Polydopamine and eumelanin: From structure-property relationships to a unified tailoring strategy

Accounts of Chemical Research

Volumn 47, Issue 12, 2014, Pages 3541-3550

  D'Ischia, Marco ^a   Napolitano, Alessandra ^a   Ball, Vincent ^b,c   Chen, Chun Teh ^d   Buehler, Markus J ^d  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b UNIVERSITÉ DE STRASBOURG   (France)

^c INSERM   (France)

^d Massachusetts Institute of Technology Cambridge   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EUMELANIN; INDOLE DERIVATIVE; MELANIN; NEUROMELANIN; POLYDOPAMINE; POLYMER;

CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER SIMULATION; DRUG DESIGN; SYNTHESIS;

COMPUTER SIMULATION; DRUG DESIGN; INDOLES; MELANINS; MOLECULAR STRUCTURE; POLYMERS;

EID: 84918535218     PISSN: 00014842     EISSN: 15204898     Source Type: Journal    
DOI: 10.1021/ar500273y     Document Type: Article

References (84)

1. Sun, T.; Qing, G.; Su, B.; Jiang, L. Functional Biointerface Materials Inspired from Nature. Chem. Soc. Rev. 2011, 40, 2909-2921.
2. Xia, F.; Jiang, L. Bio-Inspired, Smart, Multiscale Interfacial Materials. Adv. Mater. 2008, 20, 2842-2858.
3. Meredith, P.; Bettinger, C. J.; Irimia-Vladu, M.; Mostert, A. B.; Schwenn, P. E. Electronic and Optoelectronic Materials and Devices Inspired by Nature. Rep. Prog. Phys. 2013, 76, 034501/1-034501/36.
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. Simon, J. D.; Peles, D. N. The Red and the Black. Acc. Chem. Res. 2010, 43, 1452-1460.
6. Ito, S.; Wakamatsu, K.; d'Ischia, M.; Napolitano, A.; Pezzella, A. Structure of Melanins. In Melanins and Melanosomes ; Borovanský, J., Riley, P. A., Eds.; Wiley-VCH: Weinheim, 2011, 167-185.
7. d'Ischia, M.; Napolitano, A.; Pezzella, A.; Meredith, P.; Sarna, T. Chemical and Structural Diversity in Eumelanins: Unexplored Bio-Optoelectronic Materials. Angew. Chem., Int. Ed. 2009, 48, 3914-3921.
8. Panzella, L.; Gentile, G.; D' Errico, G.; Della Vecchia, N. F.; Errico, M. E.; Napolitano, A.; Carfagna, C.; d'Ischia, M. Atypical Structural and π-Electron Features of a Melanin Polymer That Lead to Superior Free-radical-Scavenging Properties. Angew. Chem., Int. Ed. 2013, 52, 12684-12687.
9. Napolitano, A.; Panzella, L.; Leone, L.; d'Ischia, M. Red Hair Benzothiazines and Benzothiazoles: Mutation-Inspired Chemistry in the Quest for Functionality. Acc. Chem. Res. 2013, 46, 519-528.
10. Meredith, P.; Sarna, T. The Physical and Chemical Properties of Eumelanin. Pigment Cell Res. 2006, 19, 572-594.
11. 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 Stateand Aggregation-Dependent Dynamic Interactions in a Model Water-Soluble 5,6-Dihydroxyindole Polymer. J. Am. Chem. Soc. 2009, 131, 15270-15275.
12. Mostert, A. B.; Hanson, G. R.; Sarna, T.; Gentle, I. R.; Powell, B. J.; Meredith, P. Hydration-Controlled X-Band EPR Spectroscopy: A Tool for Unravelling the Complexities of the Solid-State Free Radical in Eumelanin. J. Phys. Chem. B 2013, 117, 4965-4972.
13. Gauden, M.; Pezzella, A.; Panzella, L.; Neves-Petersen, M. T.; Skovsen, E.; Petersen, S. B.; Mullen, K. M.; Napolitano, A.; d'Ischia, M.; Sundstrom, V. Role of Solvent, pH, and Molecular Size in Excited-State Deactivation of Key Eumelanin Building Blocks: Implications for Melanin Pigment Photostability. J. Am. Chem. Soc. 2008, 130, 17038-17043.
14. Mostert, A. B.; Powell, B. J.; Pratt, F. L.; Hanson, G. R.; Sarna, T.; Gentle, I. R.; Meredith, P. Role of Semiconductivity and Ion Transport in the Electrical Conduction of Melanin. Proc. Natl. Acad. Sci. U.S.A. 2012, 109, 8943-8947.
15. Bettinger, C. J.; Bruggeman, J. P.; Misra, A.; Borenstein, J. T.; Langer, R. Biocompatibility of Biodegradable Semiconducting Melanin Films for Nerve Tissue Engineering. Biomaterials 2009, 30, 3050-3057.
