Eumelanin buildup on the nanoscale: Aggregate growth/assembly and visible absorption development in biomimetic 5,6-dihydroxyindole polymerization.

Biomacromolecules

Volumn 13, Issue 8, 2012, Pages 2379-2390

  Arzillo, Marianna ^a   Mangiapia, Gaetano ^a,b   Pezzella, Alessandro ^a   Heenan, Richard K ^c   Radulescu, Aurel ^d   Paduano, Luigi ^a,b   D'Ischia, Marco ^a  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b UNIVERSITY OF FLORENCE   (Italy)

^c RUTHERFORD APPLETON LABORATORY   (United Kingdom)

^d Julich Centre for Neutron Science   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADVANCED MATERIALS; AGGREGATE GROWTH; AGGREGATION PROCESS; CURRENT DRIVES; EUMELANINS; HYDRODYNAMIC RADIUS; KEY DETERMINANTS; LARGE AGGREGATES; MONOMER CONVERSIONS; NANO SCALE; NANOSCALE LEVELS; OXIDATIVE POLYMERIZATION; PARTICLE GROWTH; POLY(VINYL ALCOHOL) (PVA); POLYMER SYNTHESIS; POLYMERIZATION MECHANISMS; SMALL-ANGLE NEUTRON SCATTERING; STRUCTURE PROPERTY RELATIONSHIPS; SUPRAMOLECULAR ORGANIZATIONS; VISIBLE LIGHT ABSORPTION; WATER SOLUBILIZATION;

AGGLOMERATION; BIOMIMETICS; BIOMOLECULES; BIOPOLYMERS; DIMERS; DYNAMIC LIGHT SCATTERING; LIVING POLYMERIZATION; MONOMERS; NANOTECHNOLOGY; NEUTRON SCATTERING; POLYMERS; PRECIPITATION (CHEMICAL);

AGGREGATES;

5,6 DIHYDROXYINDOLE; BIOMIMETIC MATERIAL; EUMELANIN; POLYVINYL ALCOHOL; UNCLASSIFIED DRUG;

ARTICLE; CHEMICAL STRUCTURE; LIGHT ABSORPTION; LIGHT SCATTERING; NANOTECHNOLOGY; NEUTRON SCATTERING; PARTICLE SIZE; POLYMERIZATION; PRECIPITATION; PRIORITY JOURNAL; SPECTROPHOTOMETRY;

ALGORITHMS; BIOMIMETICS; BIOPOLYMERS; INDOLES; LIGHT; MELANINS; MODELS, CHEMICAL; NANOPARTICLES; NEUTRON DIFFRACTION; OXIDATION-REDUCTION; PARTICLE SIZE; POLYMERIZATION; POLYVINYL ALCOHOL; SCATTERING, RADIATION; SCATTERING, SMALL ANGLE;

EID: 84865031093     PISSN: 15257797     EISSN: 15264602     Source Type: Journal    
DOI: 10.1021/bm3006159     Document Type: Article

References (50)

