Effect of prenatal copper exposure on the central dopaminergic system in adult rats
 
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1
Katedra i Zakład Farmakologii Śląskiego Uniwersytetu Medycznego w Katowicach
 
2
Katedra i Zakład Medycyny i Epidemiologii Śląskiego Uniwersytetu Medycznego w Katowicach
 
3
Wyższa Szkoła Planowania Strategicznego w Dąbrowie Górniczej
 
 
Corresponding author
Ryszard Brus   

Katedra i Zakład Farmakologii SUM, 41-808 Zabrze, ul. H. Jordana 38, tel./faks +(48 32)272 26 83
 
 
Ann. Acad. Med. Siles. 2009;63:7-14
 
KEYWORDS
ABSTRACT
Background:
The eff ect of prenatal exposition of rats with copper on its level in the newborns’ organs and central dopaminergic system activity in adult rats was examined.

Material and Methods:
Pregnant rats during entire time of pregnancy drank water with cupprum sulfuricum (CuSO4) where concentration of metal was 100 ppm. Control rats drank the water only without cuprum. After delivery water with metal was substituted with water only, and newborns stayed with their mothers till 21st day of life, then separated. In newborn copper content was estimated in the brain, liver and kidney. In adult rats the level of biogenic amines was measured in the brain and some behavioral studies were performed such as oral activity, stereotyped and yawning behavior, using central dopamine receptor agonists (SKF 38393, apomorphine, 7-OH-DPAT).

Results and Conclusion:
Exposition of rats during intrauteral development (prenatal) with copper caused significant increase concentration examined metal in the brain, liver and kidney of newborn rats. In adult rats signifi cant decrease of dopamine in the striatum was noticed in the rats pretreated with copper. Beside increase reactivity of the central dopamine D1 receptor reactivity was observed, and manifested by increased oral activity after SKF 38393 and stereotyped behavior after apomorphine apply. Additionally decreased reactivity of the central dopamine D3 receptor was manifested by decreased yawning behavior after 7-OH-DPAT injection. From above we concluded that copper can be one of the environmental agent which can affected of the central dopaminergic system in mammalians

 
REFERENCES (52)
1.
Felińska W., Brus R., Szkilnik R., Rykaczewska M., Plech A., Kostrzewa R.M., Frydrych J. Cadmium modulates reactivity of central dopamine receptors in rats prenatally exposed to ethanol. Pol. J. Environ. Stud. 1995; 1: 31-36.
 
2.
Brus R., Szkilnik R., Nowak P., Konecki J., Głowacka M., Kasperska A., Oświęcimska J., Sawczuk K., Shani J. Prenatal exposure of rats to lead, induce changes in the reactivity of the central dopaminergic, serotoninergic and muscarinic receptors but in glucose uptake in their off spring. Pharmacol. Rev. Comm. 1997; 9: 299-310.
 
3.
Szkilnik R., Nowak P., Winiarska H., Durczok A., Małecki S., Rycerska A., Brus R., Shani J. Eff ect of zinc on the reactivity of the central dopaminergic receptors in rats, prenatally expose to lead. Pharmacol. Rev. Comm. 2001; 11: 319-328.
 
4.
Brus R., Szkilnik R., Konecki J., Stępień M., Małecki S., Kuballa G., Mengel K., Shani J. Prenatal exposure of rats to manganese: changes in reactivity of their central dopaminergic, serotoninergic and muscarinic receptors, but not of glucose uptake in their adult off springs. Pharmacol. Rev. Comm. 2002; 12: 9-24.
 
5.
Kiszka W., Szkilnik R., Brus R., Nowak P., Konecki J., Durczok A., Mengel K., Shani J. Prenatal exposure of rats to mercury induce changes in central dopaminergic activity and glucose uptake by their off - spring. Pharmacol. Rev. Comm. 2002; 12: 101-108.
 
