cultures from ischemic-like conditions [12,38] and cortical equilibrated with 95 nitrogen, 5 carbon dioxide pH and cerebellar cultures against glutamate toxicity [2,15]. 7.3. Monopolar EEG electrodes were placed on the Furthermore, brain acidosis induced by hypercarbic venti- cortical surface within each window. EEGs and arterial lation attenuated focal ischemic injury in vivo [36] and blood pressure were recorded on a Grass polygraph. Two hypoxic-ischemic damage to the immature rat brain [42]. hundred ml of warmed 378C aCSF were pipetted into Sapolsky et al. [35] subsequently referred to the potential each window at 10-min intervals, after removal of the for acidosis to be neuroprotective under certain circum- previous superfusate sample with Pasteur pipettes. The stances as a ‘paradoxical wrinkle’. temperature of fluids within the windows was maintained The term ‘pH paradox’ was used by Bond et al. [4] to at 378C using a heat lamp, and the windows were then account for the protective action of intracellular acidosis closed with black plastic covers to protect the superfusate on cultured cardiac myocytes exposed to simulated is- contents from light degradation. chemia, proposing instead that the injury actually occurs Cerebral ischemia was elicited by occluding the carotid during the return to normal pH. These investigators arteries for 20 min. Induction of cerebral ischemia was suggest that although favorable conditions for the activa- manifested by the rapid development of an isoelectric EEG tion of degradative enzymes such as phospholipases and trace from both cortices. After 20 min the carotid snares proteases exist during ischemia, they are inhibited by the were withdrawn and reperfusion verified by both the initial acidotic conditions [5,10]. During reperfusion, the inhibi- sharp decline in arterial blood pressure and visual inspec- tion is released as intracellular pH recovers, with damage tion of the pial vasculature within the windows. Most to mitochondrial and plasma membranes initiating necrotic animals ceased to respire spontaneously at some point or apoptotic processes [21]. Delays in the recovery of during the period of ischemia and were ventilated me- intracellular pH can be instigated in myocytes using chanically. 1 1 inhibitors of Na H exchangers, including di- Results from three groups of rats are presented in this methylamiloride and HOE 694 [21] or, in the case of report. One group n59 comprised the control ischemic neuronal tissue cultures, dimethylamiloride or harmaline animals in which the superfusates were aCSF10.05 [44]. In both instances, powerful protective effects of dimethylsulfoxide vehicle for EIPA. The cerebral cortices maintaining intracellular acidosis were observed. of the second group n56 were exposed to EIPA 25 mM The present experiments were designed to evaluate in 0.05 dimethylsulfoxide aCSF for 15 min after the 1 1 whether the potent and selective inhibitor of Na H completion of superfusate collection 2, and 35 min prior to 1 1 exchange, 5-N-ethyl-N-isopropyl-amiloride EIPA [43], the onset of ischemia. The Na H exchange inhibitor would block phospholipase activation, measured by the was then present in all subsequent superfusate samples. efflux of free fatty acids FFAs, in the ischemic re- For both groups, a standard protocol of superfusate sample perfused rat cerebral cortex as a consequence of its collections was followed. After two basal 10 min aCSF stabilizing action on the acidotic intracellular pH. collections the animals were exposed to either aCSF or aCSF plus EIPA for 15 min during which the window contents were replaced three times. Two more pre-is-

2. Materials and methods chemic samples were then collected, followed by two

ischemia samples 20 min of ischemia and four reperfu- Male Sprague–Dawley rats Charles River, 275–325 g sion samples 40 min. The third group of rats n56 were anesthetized with halothane and, after insertion of a differed from the first group in that the period of ischemia tracheal cannula, were maintained with methoxyflurane was extended to 30 min three superfusate collections J .W. Phillis et al. Brain Research 884 2000 155 –162 157 followed by 40 min of reperfusion. Superfusate samples EIPA-treated animals and 1 6 of the 30-min ischemia rats, were ejected into chilled microvials, centrifuged at 12003 respectively. g and stored at 2208C. HPLC assays of perfusate-free fatty acid contents were initiated within a few hours using 3.2. Superfusate glucose and lactate levels previously published procedures [34]. Superfusate glucose and lactate levels were measured with a YSI Select Mean basal glucose 4.4 mg dl; |240 mM and lactate Biochemistry Analyzer Version 2.50D Yellow Springs, 2.0 mg dl; |225 mM levels in cerebral cortical super- OH. fusates were comparable in the three groups of animals Statistical differences for free fatty acid, glucose and Figs. 1 and 2. Superfusion of EIPA did not significantly lactate levels between control and EIPA-treated animals affect basal levels of either compound Fig. 1; collections were determined by a two-tailed Student’s t-test for each 3 and 4. During ischemia, superfusate glucose levels collection period. A P,0.05 was accepted as denoting a declined rapidly to values approaching detection limits and statistically significant difference. All animal procedures reperfusion was associated with marked increases in were approved by the University Animal Care Committee and were in full accordance with the National Institutes of Health Guide for the Care and Use of Laboratory Animals.

