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http://dx.doi.org/10.5483/BMBRep.2016.49.1.103

Oxidative modification of human ceruloplasmin induced by a catechol neurotoxin, salsolinol  

Kim, Seung-Sub (Department of Biomedical Science, Cheongju University)
Kang, Jae Yoon (School of Interdisciplinary Studies, Korea University)
Kang, Jung Hoon (Department of Biomedical Science, Cheongju University)
Publication Information
BMB Reports / v.49, no.1, 2016 , pp. 45-50 More about this Journal
Abstract
Salsolinol (SAL), a compound derived from dopamine metabolism, is the most probable neurotoxin involved in the pathogenesis of Parkinson's disease (PD). In this study, we investigated the modification and inactivation of human ceruloplasmin (hCP) induced by SAL. Incubation of hCP with SAL increased the protein aggregation and enzyme inactivation in a dose-dependent manner. Reactive oxygen species scavengers and copper chelators inhibited the SAL-mediated hCP modification and inactivation. The formation of dityrosine was detected in SAL-mediated hCP aggregates. Amino acid analysis post the exposure of hCP to SAL revealed that aspartate, histidine, lysine, threonine and tyrosine residues were particularly sensitive. Since hCP is a major copper transport protein, oxidative damage of hCP by SAL may induce perturbation of the copper transport system, which subsequently leads to deleterious conditions in cells. This study of the mechanism by which ceruloplasmin is modified by salsolinol may provide an explanation for the deterioration of organs under neurodegenerative disorders such as PD. [BMB Reports 2016; 49(1): 45-50]
Keywords
Ceruloplasmin; Copper; Reactive oxygen species; Salsolinol;
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Times Cited By KSCI : 4  (Citation Analysis)
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1 Smith PK, Krohn RI, Hermanson GT et al (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150, 76-85   DOI
2 Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685   DOI
3 Imlay JA, Chin SM and Linn S (1988) Toxic DNA damage by hydrogen peroxide through the Fenton reaction in vivo and in vitro. Science 240, 640-642   DOI
4 Sato M, Gitlin JD (1991) Mechanisms of copper incorporation during the biosynthesis of human ceruloplasmin. J Biol Chem 266, 5128-5134
5 Goldstein S and Czapski G (1987) Mechanism of reduction of bleomycin-Cu(II) by CO2- and oxidation of bleomycin-Cu(I) by H2O2 in the absence and presence of DNA. Int J Radiation Biol Related Stud Phys Chem Med 51, 693-706   DOI
6 Gutteridge JM and Halliwell B (1982) The role of the superoxide and hydroxyl radicals in the degradation of DNA and deoxyribose induced by a copper-phenanthroline complex. Biochem Pharmacol 31, 2801-2805   DOI
7 Schweigert N, Zehnder AJ and Eggen RI (2001) Chemical properties of catechols and their molecular modes of toxic action in cells, from microorganisms to mammals. Environ Microbiol 3, 81-91   DOI
8 Li Q, Aubrey MT, Christion T and Free BM (1997) Differential inhibition of DNA synthesis in human T cells by the cigarette tar components hydroquinone and catechol. Fundam Appl Toxicol 38, 158-165   DOI
9 Zaitseva I, Zaitsev V, Card G et al (1996) The X-ray structure of human serum ceruloplasmin at 3.1 Å: nature of the copper centres. J Biol Inorg Chem 1, 15-23   DOI
10 Malmstom BG (1982) Enzymology of oxygen. Ann Rev Biochem 51, 21-59   DOI
11 Wang R, Qing H, Liu XQ et al (2008) Iron contributes to the formation of catechol isoquinolines and oxidative toxicity induced by overdose dopamine in dopaminergic SH-SY5Y cells. Neurosci Bull 24, 125-132   DOI
12 Mravec B (2006) Salsolinol, a derivate of dopamine, is a possible modulator of catecholaminergic transmission: a review of recent developments. Physiol Res 55, 353-364
13 Wanpen S, Govitrapong P, Shavali S et al (2004) Salsolinol, a dopamine-derived tetrahydroisoquinoline, induces cell death by causing oxidative stress in dopaminergic SH-SY5Y cells, and the said effect is attenuated by metallothionein. Brain Res 1005, 67-76   DOI
14 Ohta S, Kohno M, Makino Y et al (1987) Tetrahydroisoquinoline and 1-methyl-tetrahydroisoquinoline are present in the human brain: relation to Parkinson's disease. Biomed Res 8, 453-456   DOI
15 Naoi M, Maruyama W, Akao Y and Yi H (2002) Dopamine-derived endogenous N-methyl-(R)-salsolinol: its role in Parkinson's disease. Neurotoxicol Teratol 24, 579-591   DOI