6.
Kwieciński A., Szkilnik R., Nowak P., Kliber M., Drosik M., Noras Ł., Niwiński J., Gorzałek J., Brus R. Rekatywność ośrodkowych receptorów dopaminowych u szczurów narażonych na selen w okresie prenatalnym. Ocena za pomocą metod behawioralnych. Ann. Acad. Med. Siles. Danks D.M., Stevensen B.J., Campbell P.E., Gillespie J.M., Walker-Smith J. Menkes Kinky-hair syndrome. Lancet 1972; 1: 1100-1103.
 
7.
Goyer R.A. Toxic eff ects of metal. W: Admur M.O., Doul J., Klaassen C.D. red. Casarett and Doull’s Toxicology. The Basic Science of Poisons. Pergamon Press, New York 1991: 623-680.
 
8.
Danks D.M., Stevensen B.J., Campbell P.E., Gillespie J.M., Walker-Smith J. Menkes Kinky-hair syndrome. Lancet 1972; 1: 1100-1103.
 
9.
Goka T.J., Stevensen R.E., Hetteran P.M., Howell R.R. Menkes disease: a biochemical abnormality in cultured human fi broblast. Proc. Natl. Acad. Sci. (USA) 1976; 73: 604-606.
 
10.
Brewer G.J. Practical recommendations and new therapies for Willson’s disease. Drugs 1995; 3: 240-249.
 
11.
Jabłońska-Kaszewska I., Dąbrowska E., Ozibłowski A. Wilson’s disease impresonal material disturbances in hoemostasis. Pol. Tyg. Lek. 1995; 50: 79-81.
 
12.
Samuele A., Mangiagalli A., Armentero M.T., Fancellu R., Bazzini E., Vairetti M., Ferrigno A., Pichelmi P., Nappi G., Blandini F. Oxidative stress and pro-apoptotic conditions in a rodent model of Wilson’s disease. Biochem. Biophys. Acta 2005; 1741: 325-330.
 
13.
Bush A.I. The metallobiology of Alzheimer’s disease. Trends Neurosci. 2003; 26: 207-214.
 
14.
Mulhaup G., Schlicksupp A., Hesse L., Beher D., Ruppert T., Masters C.L., Beyreuther K. The amyloid precursor protein of Alzheimer’s disease in the reduction of copper (II) to copper (I). Science 1996; 271: 1406-1409.
 
15.
Huang X., Cuajungco M.P., Atwood C.S., Hartshorn M.A., Tyndal J.D., Harrison G.R., Stokes K.C., Leopold M., Multhaup G., Goldstein L.E., Scarpa R.C., Sanders A.J., Lim J., Moris R.D., Glabe C., Bowden E.F., Masters C.L., Fairlie D.P., Tanzi R.E., Bush A.I. Cu(II) potentiation of Alzheimer neurotoxicity. Correlation with cell-free hydrogen peroxide production and metal reduction. J. Biol. Chem. 1999; 274: 37111-37116.
 
16.
Tobuer B.J., Turnbull S., El-Agnaf O.M., Allsop D. Formation of hydrogen peroxide and hydroxyl radicals from A (beta) and alfa synuclein as a possible mechanism of cell death in Alzheimer’s disease and Parkinson’s disease. Free Radic. Biol. Med. 2002; 32: 1076-1083.
 
17.
Johnson S. Micronutrient accumulation and depletion in schizophrenia, epilepsy, autism and Parkinson’s disease? Med. Hypothesis 2001; 56: 641-645.
 
18.
Paris I., Dagnino-Subiobre A., Marcelain K., Bennett L.B., Caviedes P., Caviedes R., Azar C.O., Segura-Aguilar J. Copper neurotoxicity is ependent on dopaminemediated copper uptake and one-electron reduction of aminochronic in a rat substantia nigra neuronal cell line. J. Neurochem. 2001; 77: 519-529.
 
19.
Woggoner D.J., Bartnikas T.B., Gitlin J.D. The role of copper in neurodegenerative disease. Neurobiol. Dis. 1999; 6: 221-230.
 
