Superoxide dismutase activity and zinc and copper concentrations in Parkinson s disease
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1 Pathophysiology 7 (2000) Superoxide dismutase activity and zinc and copper concentrations in Parkinson s disease Pelin Aribal Kocatürk a, *, M. Cenk Akbostanci b, Funda Tan b,güzin O zelçi Kavas a a Department of Pathophsiology, Faculty of Medicine, Ankara Uni ersity, Sihhiye, Ankara, Turkey b Department of Neurology, Faculty of Medicine, Ankara Uni ersity, Sihhiye, Ankara, Turkey Accepted 2 February 2000 Abstract Although several hypotheses are currently being investigated the cause of Parkinson s disease (PD) is still unknown. The aim of this study was to determine red cell copper/zinc-superoxide dismutase (Cu/Zn-SOD) activity and copper and zinc concentrations both in plasma and in red cell in PD. In this preliminary assay, 30 patients with PD the mean age of 64 were studied. Additionally, a second group of older individuals without PD mean age of 61, were recruited to the study. The patient group was compared with the other group according to their red cell Cu/Zn-SOD activities, and plasma and red cell copper, zinc concentrations. Red cell Cu/Zn-SOD activity was measured spectrophotometrically while plasma and red cell copper, zinc concentrations were determined by atomic absorption spectrophotometer. The results were analysed by Student t-test statistically. The results showed that red cell Cu/Zn-SOD activities and red cell copper and zinc and also plasma copper concentrations of the PD patients increased compared to older individuals without PD. These findings suggested that possibility of oxidative stress in PD was reflected on the blood including the red cell and plasma parameters Elsevier Science Ireland Ltd. All rights reserved. Keywords: Parkinson s disease; Red cell superoxide dismutase; Zinc; Copper 1. Introduction Parkinson s disease (PD) is a neurodegenerative disorder that is characterized by a loss of nigrostriatal dopaminergic neurons in the substantia nigra pars compacta (SNc) and a consequent reduction in striatal dopamine (DA) [1]. The cell degeneration in PD depends on several factors as, increased reactive oxygen metabolites (ROMs), mitochondrial energy crisis, and exogenous and/or endogenous neurotoxins [2]. There are reports on increased production of ROMs resulting from increased DA turnover and metabolism, altered antioxidant defence system and altered trace element concentrations, leading to neurodegeneration in PD [1,3 5]. Local inflammation in brain tissue may be another source of ROMs while leading several cytokine release which alters the concentrations of copper and zinc intra and extracellularly [6]. Although it remains unclear whether ROMs are the primary factors in the etiology of PD, there is no doubt that the generated ROMs enhance and promote the pathogenicity of the disease. Because of the difficulty in determining the alterations and pathological processes occurred in brain tissue, the effects of these processes which might be reflected on plasma and red cells are investigated in this study. Therefore, the purpose of this study was to determine red cell copper/zinc-superoxide dismutase (Cu/Zn-SOD) activity and copper and zinc concentrations both in plasma and in red cell in PD. This work was presented at the Third International Congress of Pathophysiology, Lahti, Finland, 28 June 3 July, * Corresponding author. Ankara U niversitesi Tip Fakültesi, Fizyopatoloji Bilim Dali, Morfoloji Bínasi, Sihhiye, Ankara, Turkey. Tel.: /230; fax: Material and methods Thirty patients with idiopathic PD and without any other chronic diseases as essential hypertension and /00/$ - see front matter 2000 Elsevier Science Ireland Ltd. All rights reserved. PII: S (00)
2 64 P.A. Kocatürk et al. / Pathophysiology 7 (2000) diabetes mellitus were selected for this study and their average age was 64. A second group of 24 individuals who were in good general health and without PD and whose average age was 61 were included to the study. The blood was drawn always at the same time from the forearm veins and was put in the heparinized tubes, the plasma was kept in polypropylene tubes and each sample was studied daily. Red cell Cu/Zn-SOD activity was evaluated by spectrophotometry. The principle of this method was percent inhibition of nitro blue tetrazolium reduction in the presence of Cu/Zn-SOD activity [7]. Copper and zinc concentrations in the plasma and red cells were determined by atomic absorption spectrophotometry according to Perkin-Elmer s principles [8]. All the laboratory procedures were performed at pathophysiology department laboratories. The results were analyzed by Student t-test in the Department of Biostatiscs, University of Ankara Faculty of Medicine. The results of this study are presented as means S.D. 3. Results The results of this study were given in Figs The mean value of red cell SOD activity of patient group ( U/g Hb) was found to be increased as compared to the older individuals without PD ( U/g Hb) (P 0.05). The mean values of blood parameters of the older individuals without PD were as follows: plasma copper concentration was g/dl, the red cell copper concentration was g/ml, plasma zinc concentration was g/dl, red cell zinc concentration was g/ml. There were also a marked increase in red cell zinc ( g/ml) (P 0.001), copper ( g/ml) (P 0.01) and also in plasma copper ( g/dl) (P 0.01) concentrations when compared to the older individuals without PD. Plasma zinc concentration showed mild decrease ( g/dl) in PD patients when compared to the individuals without PD but these alterations were not statistically significant. 4. Discussion The relation of red cell Cu/Zn-SOD activity with red cell and plasma copper and zinc concentrations of patients with PD would be an interesting concept since these parameters might reflect the alterations produced in brain tissue during the possible oxidative stress in PD. Another interesting point of view was the absence of any data in literature about both red cell Cu/Zn-SOD activity and blood copper and zinc concentrations in PD. Fig. 1. The Red cell superoxide dismutase activity. The results are presented as means S.D.