16 Olasode B, Niger JJ (2001) Idiopathic Parkinson's disease: a review of clinical types and pathology. Med 10, 116-120
17 Scott TR, Netsky MG (1961) The pathology of Parkinson's syndrome: a critical review. Int J Neurol 2, 51-60
18 Ikeda H, Markey CJ, Markey SP (1993) Search for neurotoxins structurally related to 1-methyl-4-phenylpyridine (MPP＋) in the pathogenesis of Parkinson's disease. Brain Res 575, 285-298   DOI
19 Moser A, Kompf D (1992) Presence of methyl-6,7-dihydroxy-1,2,3,4-tetrahydroisoquinolines, derivatives of the neurotoxin isoquinoline, in parkinsonian lumbar CSF. Life Sciences 50, 1885-1891   DOI
20 Kang JH (2013) Modification and inactivation of Cu,Zn-superoxidee dismutase. BMB Rep 46, 555-560   DOI
21 Bento I, Peixoto C, Zaisev VN and Lindley PF (2007) Ceruloplasmin revisited: structural and functional roles of various metal cation-binding sites. Acta Cryst 63, 240-248
22 Choi SY, Kwon HY, Kwon OB et al (2000) Fragmentation of human ceruloplasmin induced by hydrogen peroxide. Biochimie 82, 175-180   DOI
23 Jin L, Wang J, Jin H et al (2012) Nigral iron deposition occurs across motor phenotypes of Parkinson's disease. Eur J Neurol 19, 969-976   DOI
24 Kang JH, Kim KS, Choi SY et al (2001) Oxidative modification of human ceruloplasmin by peroxyl radicals. Biochim Biophys Acta 1568, 30-36   DOI
25 Torsdottir G, kristinsson J, Sveinbjornsdottir S et al (1999) Copper, ceruloplasmin, superoxide dismutase and iron parameters in Parkinson's disease. Pharmacol Toxical 85, 239-243   DOI
26 Jin L, Wang J, Zhao L et al (2011) Decreased serum ceruloplasmin levels characteristically aggravate nigral iron deposition in Parkinson's disease. Brain 134, 50-58   DOI
27 Torsdottir G, Sveinbjornsdottir S, Kristinsson J et al (2006) Ceruloplasmin and superoxide dismutase (SOD1) in Parkinson's disease: a follow-up study. J Neurol Sci 241, 53-58   DOI
28 Osaki S, Johnson DA and Frieden E (1966) The possible significance of the ferrous oxidase activity of ceruloplasmin in normal human serum. J Boil Chem 241, 2746-2751
29 Levine RL, Williams JA, Stadtman ER and Shacter E (1994) Carbonyl assays for determination of oxidatively modified proteins. Methods Enzymol 233, 346-357   DOI
30 Kang JH (2004) Modification of Cu,Zn-superoxide dismutase by oxidized catecholamines. J Biochem Mol Biol 37, 325-329   DOI
31 Wanpen S, Govitrapong P, Shavali S, Sangchot PM and Ebadi M (2004) Salsolinol, a dopamine-derived tetrahydroisoquinoline, induces cell death by causing oxidative stress in dopaminergic SH-SY5Y cells, and the said effect is attenuated by metallothionein. Brain Res 1005, 67-76   DOI
32 Niwa T, Takeda T, Yoshizumi H et al (1991) Presence of 2-methyl-6,7-dihydroxy-1,2,3,4-tetrahydroisoqui-noline and 1,2-dimethyl-6,7-dihydroxy-1,2,3,4-tetrahydro-isoquinoline, novel endogenous amines, in parkinsonian and normal human brains. Biochem Biophys Res Commun 177, 603-609   DOI
33 Levine RL (1982) Rapid benchtop method of alkaline hydrolysis of proteins. J Chromatogr 236, 496-498   DOI
34 Jung YJ and Surh YJ (2001) Oxidative DNA damage and cytotoxicity induced by copper-stimulated redox cycling of salsolinol, a neurotoxic tetrahydroisoquinoline alkaloid. Free Radic Biol Med 30, 1407-1417   DOI
35 Montes S, Rivera-Mancia S, Diaz-Ruiz A, Tristan-Lopez L and Rios C (2014) Copper and copper proteins in Parkinson's disease. Oxid Med Cell Longev 2014, 147251-147266   DOI
36 Surh YJ, Jung YJ, Jung JH, Lee JS and Yoon HR (2002) Iron enhancement of oxidative DNA damage and neuronal cell death induced by salsolinol. J Toxicol Environ Health Part A 65, 473-488   DOI
37 Maruyama W, Sobuc G, Matsubara K et al (1997) A dopaminergic neurotoxin, 1(R), 2(N)-dimethyl-6,7-dihydroxy-1,2,3,4-tetrahydro-isoquinoline, N-methyl(R)salsolinol, and its oxidation product, 1,2(N)-dimethyl-6,7-dihydroxyisoquinolinium ion, accumulate in the nigro-striatal system of the human brain. Neurosci Lett 223, 61-64   DOI
38 Maruyama W, Abe T, Tohgi H, Dostert P and Naoi M (1996) A dopaminergic neurotoxin, (R)-N-methylsalsolinol, increases in Parkinsonian cerebrospinal fluid. Ann Neurol 40, 119-122   DOI
39 Choi SY, Kwon HY, Kwon OB and Kang JH (1999) Hydrogen peroxide-mediated Cu,Zn-superoxide dismutase fragmentation: protection by carnosine, homocarnosine and anserine. Biochim Biophys Acta 1472, 651-657   DOI