1. Ito, S.; Wakamatsu, K., Chemistry of Melanins. In The Pigmentary Systems Physiology and Pathophysiology; Nordlund, J. J., Boissy, R. E., Hearing, V. J., King, R. A., Oetting, W. S., Ortonne, J. P., Eds.; Oxford Blackwell Publishing, Ltd.: Oxford, U.K., 2006; pp 282-310.
2. Prota, G. Melanins and Melanogenesis; Academic Press: San Diego, CA, 1992.
3. Simon, J. D.; Hong, L.; Peles, D. N. Insights into melanosomes and melanin from some interesting spatial and temporal properties J. Phys. Chem. B 2008, 112, 13201-13217
4. Simon, J. D.; Peles, D.; Wakamatsu, K.; Ito, S. Current challenges in understanding melanogenesis: bridging chemistry, biological control, morphology, and function Pigm. Cell Melanoma Res. 2009, 22, 563-579
5. Hatcher, L. Q.; Simon, J. D. Ultra-low temperature oxidation of 5,6-dihydroxyindole: a novel approach to study synthetic melanogenesis Photochem. Photobiol. 2008, 84, 608-612
6. Meredith, P.; Sarna, T. The physical and chemical properties of eumelanin Pigm. Cell Res. 2006, 19, 572-594
7. Simon, J. D.; Peles, D. N. The red and the black Acc. Chem. Res. 2010, 43, 1452-1460
8. Clancy, C. M. R.; Simon, J. D. Ultrastructural organization of eumelanin from sepia officinalis measured by atomic force microscopy Biochemistry 2001, 40, 13353-13360
9. Gallas, J. M.; Littrell, K. C.; Seifert, S.; Zajac, G. W.; Thiyagarajan, P. Solution structure of copper ion-induced molecular aggregates of tyrosine melanin Biophys. J. 1999, 77, 1135-1142
10. Watt, A. A. R.; Bothma, J. P.; Meredith, P. The supramolecular structure of melanin Soft Matter 2009, 5, 3754-3760
11. Cheng, J.; Moss, S. C.; Eisner, M.; Zschack, P. X-ray characterization of melanins-I Pigm. Cell Res. 1994, 7, 255-262
12. Zajac, G. W.; Gallas, J. M.; Cheng, J.; Eisner, M.; Moss, S. C.; Alvarado-Swaisgood, A. E. The fundamental unit of synthetic melanin: a verification by tunneling microscopy of X-ray scattering results Biochim. Biophys. Acta, Gen. Subj 1994, 1199, 271-278
13. Kaxiras, E.; Tsolakidis, A.; Zonios, G.; Meng, S. Structural model of eumelanin Phys. Rev. Lett. 2006, 97, 218102/1-218102/4
14. Stark, K. B.; Gallas, J. M.; Zajac, G. W.; Eisner, M.; Golab, J. T. Spectroscopic study and simulation from recent structural models for eumelanin: I. monomer, dimers J. Phys. Chem. B 2003, 107, 3061-3067
15. Stark, K. B.; Gallas, J. M.; Zajac, G. W.; Golab, J. T.; Gidanian, S.; McIntire, T.; Farmer, P. J. Effect of stacking and redox state on optical absorption spectra of melanins-comparison of theoretical and experimental results J. Phys. Chem. B 2005, 109, 1970-1977
16. Zeise, L.; Murr, B. L.; Chedekel, M. R. Melanin standard method: particle description Pigm. Cell Res. 1992, 5, 132-142
17. Huang, J. S.; Sung, J.; Eisner, M.; Moss, S. C.; Gallas, J. The fractal structure and the dynamics of aggregation of synthetic melanin in low pH aqueous solutions J. Chem. Phys. 1989, 90, 25-29
18. Bridelli, M. G. Self-assembly of melanin studied by laser light scattering Biophys. Chem. 1998, 73, 227-239
19. Crippa, P. R.; Giorcelli, C.; Zeise, L. Determination of surface characteristics and fractal dimensions of natural and synthetic eumelanins from nitrogen adsorption isotherms Langmuir 2003, 19, 348-353
20. d'Ischia, M.; Napolitano, A.; Pezzella, A.; Land, E. J.; Ramsden, C. A.; Riley, P. A. 5,6-Dihydroxyindoles and indole-5,6-diones Adv. Heterocycl. Chem. 2005, 89, 1-63
