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Effects of the Hydroxyl Radical Scavenger, Dimethylthiourea, on Peripheral Nerve Tissue Perfusion, Conduction Velocity and Nociception in Experimental Diabetes

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Effects of the Hydroxyl Radical Scavenger, Dimethylthiourea, on Peripheral Nerve Tissue Perfusion, Conduction Velocity and Nociception in Experimental Diabetes Diabetologia &2001) 44: 1161±1169 Ó Springer-Verlag 2001 Effects of the hydroxyl radical scavenger, dimethylthiourea, on peripheral nerve tissue perfusion, conduction velocity and nociception in experimental diabetes N. E.Cameron, Z.Tuck, L.McCabe, M.A.Cotter Department of Biomedical Sciences, Institute of Medical Sciences, University of Aberdeen, Scotland, UK Abstract for motor conduction was 9 mg ´ kg±1 ´ day±1. Mechan- ical and thermal nociceptive sensitivities were 18.9% Aims/hypothesis. Increased oxidative stress has been and 25.0% increased by diabetes, respectively, indi- linked to diabetic neurovascular complications, cating hyperalgesia which was 70% reduced by dim- which are reduced by antioxidants. Our aim was to ethylthiourea. Sciatic endoneurial and superior cervi- assess the contribution of hydroxyl radicals to early cal ganglion blood flows were 51.2% and 52.4% re- neuropathic changes by examining the effects of duced by diabetes and there was an approximately treatment with the specific scavenger, dimethylthiou- 80% improvement with treatment. rea, on nerve function and neural tissue blood flow in Conclusion/interpretation. Hydroxyl radicals seem to diabetic rats. make a major contribution to neuropathy and vascul- Methods. Diabetes was induced by streptozotocin. opathy in diabetic rats. Treatment with the hydroxyl Measurements comprised sciatic nerve motor and scavenger, dimethylthiourea, was highly effective. saphenous nerve sensory conduction velocity. Re- The data suggest that the development of potent hy- sponses to noxious mechanical and thermal stimuli droxyl radical scavengers suitable for use in man were estimated by Randall-Sellito and Hargreaves could markedly enhance the potential therapeutic tests respectively. Sciatic nerve and superior cervical value of an antioxidant approach to the treatment of ganglion blood flow were measured by hydrogen diabetic neuropathy and vascular disease. [Diabeto- clearance microelectrode polarography. logia &2001) 44: 1161±1169] Results. Eight weeks of diabetes reduced motor and sensory conduction velocity by 19.9% and 15.7% re- Keywords Neuropathy, pain, nerve conduction, blood spectively, and these were completely corrected by flow, autonomic ganglion, oxidative stress, hydroxyl 2 weeks of dimethylthiourea treatment. The ED50 radical, dimethylthiourea, diabetic rat. Oxidative stress contributes to the neural and vascu- diminished and lipid peroxidation markers are in- lar complications of diabetes [1, 2]. For nerve, antiox- creased [2, 3]. Vascular endothelium is also vulnera- idant protection is impaired; glutathione content is ble to oxidative stress, including the nitric oxide sys- tem [1, 4]. Treatment with free radical scavengers in- Received: 13April 2001 and in revised form: 28 May 2001 creases nerve conduction velocity &NCV), blood flow and regenerative capacity [3, 5±9] and protects Corresponding author: Dr. Norman E.Cameron, Diabetic endothelial function [10±12]. The vasa nervorum and Complications Lab, Department of Biomedical Sciences, Insti- the nitric oxide system in nerve complications is im- tute of Medical Sciences, University of Aberdeen, Foresterhill, portant in that antioxidant effects on function are Aberdeen AB25 2ZD, Scotland, UK. E-mail: n.e.cameron largely abolished by nitric oxide synthase inhibitor @abdn.ac.uk Abbreviations: DMTU, dimethylthiourea; NCV,nerve conduc- co-treatment in experimental models [13]. It has tion velocity; ROS, reactive oxygen species; SCG, superior cer- been noted, however, that extremely high doses of vical ganglion natural scavengers such as vitamins E or C are re- 1162 N. E.Cameron et al.: Hydroxyl radicals, nerve function and perfusion quired to correct nerve and vascular dysfunction [6, investigation, also an intervention study, measurement of re- 10] possibly because they do not optimally scavenge sponses to noxious mechanical and thermal stimulation were the most important reactive oxygen species &ROS), made to assess function of pain small-fibre systems before and after 2 weeks of treatment, followed by measurement of supe- or because they do not distribute well in the appropri- rior cervical ganglion &SCG) blood flow. ate cellular or body compartment. Dimethylthiourea dissolved in sterile saline &Sigma, Poole, Several potential sources of ROS have been sug- Dorset, UK) was injected daily intraperitoneally, for all studies gested; superoxide could be generated by endothelial except the dose-response determination, the dose was set at NAD&P)H oxidase, nitric oxide synthase, mitochon- 100 mg/kg. drial respiratory