3. Results

3.1. Physiological parameters Although there were significant declines in pH and PaO 2 levels, and increases in PaCO levels post-ischemia there 2 were no statistically significant differences between the three groups of animals in the physiological parameters of mean arterial blood pressure, blood gases and pH values in arterial blood samples recorded either prior to EIPA administration and ischemia or after 40 min of reperfusion Table 1. In all groups, the EEG became isoelectric within a few seconds of the onset of ischemia. Some recovery of EEG activity became apparent in 4 9 control animals, 3 6 Table 1 Mean arterial blood pressure MABP and arterial blood gases in control and EIPA 25 mM-treated rats prior to 20 min or 30 min of ischemia and a,b after 40 min of reperfusion Group Pre-ischemia Post-ischemia MABP 20 min control 93.661.2 92.362.7 EIPA 96.061.6 90.060.8 30 min ischemia 93.362.1 93.062.4 pH 20 min control 7.4060.01 7.3260.02 EIPA 7.4060.01 7.3260.01 Fig. 1. Effect of 5-N-ethyl-N-isopropyl-amiloride EIPA, 25 mM, an 30 min ischemia 7.4260.01 7.3060.03 1 1 inhibitor of Na H exchange, on basal and ischemia-evoked four-vessel occlusion levels of glucose and lactate in cerebral cortical superfusates. PaCO 20 min control 35.661.2 42.262.0 2 The line plots show the time course of changes in cortical superfusate EIPA 37.060.9 46.062.8 levels of these compounds before, during and after a 20-min period of 30 min ischemia 35.861.6 46.262.2 four-vessel cerebral ischemia collections 5 and 6, open box. Effluxes of glucose and lactate are compared in control 0.05 DMSO in aCSF; d PaO 20 min control 94.963.7 76.163.8 2 and EIPA 25 mM, applied topically; h treated animals. EIPA was EIPA 89.863.4 74.761.3 administered for 15 min prior to the start of collection 3 and was present 30 min ischemia 92.862.8 73.866.2 in all subsequent collections. Statistically significant differences between a All values are means6S.E.M. n59 for control rats 20 min ischemia; 6 superfusate glucose and lactate levels in control and EIPA-treated animals for the EIPA group and 6 for the 30-min ischemia group. were determined by a two-tailed Student’s t-test; P,0.05. Significant b o Significance values in comparison with pre-ischemic levels: P,0.05, increases in glucose or lactate levels above basal values; P,0.05, oo ooo P,0.01. P,0.01, P,0.001. 158 J 3.3. Free fatty acid efflux Basal extracellular levels of FFA in cortical superfusates of the control group were: arachidonic acid, 103611 mg l 329635 nM; myristic acid, 172616 mg l 755670 nM; linoleic acid, 213618 mg l 760664 nM; palmitic acid, 499635 mg l 19516137 nM and oleic acid, 297639 mg l 10526138 nM. During a 20-min ischemia, the levels of arachidonic acid rose slightly, whilst those of the other FFAs were not affected Fig. 3. Following reperfu- sion there were significant increases in the superfusate levels of all of the FFAs, with the exception of myristic acid. Application of EIPA 25 mM reduced basal levels of myristic acid, but not those of the other FFAs, and there were significant reductions in the ischemia reperfusion evoked effluxes of arachidonic and linoleic acids and non-significant reductions in superfusate levels of palmitic and oleic acids in comparison with their control ischemia reperfusion evoked efflux Fig. 3. The small increases in arachidonic, linoleic, palmitic and oleic acids during reperfusion were not significant. Extending the duration of the cerebral ischemia of rats in the third group to 30 min resulted in decreases in the efflux of linoleic, palmitic and oleic acids during ischemia with a marked increase in the efflux of arachidonic, linoleic, palmitic and oleic acids again being clearly coincident with reperfusion Fig. 4.

4. Discussion