21. Pezzella, A.; Panzella, L.; Crescenzi, O.; Napolitano, A.; Navaratman, S.; Edge, R.; Land, E. J.; Barone, V.; d'Ischia, M. Short-lived quinonoid species from 5,6-dihydroxyindole dimers en route to eumelanin polymers: integrated chemical, pulse radiolytic, and quantum mechanical investigation J. Am. Chem. Soc. 2006, 128, 15490-15498
22. Pezzella, A.; Panzella, L.; Crescenzi, O.; Napolitano, A.; Navaratnam, S.; Edge, R.; Land, E. J.; Barone, V.; d'Ischia, M. Lack of visible chromophore development in the pulse radiolysis oxidation of 5,6-dihydroxyindole-2- carboxylic acid oligomers: DFT investigation and implications for eumelanin absorption properties J. Org. Chem. 2009, 74, 3727-3734
23. Pezzella, A.; Panzella, L.; Natangelo, A.; Arzillo, M.; Napolitano, A.; d'Ischia, M. 5,6-Dihydroxyindole tetramers with anomalous interunit bonding patterns by oxidative coupling of 5,5′,6,6′-tetrahydroxy-2,7′- biindolyl: emerging complexities on the way toward an improved model of eumelanin buildup J. Org. Chem. 2007, 72, 9225-9230
24. Arzillo, M.; Pezzella, A.; Crescenzi, O.; Napolitano, A.; Land, E. J.; Barone, V.; d'Ischia, M. Cyclic structural motifs in 5,6-dihydroxyindole polymerization uncovered: biomimetic modular buildup of a unique five-membered macrocycle Org. Lett. 2010, 12, 3250-3253
25. Panzella, L.; Pezzella, A.; Napolitano, A.; D'Ischia, M. The first 5,6-dihydroxyindole tetramer by oxidation of 5,5′,6,6′-tetrahydroxy- 2,4′-biindolyl and an unexpected issue of positional reactivity en route to eumelanin-related polymers Org. Lett. 2007, 9, 1411-1414
26. Pezzella, A.; Napolitano, A.; d'Ischia, M.; Prota, G.; Seraglia, R.; Traldi, P. Identification of partially degraded oligomers of 5,6-dihydroxyindole-2-carboxylic acid in Sepia melanin by matrix-assisted laser desorption/ionization mass spectrometry Rapid Commun. Mass Spectrom. 1997, 11, 368-372
27. Seraglia, R.; Traldi, P.; Elli, G.; Bertazzo, A.; Costa, C.; Allegri, G. Laser desorption ionization mass spectrometry in the study of natural and synthetic melanins. I-tyrosine melanins Biol. Mass Spectrom. 1993, 22, 687-697
28. Reale, S.; Crucianelli, M.; Pezzella, A.; d'Ischia, M.; De Angelis, F. Exploring the frontiers of synthetic eumelanin polymers by high-resolution matrix-assisted laser/desorption ionization mass spectrometry J. Mass Spectrom. 2012, 47, 49-53
29. Kroesche, C.; Peter, M. G. Detection of melanochromes by MALDI-TOF mass spectrometry Tetrahedron 1996, 52, 3947-3952
30. Tran, M. L.; Powell, B. J.; Meredith, P. Chemical and structural disorder in eumelanins: a possible explanation for broadband absorbance Biophys. J. 2006, 90, 743-752
31. Schweitzer Andrew, D.; Howell Robertha, C.; Jiang, Z.; Bryan Ruth, A.; Gerfen, G.; Chen, C.-C.; Mah, D.; Cahill, S.; Casadevall, A.; Dadachova, E. Physico-chemical evaluation of rationally designed melanins as novel nature-inspired radioprotectors PLoS One 2009, 4, e7229
32. Edge, R.; d'Ischia, M.; Land, E. J.; Napolitano, A.; Navaratnam, S.; Panzella, L.; Pezzella, A.; Ramsden, C. A.; Riley, P. A. Dopaquinone redox exchange with dihydroxyindole and dihydroxyindole carboxylic acid Pigm. Cell Res. 2006, 19, 443-450
33. Napolitano, A.; Pezzella, A.; Vincensi, M. R.; Prota, G. Oxidative-degradation of melanins to pyrrole acids-a model study Tetrahedron 1995, 51, 5913-5920
