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01-12-2014 | Translational Neurosciences - Original Article

A reappraisal of Fe(III) adsorption by melanin

Authors: Rhiannon Lee Schroeder, Jacobus Petrus Gerber

Published in: Journal of Neural Transmission | Issue 12/2014

Abstract

The adsorptive capacity of melanin for Fe(III) was investigated. Iron is involved in promoting the formation of reactive oxygen species which has consequently been associated with Parkinson’s disease. Neuromelanin has been suggested to act as an iron scavenger and, therefore, determining the capacity of melanin to adsorb iron is relevant. Although a few reports have quantified the binding capacity, the current research examined the effect of solution pH on adsorption as well as considering physiologically relevant matrices. In addition, desorption is described for the first time. Our results indicated that adsorption over an acidic pH range was relatively constant and was not significantly affected by the presence of protein or lipid. This paper, therefore, goes beyond published reports by investigating a broader range of factors. It also highlights the importance of melanin in the brain through its homeostatic regulation of Fe(III), through the desorption profile of melanin, a novel result.

Aroca P, Solano F, Salinas C, García-Borrón JC, Lozano JA (1992) Regulation of the final phase of mammalian melanogenesis. Eur J Biochem 208(1):155–163PubMedCrossRef

Bhatnagar V, Anjaiah S, Puri N, Darshanam BNA, Ramaiah A (1993) pH of melanosomes of B16 murine melanoma is acidic: its physiological importance in the regulation of melanin biosynthesis. Arch Biochem Biophys 307(1):183–192PubMedCrossRef

Bolzoni F, Giraudo S, Lopiano L, Bergamasco B, Fasano M, Crippa PR (2002) Magnetic investigations of human mesencephalic neuromelanin. Biochimica et Biophysica Acta 1586(2):210–218PubMedCrossRef

Bridelli MG, Tampellini D, Zecca L (1999) The structure of neuromelanin and its iron binding site studied by infrared spectroscopy. FEBS Lett 457(1):18–22PubMedCrossRef

Castellano C, Cestari V, Cabib S, Puglisi-Allegra S (1991) Post-training dopamine receptor agonists and antagonists affect memory storage in mice irrespective of their selectivity for D1 or D2 receptors. Behavioral and Neural Biol 56(3):283–291CrossRef

Chinta SJ, Andersen JK (2005) Dopaminergic neurons. Int J Biochem Cell Biolo 37(5):942–946CrossRef

Crichton R, Dexter D, Ward R (2011) Brain iron metabolism and its perturbation in neurological diseases. J Neural Trans 118(3):301–314CrossRef

Crippa PR, Giorcelli C, Zeise L (2003) Determination of surface characteristics and fractal dimensions of natural and synthetic eumelanins from nitrogen adsorption isotherms. Langmuir 19(2):348–353CrossRef

Djebbar KE, Zertal A, Debbache N, Sehili T (2008) Comparison of diuron degradation by direct UV photolysis and advanced oxidation processes. J Environ Manage 88(4):1505–1512PubMedCrossRef

Double KL (2006) Functional effects of neuromelanin and synthetic melanin in model systems. J Neural Trans 113(6):751–756 (Vienna, Austria: 1996)CrossRef

Faucheux BA, Martin M-E, Beaumont C, Hauw J–J, Agid Y, Hirsch EC (2003) Neuromelanin associated redox-active iron is increased in the substantia nigra of patients with Parkinson’s disease. J Neurochem 86(5):1142–1148PubMedCrossRef

Fedorow H, Pickford R, Hook JM, Double KL, Halliday GM, Gerlach M, Riederer P, Garner B (2005a) Dolichol is the major lipid component of human substantia nigra neuromelanin. J Neurochem 92(4):990–995PubMedCrossRef

Fedorow H, Tribl F, Halliday G, Gerlach M, Riederer P, Double KL (2005b) Neuromelanin in human dopamine neurons: comparison with peripheral melanins and relevance to Parkinson’s disease. Prog Neurobiol 75(2):109–124PubMedCrossRef

Ferrari E, Engelen M, Monzani E, Sturini M, Girotto S, Bubacco L, Zecca L, Casella L (2013) Synthesis and structural characterization of soluble neuromelanin analogs provides important clues to its biosynthesis. J Biol Inorg Chem 18(1):81–93PubMedCrossRef

Forno LS (1996) Neuropathology of Parkinson’s disease. J Neuropathol Exp Neurol 55(3):259–272PubMedCrossRef

Galazka-Friedman J, Bauminger ER, Friedman A, Koziorowski D, Szlachta K (2007) Human nigral and liver iron—comparison by Mössbauer spectroscopy, electron microscopy and ELISA. In: Lippens PE, Jumas JC, Génin JMR (eds) ICAME 2005. Springer, Berlin, pp 285–288