16. Prasetyanto, E. A.; Manini, P.; Napolitano, A.; Crescenzi, O.; d'Ischia, M.; De Cola, L. Towards Eumelanin@zeolite Hybrids: Pore-Size-Controlled 5,6-Dihydroxyindole Polymerization. Chem. - Eur. J. 2014, 20, 1597-1601.
17. Shanmuganathan, K.; Cho, J. H.; Iyer, P.; Baranowitz, S.; Ellison, C. J. Thermooxidative Stabilization of Polymers Using Natural and Synthetic Melanins. Macromolecules 2011, 44, 9499-9507.
18. Waite, J. H. Surface chemistry: Mussel Power. Nat. Mater. 2008, 7, 8-9.
19. Lee, H.; Dellatore, S. M.; Miller, W. M.; Messersmith, P. B. Mussel-inspired Surface Chemistry for Multifunctional Coatings. Science 2007, 318, 426-430.
20. Dreyer, D. R.; Miller, D. J.; Freeman, B. D.; Paul, D. R.; Bielawski, C. W. Perspectives on Poly(dopamine). Chem. Sci. 2013, 4, 3796-3802.
21. Sedó, J.; Saiz-Poseu, J.; Busqué, F.; Ruiz-Molina, D. Catechol- Based Biomimetic Functional Materials. Adv. Mater. 2013, 25, 653-701.
22. Liu, Y.; Ai, K.; Lu, L. Polydopamine and Its Derivative Materials: Synthesis and Promising Applications in Energy, Environmental, and Biomedical Fields. Chem. Rev. 2014, 114, 5057-5115.
23. Kasemset, S.; Lee, A.; Miller, D. J.; Freeman, B. D.; Sharma, M. M. Effect of Polydopamine Deposition Conditions on Fouling Resistance, Physical Properties, and Permeation Properties of Reverse Osmosis Membranes in Oil/Water Separation. J. Membr. Sci. 2013, 425-426, 208-216.
24. Kang, S. M.; Hwang, N. S.; Yeom, J.; Park, S. Y.; Messersmith, P. B.; Choi, I. S.; Langer, R.; Anderson, D. G.; Lee, H. One-Step Multipurpose Surface Functionalization by Adhesive Catecholamine. Adv. Funct. Mater. 2012, 22, 2949-2955.
25. Lynge, M. E.; van der Westen, R.; Postma, A.; Städler, B. Polydopamine - a Nature-Inspired Polymer Coating for Biomedical Science. Nanoscale 2011, 3, 4916-4928.
26. Kim, J. H.; Lee, M.; Park, C. B. Polydopamine as a Biomimetic Electron Gate for Artificial Photosynthesis. Angew. Chem., Int. Ed.. 2014, 53, 6364-6368.
27. 4@Poly(dopamine) Magnetic Nanoparticles for Biosensor Construction. J. Mater. Chem. B 2014, 2, 739-746.
28. Black, K. C.; Yi, J.; Rivera, J. G.; Zelasko-Leon, D. C.; Messersmith, P. B. Polydopamine-enabled surface functionalization of gold nanorods for cancer cell-targeted imaging and photothermal therapy. Nanomedicine 2013, 8, 17-28.
29. Ju, K.-Y.; Lee, Y.; Lee, S.; Park, S. B.; Lee, J.-K. Bioinspired Polymerization of Dopamine to Generate Melanin-Like Nanoparticles Having an Excellent Free-Radical-Scavenging Property. Biomacromolecules 2011, 12, 625-632.
30. Zhou, J.; Duan, B.; Fang, Z.; Song, J.; Wang, C.; Messersmith, P. B.; Duan, H. Interfacial assembly of mussel-inspired au@ag@polydopamine core-shell nanoparticles for recyclable nanocatalysts. Adv. Mater. 2014, 26, 701-705.
31. Quignard, S.; Chen, Y.; d'Ischia, M.; Fattaccioli, J. UV-induced fluorescence of polydopamine-coated emulsion droplets. ChemPlusChem 2014, 79, 1254-1257.
32. Cui, J.; Yan, Y.; Such, G. K.; Liang, K.; Ochs, C. J.; Postma, A.; Caruso, F. Immobilization and intracellular delivery of an anticancer drug using mussel-inspired polydopamine capsules. Biomacromolecules 2012, 13, 2225-2228.
33. Chen, X.; Yan, Y.; Müllner, M.; van Koeverden, M. P.; Noi, K. F.; Zhu, W.; Caruso, F. Engineering fluorescent poly(dopamine) capsules. Langmuir 2014, 30, 2921-2925.
34. Della Vecchia, N. F.; Avolio, R.; Alfe, M.; Errico, M. E.; Napolitano, A.; d'Ischia, M. Building-Block Diversity in Polydopamine Underpins a Multifunctional Eumelanin-Type Platform Tunable Through a Quinone Control Point. Adv. Funct. Mater. 2013, 23, 1331-1340.
35. Liebscher, J.; Mrowczynski, R.; Scheidt, H. A.; Filip, C.; Hadade, N. D.; Turcu, R.; Bende, A.; Beck, S. Structure of Polydopamine: A Never-Ending Story? Langmuir 2013, 29, 10539-10548.
