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Chapter 7 Biophysical Studies of Melanin

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Chapter 7 Biophysical Studies of Melanin Chapter 7 Biophysical Studies of Melanin: Paramagnetic, Ion-Exchange and Redox Properties of Melanin Pigments and Their Photoreactivity Tadeusz Sarna and Przemyslaw M. Plonka Department of Biophysics, Faculty of Biotechnology, Jagiellonian University, Krakow, Poland Abstract: Melanin is a ubiquitous biological pigment with unusual physicochemical properties. This paper emphasizes selected aspects of melanin research in which significant contributions have been made thanks to the application of EPR spectroscopy. A historical overview of the last 25 years of EPR studies of melanin is given. These studies have led to development of the concept of melanin being a.natural antioxidant that can protect pigment cells from oxidative stress by sequestration of redox-active metal ions, quenching of electronically excited states of photosensitizing dye molecules and singlet oxygen, and by scavenging of reactive free radicals. The paper also briefly reviews results of recent melanin studies that employed alternative techniques such as transient optical spectroscopy with femtosecond time resolution, photoacoustic calorimetry and scanning electron and atomic force microscopies. It is concluded that time-domain EPR and very high frequency EPR spectroscopy are expected to be powerful tools for studying the photodynamics and structure of melanin free radicals and their interactions with the environment and physicochemical agents. 1. INTRODUCTION Melanin is a key component of the human pigmentary system. Pigmentation of the human skin, hair and eyes is, to a large extent, determined by the ability of specialized cells – the melanocytes – to synthesize the brown-black eumelanin, the yellow-reddish pheomelanin, or a mixture of both polymers (Hearing, 1998). A contemporary view of melanin biosynthesis is shown in Fig. 1. Of course, skin, hair and eye melanocytes of individuals with the most severe types of albinism that lack the active machinery necessary for melanin synthesis are devoid of any 125 126 TADEUSZ SARNA AND PRZEMYSLAW M. PLONKA melanin (King, 1998). Although the biological function of melanin is not fully understood, it is widely believed that melanin pigmentation plays an important role in photoprotection of the skin and eyes (Kollias et al., 1991; Sarna, 1992). The complexities of melanins due to their physicochemical properties and inherent heterogeneities make it difficult to reach specific conclusions as to their properties and structure. Attempts to characterize melanins have involved a large number of different experimental techniques and methodological approaches. Although these have led to large amounts of data, the conclusions on composition and structure of melanins are incomplete and some times contradictory. In spite of these limitations, much of what is known about melanin is due to the use of sophisticated physical and chemical approaches. This is particularly true in the case of EPR spectroscopy, whose application to melanin research was of crucial importance for understanding basic redox and ion-exchange properties of this unusual class of biopolymers and the nature of their photoreactivity (Sarna and Swartz, 1993). Because of the extent of the subject and the purpose of this book, our coverage is illustrative rather than comprehensive. We will particularly emphasize those aspects of melanin research in which significant contributions have been made through direct or indirect application of EPR spectroscopy. For a number of years, such studies were carried out in a close collaboration between the National Biomedical EPR Center, Medical College of Wisconsin, and the Department of Biophysics, Jagiellonian University, Poland. It is fair to say that melanin research gained new momentum when a long-standing problem in the biophysics of melanin was brought by one of us to the attention of Jim Hyde, who saw a solution and proposed specific experiments to test it (Sarna et al., 1976). 2. MELANIN AS A FREE RADICAL AND ANTIOXIDANT One of the most unusual features of melanin as a biopolymer is its persistent EPR signal (Blois et al., 1964). Indeed, melanin was among the first biological materials examined by EPR spectroscopy (Commoner et al., 1954). Contrary to one view shared by many melanin researchers, that melanin free radicals are stable, the content of melanin free radicals and their corresponding EPR signal intensity can easily be modified by a number of physicochemical agents (Sealy et al., 1980). An intriguing observation related to melanin radicals was reported by Blois et al. (1964). Their early EPR study indicated that paramagnetic metal BIOPHYSICAL STUDIES OF MELANIN 127 ions such as iron(III) or copper(II) were able to quench the melanin