Galazka-Friedman J, Friedman A, Bauminger E (2009) Iron in the brain. Hyperfine Interact 189(1):31–37CrossRef

Gerfen CR (1992) The neostriatal mosaic: multiple levels of compartmental organization in the basal ganglia. Annu Rev Neurosci 15(1):285–320PubMedCrossRef

Gerlach M, Trautwein AX, Zecca L, Youdim MBH, Riederer P (1995) Mössbauer spectroscopic studies of purified human neuromelanin isolated from the substantia nigra. J Neurochem 65(2):923–926PubMedCrossRef

Gessa GL, Muntoni F, Collu M, Vargiu L, Mereu G (1985) Low doses of ethanol activate dopaminergic neurons in the ventral tegmental area. Brain Res 348(1):201–203PubMedCrossRef

Griffiths PD, Dobson BR, Jones GR, Clarke DT (1999) Iron in the basal ganglia in Parkinson’s disease: an in vitro study using extended X-ray absorption fine structure and cryo-electron microscopy. Brain 122(4):667–673PubMedCrossRef

He X, Hahn P, Iacovelli J, Wong R, King C, Bhisitkul R, Massaro-Giordano M, Dunaief JL (2007) Iron homeostasis and toxicity in retinal degeneration. Prog Retinal Eye Res 26(6):649–673CrossRef

Hong L, Liu V, Simon JD (2004) Binding of metal ions to melanin and their effects on the aerobic reactivity. Photochem Photobiol 80(3):477PubMedCrossRef

Ings RMJ (1984) The melanin binding of drugs and its implications. Drug Metab Rev 15(5–6):1183–1212PubMedCrossRef

Jellinger K, Kienzl E, Rumpelmair G, Riederer P, Stachelberger H, Ben-Shachar D, Youdim MBH (1992) Iron-melanin complex in substantia nigra of parkinsonian brains: an X-ray microanalysis. J Neurochem 59(3):1168–1171PubMedCrossRef

Jenner P, Dexter DT, Sian J, Schapira AHV, Marsden CD (1992) Oxidative stress as a cause of nigral cell death in Parkinson’s disease and incidental lewy body disease. Annals Neurol 32(S1):S82–S87CrossRef

Liu Y, Simon JD (2003) The effect of preparation procedures on the morphology of melanin from the ink sac of sepia officinalis. Pigment Cell Res 16(1):72–80PubMedCrossRef

Liu Y, Kempf VR, Brian Nofsinger J, Weinert EE, Rudnicki M, Wakamatsu K, Ito S, Simon JD (2003) Comparison of the structural and physical properties of human hair eumelanin following enzymatic or acid/base extraction. Pigment Cell Res 16(4):355–365PubMedCrossRef

Liu Y, Hong L, Kempf VR, Wakamatsu K, Ito S, Simon JD (2004) Ion-exchange and adsorption of Fe(III) by Sepia melanin. Pigment Cell Res 17(3):262–269PubMedCrossRef

Liu Y, Hong L, Wakamatsu K, Ito S, Adhyaru B, Cheng C-Y, Bowers CR, Simon JD (2005a) Comparison of structural and chemical properties of black and red human hair melanosomes. Photochem Photobiol 81(1):135–144PubMedCrossRef

Liu Y, Hong L, Wakamatsu K, Ito S, Adhyaru BB, Cheng C-Y, Bowers CR, Simon JD (2005b) Comparisons of the structural and chemical properties of melanosomes isolated from retinal pigment epithelium, iris and choroid of newborn and mature bovine eyes. Photochem Photobiol 81(3):510–516PubMedCrossRef

Madaras F, Gerber J, Peddie F, Kokkinn M (2010) The effect of sampling methods on the apparent constituents of ink from the squid sepioteuthis australis. J Chem Ecol 36(11):1171–1179PubMedCrossRef

Mills E, Dong XP, Wang FD, Xu HX (2010) Mechanisms of brain iron transport: insight into neurodegeneration and CNS disorders. Future Med Chem 2(1):51–64PubMedCentralPubMedCrossRef

Nicolaus BJR (2005) A critical review of the function of neuromelanin and an attempt to provide a unified theory. Med Hypotheses 65(4):791–796PubMedCrossRef

Prem P, Dube KJ, Madison SA, Bartolone J (2003) New insights into the physicochemical effects of ammonia/peroxide bleaching of hair and Sepia melanin. J Soc Cosmet Chem 54(4):395–409

Rodgers AD, Curzon G (1975) Melanin formation by human brain in vitro. J Neurochem 24(6):1123–1129PubMedCrossRef

Schultz W (2000) Multiple reward signals in the brain. Nat Rev Neurosci 1(3):199–207PubMedCrossRef