20.
Hozelhoff -Roelfzemia W.H., Roelofsen A.M., Leene W., Copius Peereboom-Stegeman J.H.J. Eff ect of cadmium exposure during pregnancy on cadmium and zinc concentration in neonatal liver and consequences for the off spring. Arch. Toxicol. 1989; 63: 38-42.
 
21.
Magnusson O., Nilson L.B., Westerland D. Simultaneous determination of dopamine, DOPAC and homovanillic acid. Direct injection of supernatants from brain tissue homogenates in a liquid chromatography-electrochemical detection system. J. Chromatogr. 1980; 221: 237-247.
 
22.
Whiteside P. Atomic Absorption. Pye Unicam Ltd, Cambridge, UK 1976.
 
23.
Brus R., Kostrzewa R.M., Perry K.W., Fuller R.W. Supersensitization of the oral response to SKF 38393 in neonatal 6-hydroxydopamine-lesioned rats is eliminated by neonatal 5,7-dihydroxytryptamine treatment. J. Pharmacol. Exp. Therap. 1999; 268: 231-237.
 
24.
Brus R., Szkilnik R., Kostrzewa R.M. Quinpirole-induced yawning behavior in rats neonatally pretreated with 6-hydroxyedopamine (6-OHDA) and 5,7-dihydroxytryptamine (5,7-DHT). Med. Sci. Monit. 1997; 3: 324-327.
 
25.
Damsma G., Bottema T., Westerink B.H.C., Tepper P.G., Dijkstra D., Pugsley T.A. MacKenzie R.G., Heff ner T.G., Wikstrom H. Pharmacological aspects of R-(+)-7-OH-DPAT, a putative dopamine D3 receptor ligand. Eur. J. Pharmacol. 1993; 249: R9-R10.
 
26.
Creese I., Iversen S.D. Behavioral sequel of dopaminergic degeneration. W: E. Usodin J.R., Bunney J.R. red. Modern Pharmacology – Toxicology. Marcel Dekker Publ. 1975; 3: 171-190.
 
27.
Kostrzewa R.M., Kostrzewa J.P., Brus R., Kostrzewa R.A., Nowak P. Proposed animal model of severe Parkinson’s disease: neonatal 6-hydroxydopamine lesion of dopaminergic innervation of striatum. J. Neurol. Transm. 2006; 70: 277-279.
 
28.
Schwartz J.C., Levesque D., Martres M.P., Sokoloff P. Dopamine D3 receptor: basic and clinical aspects. Clin. Neuropharmacol. 1993; 16: 295-314.
 
29.
Kostrzewa R.M., Brus R. Is dopamineagonist induced yawning behavior a D3 mediated event? Life Sci. 1991; 48: PL-129.
 
30.
Paris I., Perez-Pastene C., RaismanVazari R., Caviedes P., Conve E., SeguraAguilar J. Mechanism of copper-induced cell death. Pharmacol. Rep. 2008; 60: 255.
 
31.
Loeff er D.A., Le Witt P.A., Janeau P.L., Nguyen H.U., De Maggio A.J., Brickman C.M., Brewer G.J., Dick R.D., Troyer M.D., Kanaley L. Increased regional brain concentration of ceruloplamsin in neurodegenerative disorders. Brain Res. 1996; 738: 265-274.
 
32.
Deibel M.A., Ehmann W.D., Markesbery W.R. Copper, iron and zinc imbalances in severly degenerated brain regions in Alzheimer’s disease: possible relation to oxidative stress. J. Neurol. Sci. 1996; 143: 137-142.
 
33.
Futura A., Price D.L., Pardo C.A., Troncoso J.C., Xu Z.S., Taniguchi N., Martin L.J. Localization of superoxide dismutases in Alzheimer’s disease and Down’s syndrome neocortex and hippocampus. Am. J. Pathol. 1995; 146: 357-367.
 
34.
Nakao N., Frodl E.M., Widner H., Carlson E., Eggerding F.A., Epstein C.J., Brundin P. Operexpressing Cu/Zn superoxide dismutase enhances survival of transplanted neurons in a rat model of Parkinson’s disease. Nat. Med. 1995; 1: 201-203.
 