3 P.A. Kocatürk et al. / Pathophysiology 7 (2000) Fig. 2. Plasma copper concentration. The results are presented as means S.D. Fig. 3. The red cell copper concentration. The results are presented as means S.D.
4 66 P.A. Kocatürk et al. / Pathophysiology 7 (2000) Fig. 4. Plasma zinc concentration. The results are presented as means S.D. Fig. 5. The red cell zinc concentration. The results are presented as means S.D.
5 P.A. Kocatürk et al. / Pathophysiology 7 (2000) There are increasing evidence for the upregulation of both Cu/Zn-SOD and manganese dependent SOD activities in brain tissue of PD patients [3,4,9]. On the other hand, there are also studies on cerebrospinal fluid manganese dependent SOD activity reporting an increase in PD [10]. Similar results were reported for both plasma Cu/Zn-SOD, manganase dependent SOD in various neurodegenerative diseases [10 12]. All these reports suggested that increases in SOD activities might be a protective mechanism against the risk from ROMs damage. Our results also supported their suggestions. Trace element alterations are also an important feature in PD. There is an increased prooxidant effect of metal ions in PD [5]. Although copper is essential for the antioxidant function of Cu/Zn-SOD it may act as a prooxidant for instance towards brain lipids when present in low molecular mass loosely bound complexes [5,13]. There are numerous reports on the SNc copper and zinc concentrations and one report about cerebrospinal fluid copper concentration but no data on blood values of copper and zinc in PD [5,14]. Therefore, both plasma and red cell copper and zinc concentrations given in this study might reflect the copper and zinc status of blood during this disease. Both plasma and red cell copper concentrations of PD patients were increased compared to older individuals without PD in this study. There have been reports on a localized inflammatory response occuring in the brains of PD patients. For this reason, in early phase of the disease, ceruloplasmin concentration specially in SNc has been found markedly elevated [15]. Similar elevations are demonstrated in some cytokine concentrations, particularly TNF-, IL-1 and IL-6 [2,16]. These cytokines, by inducing metal ion concentration changes, may contribute to the oxidative stress as well. The alterations observed in blood copper and zinc concentrations might be the result of these processes. Another trace element, zinc, may have an antioxidant role in PD. Increased nigral levels of zinc have been reported in PD [14]. Since there is a localized inflammation and therefore increased release of some cytokines, including IL-6, zinc may accumulate intracellularly during the disease [6]. Increased concentration of red cell zinc found in PD group, may be considered as the result of increased cellular uptake of zinc from the plasma, which is corresponding to the slightly decreased plasma concentrations. 5. Conclusion The results of this study on blood may contribute to the literature data, reporting the suggestions on the increased oxidative stress and corresponding copper and zinc concentration changes in brain tissue in PD. Acknowledgements The authors gratefully acknowledge the excellent laboratory work of Demet Büyükkagnici from the Pathophysiology Department and Biostatisticians of the Medical Faculty. References [1] C.W. Olanov, G.V. Arendash, Metals and free radicals in neurodegeneration, Curr. Opin. Neurol. 7 (1994) [2] T. Kondo, Parkinson s disease and free radicals, Ann. NY Acad. Sci. 786 (1996) [3] P. Jenner, Oxidative damage in neurodegenerative disease, Lancet 344 (1994) [4] S. Fahn, G. Cohen, The oxidant stress hypothesis in Parkinson s disease: evidence supporting it, Ann. Neurol. 32 (1992) [5] H.S. Pall, A.C. Williams, Raised cerebrospinal-fluid copper concentration in Parkinson s disease, Lancet 2 (1987) [6] L. Kushner, Regulation of the acute phase response by cytokines, Perspect. Biol. Med. 36 (1993) [7] C.C. Winterbourn, R.E. Hawkins, M. Brain, The estimation of red cell superoxide dismutase activity, J. Lab. Clin. Med. 85 (1975) [8] E. Perkin, Analysis of serum determination of copper and zinc (BC-8). Analytical Method for Atomic Absorption Spectrophotometry, Perkin-Elmer, Norwalk, Connecticut, [9] J.B. Lohr, Oxygen radicals and neuropsychiatric illness, Arch. Gen. Psych. 48 (1991) [10] E. Yoshida, K. Mokuno, S.I. Aoki, Cerebrospinal fluid levels of superoxide dismutases in neurological diseases detected by sensitivie enzyme immunoassays, J. Neurol. Sci. 124 (1994) [11] G.A. Erausquin, E. Costa, I. Hanbauer, Calcium homeostasis, free radical formation, and tropic factor dependence mechanisms in Parkinson s disease, Pharmacol. Rev. 46 (1994) [12] P.H. Evans, Free radicals in brain metabolism and pathology, Br. Med. B 49 (1993) [13] J.A. Swain, V. Darley-Usmar, J.M.C. Gutteridge, Perxynitrite releases copper from caeruloplasmin: in implications for atherosclerosis, FEBS Lett. 342 (1994) [14] D.T. Dexter, P. Jener, A.H.V. Schapira, C.D. Marsden, Alterations in levels of iron, ferritin, and other trace metals in neurodegenerative diseases affecting the basal ganglia, Ann. Neurol. Suppl. 32 (1992) S94 S100. [15] D.A. Loeffler, P.A. LeWitt, P.L. Juneau, et al., Increased regional brain concentrations of ceruloplasmin in neurodegenerative disorders, Brain Res. 738 (1996) [16] J.B. Gupta, M. Prasad, Platelet-activating-factor-induced changes in cardiovascular function and oxyradical status of myocardium in presence of the PAF antagonist CV-6209, Angiology 45 (1994)
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