Shang L, Wang Y, Jiang J, Dong S (2007) pH-dependent protein conformational changes in albumin: gold nanoparticle bioconjugates: a spectroscopic study. Langmuir 23(5):2714–2721PubMedCrossRef

Sung-Min A, Byun K, Kun C, Kim JY, Jong Shin Y, Deokhoon K, Sun Ha P, Kim SU, Simpson RJ, Bonghee L (2008) Human microglial cells synthesize albumin in brain. PLoS One 3(7):1–6

Watt AAR, Bothma JP, Meredith P (2009) The supramolecular structure of melanin. Soft Matter 5(19):3754–3760CrossRef

Whitnall M, Richardson DR (2006) Iron: a new target for pharmacological intervention in neurodegenerative diseases. Seminars in Pediatric Neurol 13(3):186–197CrossRef

Winterbourn CC (1995) Toxicity of iron and hydrogen peroxide: the Fenton reaction. Toxicol Lett 82–83:969–974PubMedCrossRef

Zecca L, Swartz HM (1993) Total and paramagnetic metals in human substantia nigra and its neuromelanin. J Neural Trans—Parkinson’s Dis Dementia Sec 5(3):203–213CrossRef

Zecca L, Pietra R, Goj C, Mecacci C, Radice D, Sabbioni E (1994) Iron and other metals in neuromelanin, substantia nigra, and putamen of human brain. J Neurochem 62(3):1097–1101PubMedCrossRef

Zecca L, Shima T, Stroppolo A, Goj C, Battiston GA, Gerbasi R, Sarna T, Swartz HM (1996) Interaction of neuromelanin and iron in substantia nigra and other areas of human brain. Neuroscience 73(2):407–415PubMedCrossRef

Zecca L, Costi P, Mecacci C, Ito S, Terreni M, Sonnino S (2000) Interaction of human substantia nigra neuromelanin with lipids and peptides. J Neurochem 74(4):1758–1765PubMedCrossRef

Zecca L, Tampellini D, Gatti A, Crippa R, Eisner M, Sulzer D, Ito S, Fariello R, Gallorini M (2002) The neuromelanin of human substantia nigra and its interaction with metals. J Neural Trans 109(5):663–672CrossRef

Zecca L, Stroppolo A, Gatti A, Tampellini D, Toscani M, Gallorini M, Giaveri G, Arosio P, Santambrogio P, Fariello RG, Karatekin E, Kleinman MH, Turro N, Hornykiewicz O, Zucca FA (2004a) The role of iron and copper molecules in the neuronal vulnerability of locus coeruleus and substantia nigra during aging. Proc Natl Acad Sci USA 101(26):9843–9848PubMedCentralPubMedCrossRef

Zecca L, Youdim MBH, Riederer P, Connor JR, Crichton RR (2004b) Iron, brain ageing and neurodegenerative disorders. Nat Rev Neurosci 5(11):863–873PubMedCrossRef

Zecca L, Casella L, Albertini A, Bellei C, Zucca FA, Engelen M, Zadlo A, Szewczyk G, Zareba M, Sarna T (2008a) Neuromelanin can protect against iron-mediated oxidative damage in system modeling iron overload of brain aging and Parkinson’s disease. J Neurochem 106(4):1866–1875PubMed

Zecca L, Turro NJ, Eisner M, Crippa PR, Ito S, Wakamatsu K, Bush WD, Ward WC, Simon JD, Zucca FA, Bellei C, Costi P, Albertini A, Monzani E, Casella L, Gallorini M, Bergamaschi L, Moscatelli A (2008b) New melanic pigments in the human brain that accumulate in aging and block environmental toxic metals. Proc Natl Acad Sci USA 105(45):17567–17572PubMedCentralPubMedCrossRef

Zucca FA, Giaveri G, Gallorini M, Albertini A, Toscani M, Pezzoli G, Lucius R, Wilms H, Sulzer D, Ito S, Wakamatsu K, Zecca L (2004) The neuromelanin of human substantia nigra: physiological and pathogenic aspects. Pigment Cell Res 17(6):610–616PubMedCrossRef

Zucca FA, Bellei C, Giannelli S, Terreni MR, Gallorini M, Rizzio E, Pezzoli G, Albertini A, Zecca L (2006) Neuromelanin and iron in human locus coeruleus and substantia nigra during aging: consequences for neuronal vulnerability. J Neural Trans 113(6):757–767CrossRef

Title: A reappraisal of Fe(III) adsorption by melanin
Authors: Rhiannon Lee Schroeder
Jacobus Petrus Gerber
Publication date: 01-12-2014
Publisher: Springer Vienna
Published in: Journal of Neural Transmission / Issue 12/2014
Print ISSN: 0300-9564
Electronic ISSN: 1435-1463
DOI: https://doi.org/10.1007/s00702-014-1236-9

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A reappraisal of Fe(III) adsorption by melanin

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