40 Kim SM and Kang JH (1997) Peroxidative activity of human Cu,Zn-superoxide dismutase. Mol Cells 7, 120-124
41 Halliwell B and Gutteridge JMC (2007) Free Radicals in Biology and Medicine, Oxford, New York.
42 Rouault TA and Cooperman S (2006) Brain iron metabolism. Semin Padiatr Neurol 13, 142-148   DOI
43 Davies KJ, Delsignore ME and Lin SW (1987) Protein damage and degradation by oxygen radicals. II. Modification of amino acids. J Biol Chem 262, 9902-9907
44 Kang JH (2013) Salsolinol, a catechol neurotoxin, induces oxidative modification of cytochrome c. BMB Rep 46, 119-123   DOI
45 Kang JH (2007) Salsolinol, a tetrahydroisoquinoline catechol neurotoxin, induces human Cu,Zn-superoxidie dismutase modificaiton. J Biochem Mol Biol 40, 684-689   DOI
46 Harris ZL, Takahashi Y, Miyajima H et al (1995) Aceruloplasminemia: molecular characterization of this disorder of iron metabolism. Proc Natl Acad Sci U S A 92, 2539-2543   DOI
47 Kim KS, Choi SY, Kwon HY et al (2002) The ceruloplasmin and hydrogen peroxide system induces alpha-synuclein aggregation in vitro. Biochimie 84, 625-631   DOI
48 Boll MC (2008) Free copper, ferroxidase and SOD1 activities, lipid peroxidation and NO(x) content in the CSF. A different marker profile in four neurodegenerative diseases. Neurochem Res 33, 1717-1723   DOI
49 Olivieri S, Conti A, Iannaccone S et al (2011) Ceruloplasmin oxidation, a feature of Parkinson's disease CSF, inhibits ferroxidase activity and promotes cellular iron retention. J Neurosci 31, 18568-18577   DOI
50 Boll MC, Sotelo J, Otero E et al (1999) Reduced ferroxidase activity in the cerebrospinal fluid from patients with Parkinson's disease. Neurosci lett 265, 155-158   DOI
51 Martinez-Hemandez R, Montes S, Higuera-Calleja J et al (2011) Plasma ceruloplasmin ferroxidase activity correlates with the nigral sonographic area in Parkinson's disease patients: a pilot study. Neurochem Res 36, 2111-2115   DOI
52 Jamal M, Ameno K, Ameno S et al (2003) In Vivo study of salsolinol produced by a high concentration of acetaldehyde in the striatum and nucleus accumbens of free-moving rats. Alcohol Clin Exp Res 27, 79S-84S   DOI
53 Bharucha KJ, Friedman JK, Vincent AS and Ross ED (2008) Lower serum ceruloplasmin levels correlate with younger age of onset in Parkinson's disease. J Neurol 255, 1957-1962   DOI
54 Naoi M, Marayama W, Dostert P et al (1996) A novel enzyme enantio-selectively synthesizes (R)salsolinol, a precursor of a dopaminergic neurotoxin, N-methyl(R)salsolinol. Neurosci Lett 212, 183-186   DOI
55 Deng Y, Luan Y, Qing H et al (2008) The formation of catechol isoquinolines in PC12 cells exposed to manganese. Neurosci Lett 444, 122-126   DOI
56 Jamal M, Ameno K, Kubota T et al (2003) In vivo formation of salsolinol induced by high acetaldehyde concentration in rat striatum employing microdialysis. Alcohol Alcohol 38, 197-201   DOI