EPR signal. Although the exact mechanism of this phenomenon was not known, it was suggested that the quenching could represent chemical interaction between the unpaired electrons of the melanin free radical centers and of paramagnetic metal ions. Eight years later, another unusual interaction between melanin and transition metal ions was reported (Sarna and Lukiewicz, 1972). The Polish researchers showed that binding of diamagnetic multivalent metal ions such as zinc(II) and cadmium(II) by melanin led to a marked increase in the intensity of its EPR signal. These and other seemingly confusing EPR observations of melanin were explained in a series of papers published during over a decade-long scientific collaboration between the center in Milwaukee and Jagiellonian University. Thus it has been shown that loss of melanin EPR signal amplitude (without apparent changes in the signal linewidth) due to the interaction of melanin radicals with copper ions was purely magnetic in nature and did not involve any chemical reaction of melanin free radical centers (Sarna et al, 1976). Using lanthanide ions such as La(3+), Gd(3+) and Dy(3+), which have similar chemical properties but quite different magnetic properties (La(3+) is diamagnetic and both Gd(3+) and Dy(3+) are paramagnetic; Gd(3+) has a relatively long spin-lattice relaxation time at 77 K and Dy(3+) has a much shorter spin-lattice relaxation time), it was possible to observe consistent changes in the amplitude and microwave power saturation of the melanin EPR signal as a function of the type and concentration of the added metal ions. The changes served as experimental observables in competition experiments between diamagnetic and paramagnetic metal ions for melanin binding sites, and between melanin and EDTA for paramagnetic metal ions. These EPR observations were among the first clear evidence for the existence of several specific types of metal binding sites in melanin. A similar experimental approach was used in a follow-up study to determine the spatial distribution of melanin binding sites in respect to the intrinsic melanin radical centers (Sarna et al., 1981). Assuming a uniform distribution of the binding sites within the melanin polymer, a reasonably good fit of the experimental data (EPR signal amplitude of melanin free radicals as a function of concentration of bound-to-melanin Mn(II)) with the calculated dependence was found. The average distance between the interacting metal ions and melanin free radicals was estimated to be 0.7 nm for the closest proximity of both paramagnetic species. 128 TADEUSZ SARNA AND PRZEMYSLAW M. PLONKA Figure 1. A contemporary view of melanin biosynthesis; the schematic indicates key enzymes and intermediates involved in the synthesis of eu- and pheomelanins (Sealy et al. 1982b; Riley 1998; Nappi and Ottaviani 2000; Ortonne and Balotti 2000; Oyehaug et al., 2002). Enzymes: DHI OX – DHIoxidase (tyrosinase and/or peroxidase); transpeptidase; GSHR – glutathione reductase; reductase inactivated by covalently bound DQ; GT – glutathione transpeptidase; TRP1 –tyrosinase-related protein-1 (DHICA oxidase); TRP2 tyrosinase-related protein -2 (DC tautomerase). Intermediates: BTA - benzothiazinylalanines; CYS – L-cysteine; CYSDOPA – cysteinylDOPA; CYSDQ – cysteinylDOPAquinone; DC – DOPAchrome; DHI – 5,6-dihydroxyindole; DHICA – 5,6- dihydroxyindole-2-carboxylic acid; DOPA – 3,4-dihydroxyphenylalanine; DQ – DOPAquinone; GSDOPA – glutathionylDOPA; GSH – glutathione (reduced); GSSG – glutathione (oxidized); IndQ – Indole-5,6-quinone, IndQCA – Indole-5,6-quinone-2- carboxylic acid; LDC – leucoDC. BIOPHYSICAL STUDIES OF MELANIN 129 Using X-band EPR spectroscopy and the isotope as a molecular probe, the molecular nature of the main binding sites in two synthetic melanins and natural melanin from bovine choroid was studied. (The use of single copper isotope with nuclear spin results in better spectral resolution than is possible using copper ions containing both and It clearly showed that, depending on the pH of the system, copper(II) can form a number of complexes with melanin that involve different functional groups of the polymer and exhibit different stabilities. At pH < 7, monodendate complexes with melanin carboxyl groups are predominantly formed, even though in eumelanins bidendate nitrogen-carboxyl complexes are also formed. The corresponding magnetic parameters are within the range: and At pH 7 and above, copper(II) binds to bidendate phenolic hydroxyl groups, but the number of such sites is much less in natural melanins than in synthetic dopa- melanin. The corresponding magnetic parameters are: 560 – 579 MHz and The assignment of complexes with Cu(II) to functional groups of melanin has been further supported by EPR and elemental analysis of chemically modified synthetic dopa-melanin (Sarna et al.,
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