35.
Allain P., Krari N. Diethyldithiocarbomate, copper and neurological disorders. Life Sci. 1991; 48: 291-299.
 
36.
Waggoner D.J., Bartnikas T.B., Gitlin J.D. The role of copper in neurodegenerative disease. Neurobiol. Dis. 1991; 6: 221-230.
 
37.
De Vrres D.J., Swell R.B., Beast P.M. Effect of copper on dopaminergic function in the rat corpus striatum. Exper. Neurol. 1986; 91: 546-558.
 
38.
Schlegel-Zawadzka M., Zięba A., Dudek D., Krośniak M., Szymaczek M., Nowak G. Serum trace elements in animal models and human depression. Part II. Copper. Hum. Psychopharmacol. Clin. Exp. 1999; 14: 447-451.
 
39.
Prohaska J.R., Bailey W.R. Regional specifi city in alterations of rat brain copper and catecholamines following perinatal copper defi ciency. J. Neurochem. 1994; 63: 1551-1557.
 
40.
Prohaska J.R., Bailey W.R., Gross A.M., Korte J.J. Eff ect of dietary defi ciency on the distribution of dopamine and norepinephrine in mice and rats. J. Nutr. Prochem. 1990; 1: 149-154.
 
41.
Sokin D., Ilbay G., Ates N. Changes in the blood-brain barrier permeability and in the brain tissue trace element concentrations after single and repeated pentylenetetrazole-induced seizures in rats. Pharmacol. Res. 2003; 48: 69-73.
 
42.
Klevay L.M., Halas E.S. The eff ects of dietary copper defi ciency and psychological stress on blood pressure in rats. Physiol. Behav. 1991; 49: 309-314.
 
43.
Seidel K.E., Faille M.L., Rosebrough R.W. Cardiac catecholamine metabolism in copper-defi cient rats. J. Nutr. 1991; 121: 474-483.
 
44.
Schuschke O.A., Reed M.W., Sarri J.T., Miller F.N. Copper defi ciency alters vasodilatation in the rat cremaster muscle microcirculation. J. Nutr. 1992;122: 1547-1552.
 
45.
Rayssignier Y., Gueux E., Bussiere L., Mazur A. Copper defi ciency increase the susceptiblity of lipoproteins and tissues to peroxidation in rats. J. Nutr. 1993; 123: 1343-1348.
 
46.
Lear P.M., Prohaska J.R. Atria and ventricles of copper-defi cient rats exhibit similar hypertrophy and similar altered biochemical characteristics. Proc. Soc. Exp. Biol. Med. 1997; 215: 377-385.
 
47.
Murthy R.C., Lal S., Saxena D.K., Shukla G.S., Ali M.M., Chandra S.V. Eff ect of manganese and copper interaction on behavior and biogenic amines in rat fed a 10% casein diet. Chem. Biol. Interact. 1981; 37: 299-308.
 
48.
Reinstein N.H., Lonnerdol B., Keen C.L., Hurley I.S. Zinc-copper interaction in pregnant rat: fetal outcome and maternal and fetal zinc, copper and iron. J. Nutr. 1984; 114: 1266-1279.
 
49.
Heilmaier H.E., Drasch G.A., Kretschmer E., Summer K.H. Metallothionein, cadmium, copper and zinc levels of human and rat tissues. Toxicol. Lett. 1987; 38: 205-211.
 
50.
Muto H., Shinada M., Tokata K., Takizawa Y. Rapid changes in concentrations of essentials elements in organs of rats exposed to methylmercury chloride and mercuric chloride as shown by simultaneous multielemental analysis. Br. J. Ind. Med. 1991; 48: 382-388.
 
51.
Barone A., Harper R.G., Wapnir R.A. Placental copper transport in the rat. III: Interaction between copper and iron in maternal protein defi ciency. Placenta 1998; 19: 113-118.
 
52.
Tanaka H. Maternal environment and developmental brain damages. Brain Develop. 1997; 29: 183-189.
 
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