34. Pezzella, A.; Iadonisi, A.; Valerio, S.; Panzella, L.; Napolitano, A.; Adinolfi, M.; d'Ischia, M. Disentangling eumelanin "black chromophore": visible absorption changes as signatures of oxidation state- and aggregation-dependent dynamic interactions in a model water-soluble 5,6-dihydroxyindole polymer J. Am. Chem. Soc. 2009, 131, 15270-15275
35. Berne, B. J.; Pecora, R. Dynamic Light Scattering: with Applications to Chemistry, Biology, and Physics; Dover Publications: Mineola, NY, 1975; p 400.
36. Vaccaro, M.; Accardo, A.; Tesauro, D.; Mangiapia, G.; Loef, D.; Schillen, K.; Soederman, O.; Morelli, G.; Paduano, L. Supramolecular aggregates of amphiphilic gadolinium complexes as blood pool MRI/MRA contrast agents: physicochemical characterization Langmuir 2006, 22, 6635-6643
37. Wignall, G. D.; Bates, F. S. Absolute calibration of small-angle neutron scattering data J. Appl. Crystallogr. 1987, 20, 28-40
38. Palumbo, A.; D'Ischia, M.; Misuraca, G.; Prota, G. Effect of metal ions on the rearrangement of dopachrome Biochim. Biophys. Acta, Gen. Subj. 1987, 925, 203-209
39. Mangiapia, G.; Ricciardi, R.; Auriemma, F.; De Rosa, C.; Lo Celso, F.; Triolo, R.; Heenan, R. K.; Radulescu, A.; Tedeschi, A. M.; D'Errico, G.; Paduano, L. Mesoscopic and microscopic investigation on poly(vinyl alcohol) hydrogels in the presence of sodium decylsulfate J. Phys. Chem. B 2007, 111, 2166-2173
40. Guinier, A.; Fournet, G. Small-Angle Scattering of X-rays; Wiley: New York, 1955; p 268.
41. Ma, G.; Barlow, D. J.; Lawrence, M. J.; Heenan, R. K.; Timmins, P. Small-angle neutron-scattering studies of nonionic surfactant vesicles J. Phys. Chem. B 2000, 104, 9081-9085
42. Ricciardi, R.; Mangiapia, G.; Lo Celso, F.; Paduano, L.; Triolo, R.; Auriemma, F.; De Rosa, C.; Laupretre, F. Structural organization of poly(vinyl alcohol) hydrogels obtained by freezing and thawing techniques: a SANS study Chem. Mater. 2005, 17, 1183-1189
43. Roscigno, P.; Paduano, L.; D'Errico, G.; Vitagliano, V. On the presumed specific interaction of anionic surfactants with nonionic polymers. aqueous solution of sodium alkylsulfonate in the presence of poly(vinylpyrrolidone): an "excluded volume" effect Langmuir 2001, 17, 4510-4518
44. Paduano, L.; Sartorio, R.; Vitagliano, V. Diffusion coefficients of the ternary system α-cyclodextrin-sodium benzenesulfonate-water at 25 °C: the effect of chemical equilibrium and complex formation on the diffusion coefficients of a ternary system J. Phys. Chem. B 1998, 102, 5023-5028
45. Annunziata, O. Private communication, 2008.
46. Molisso, A. Idrogeli modificati di PVA: Studio del comportamento di fasedel PVA in presenza di sali semplici e polimeri; Università degli Studi di Napoli "Federico II": Naples, 2008.
47. Gallas, J. M.; Zajac, G. W.; Sarna, T.; Stotter, P. L. Structural differences in unbleached and mildly-bleached synthetic tyrosine-derived melanins identified by scanning probe microscopies Pigm. Cell Res. 2000, 13, 99-108
48. Napolitano, A.; Pezzella, A.; Prota, G.; Seraglia, R.; Traldi, P. Structural analysis of synthetic melanins from 5,6-dihydroxyindole by matrix-assisted laser desorption/ionization mass spectrometry Rapid Commun. Mass Spectrom. 1996, 10, 468-472
49. Marks, M. S.; Seabra, M. C. The melanosome: membrane dynamics in black and white Nat. Rev. Mol. Cell Biol. 2001, 2, 738-748
50. Clancy, C. M. R.; Nofsinger, J. B.; Hanks, R. K.; Simon, J. D. A hierarchical self-assembly of eumelanin J. Phys. Chem. B 2000, 104, 7871-7873