chain inefficiency, or xanthine oxi- dase mechanisms [1, 14]. Autoxidation reactions of Sciatic nerve and superior cervical ganglion blood flow. Rats were anaesthetised with thiobutabarbital &Astra-Zeneca; glucose and its metabolites and advanced glycation 50±100 mg/kg), by intraperitoneal injection. The trachea was could be important sources of ROS [15]. The highly cannulated for artificial ventilation. A cannula in the right ca- reactive hydroxyl radical can be produced from su- rotid artery was used to monitor mean systemic blood pres- peroxide and hydrogen peroxide by the Haber-Weiss sure. Core temperature was monitored and regulated at 37 to reaction and from peroxide by the transition metal 38C, using a rectal probe and radiant heat. catalysed Fenton reaction. Superoxide readily reacts Blood flow was estimated by microelectrode polarography and hydrogen clearance as described [22]. For peripheral nerve with nitric oxide to give peroxynitrite, which decom- recordings, the sciatic nerve was exposed between sciatic notch poses to liberate hydroxyl radicals [16]. For vascular and knee. For ganglion recordings, the left SCG was located in and nerve complications it is not clear whether the su- the vicinity of the carotid bifurcation. In both cases, the skin peroxide itself and its interaction with nitric oxide is around the incision was used to form a pool that was filled the important pathophysiological step or whether a with paraffin oil maintained at 35 to 37C by radiant heat dur- peroxide or hydroxyl radical mechanism is more rele- ing measurements. A glass-insulated platinum microelectrode vant. Studies with metal chelators have emphasised was inserted into the appropriate neural structure and polaris- ed at 0.24 V according to a subcutaneous reference electrode. the importance of the latter process for neurovascular 10% H was added to the inspired gas, the proportions of O dysfunction [9, 17±19], however, interpretation is 2 2 and N2 were adjusted to 20% and 70% respectively. When complicated because other potential transition metal the H2 current recorded by the electrode had stabilised, indi- catalysed mechanisms also enhance the glycoxidation cating equilibrium with arterial blood, the H2 supply was shut process [20, 21]. Therefore, to further delineate the off and N2 delivery was increased appropriately. The H2 clear- ROS mechanisms responsible for neurovascular dys- ance curve was recorded until baseline, the latter was defined as no systematic decline in electrode current over 1 min for function, the effect of treatment with the hydroxyl SCG or 5 min for sciatic nerve recordings. This procedure was radical scavenger, dimethylthiourea &DMTU), on then repeated at another site. Clearance curves were digitised measures of large and small nerve fibre function and and monoexponential or biexponential curves were fitted off- peripheral nervous tissue perfusion were examined line by computer using non-linear regression, the Marquardt in diabetic rats. algorithm and the least squares method for optimising good- ness-of-fit &Prism, Graphpad, San Diego, Calif., USA). The slow exponent was considered to reflect nutritive flow [22]. Materials and methods Nerve function tests. Rats were anaesthetised with urethane &1±1.5 g/kg, dissolved in saline) by intraperitoneal injection Experiments were carried out in accordance with regulations for the preventive study, or with thiobutabarbital in the rever- specified by the United Kingdom `Animal Procedures Act, sal study when blood flow was measured. The sciatic nerve 1986' and the National Institutes of Health `Principles of Labo- was exposed between sciatic notch and knee and motor NCV ratory Animal Care, 1985 revised version'. was measured as described previously [23] in the nerve branch to the tibialis anterior muscle, which is representative of the Experimental groups and diabetes induction. Male Sprague- whole sciatic nerve in terms of susceptibility to diabetes and Dawley rats &Aberdeen University colony), 19 weeks old at treatment effects. Saphenous nerve sensory NCV was mea- the start of the study were used. Diabetes, induced by intra- sured between the groin and calf. Rectal and near nerve tem- peritoneal streptozotocin &Astra-Zeneca Pharmaceuticals, peratures were monitored and regulated between 36.5 and Macclesfield, Cheshire, UK) at 40 to 45 mg/kg freshly dis- 37.5C with radiant heat. solved in sterile 0.9% saline solution, was verified 24 h later Nociceptive thresholds for mechanical stimulation were by estimating hyperglycaemia and glycosuria &Visidex II and measured by the Randall-Sellito test [24] and latencies for Diastix; Ames, Slough, UK). Blood samples were taken from withdrawal reflexes to noxious thermal stimulation of the foot the tail vein to measure plasma glucose &GOD-Perid method; were estimated by the Hargreaves plantar test [25] using com- Boehringer Mannheim, Mannheim, Germany) just before fi- mercially available equipment
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