36. Pezzella, A.; Crescenzi, O.; Panzella, L.; Napolitano, A.; Land, E. J.; Barone, V.; d' Ischia, M. Free Radical Coupling of o-Semiquinones Uncovered. J. Am. Chem. Soc. 2013, 135, 12142-12149.
37. d'Ischia, M.; Wakamatsu, K.; Napolitano, A.; Briganti, S.; Garcia-Borron, J.-C.; Kovacs, D.; Meredith, P.; Pezzella, A.; Picardo, M.; Sarna, T.; Simon, J. D.; Ito, S. Pigm. Cell Melanoma Res. 2013, 26, 616-633.
38. Ito, S. Encapsulation of a Reactive Core in Neuromelanin. Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 14647-14648.
39. 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.
40. 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.
41. Ito, S.; Wakamatsu, K. Chemical Degradation of Melanins: Application to Identification of Dopamine-Melanin. Pigment Cell Res. 1998, 11, 120-126.
42. Bernsmann, F.; Ponche, A.; Ringwald, C.; Hemmerle, J.; Raya, J.; Bechinger, B.; Voegel, J. C.; Schaaf, P.; Ball, V. Characterization of Dopamine-Melanin Growth on Silicon Oxide. J. Phys. Chem. C 2009, 113, 8234-8242.
43. Dreyer, D. R.; Miller, D. J.; Freeman, B. D.; Paul, D. R.; Bielawski, C. W. Elucidating the structure of poly(dopamine). Langmuir 2012, 28, 6428-6435.
44. Hong, S.; Na, Y. S.; Choi, S.; Song, I. T.; Kim, W. Y.; Lee, H. Non-Covalent Self-Assembly and Covalent Polymerization Co-Contribute to Polydopamine Formation. Adv. Funct. Mater. 2012, 22, 4711-4717.
45. Yu, X.; Fan, H.; Liu, Y.; Shi, Z.; Jin, Z. Characterization of Carbonized Polydopamine Nanoparticles Suggests Ordered Supramolecular Structure of Polydopamine. Langmuir 2014, 30, 5497-5505.
46. Reale, S.; Crucianelli, M.; Pezzella, A.; d'Ischia, M.; De Angelis, F. J. Mass Spectrom. 2012, 47, 49-53.
47. 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.
48. Corani, A.; Huijser, A.; Iadonisi, A.; Pezzella, A.; Sundstroem, V.; d'Ischia, M. Bottom-Up Approach to Eumelanin Photoprotection: Emission Dynamics in Parallel Sets of Water-Soluble 5,6-Dihydrox-yindole-Based Model Systems. J. Phys. Chem. B 2012, 116, 13151-13158.
49. Manini, P.; d'Ischia, M.; Prota, G. An Unusual Decarboxylative Maillard Reaction between L-DOPA and D-Glucose under Biomimetic Conditions: Factors Governing Competition with Pictet-Spengler Condensation. J. Org. Chem. 2001, 66, 5048-5053.
50. Capelli, L.; Crescenzi, O.; Manini, P.; Pezzella, A.; Barone, V.; d'Ischia, M. π-Electron Manipulation of the 5,6-Dihydroxyindole/Quinone System by 3-Alkynylation: Mild Acid-Mediated Entry to (Cross)-Conjugated Scaffolds and Paradigms for Medium-Tunable Chromophores. J. Org. Chem. 2011, 76, 4457-4466.
51. Hong, S.; Kim, J.; Na, Y. S.; Park, J.; Kim, S.; Singha, K.; Im, G. I.; Han, D. K.; Kim, W. J.; Lee, H. Poly(norepinephrine): Ultrasmooth Material-Independent Surface Chemistry and Nanodepot for Nitric Oxide. Angew. Chem., Int. Ed. 2013, 52, 9187-9191.
52. Napolitano, A.; Manini, P.; d'Ischia, M. Oxidation Chemistry of Catecholamines and Neuronal Degeneration: an Update. Curr. Med. Chem. 2011, 18, 1832-1845.
53. Shafiq, Z.; Cui, J.; Pastor-Perez, L.; San Miguel, V.; Gropeanu, R. A.; Serrano, C.; del Campo, A. Bioinspired Underwater Bonding and Debonding on Demand. Angew. Chem., Int. Ed. 2012, 51, 4332-4335.
54. Garcia-Fernandez, L.; Cui, J.; Serrano, C.; Shafiq, Z.; Gropeanu, R. A.; San Miguel, V.; Ramos, J. I.; Wang, M.; Auernhammer, G. K.; Ritz, S. L.; Golriz, A. A.; Berger, R.; Wagner, M.; del Campo, A. Antibacterial Strategies from the Sea: Polymer-Bound Cl-Catechols for Prevention of Biofilm Formation. Adv. Mater. 2013, 25, 529-533.
55. Ambrico, M.; Della Vecchia, N. F.; Ambrico, P. F.; Cardone, A.; Cicco, S. R.; Ligonzo, T.; Avolio, R.; Napolitano, A.; d'Ischia, M. A Photoresponsive Red Hair-Inspired Polydopamine-Based Copolymer for Hybrid Photocapacitive Sensors. Adv. Funct. Mater. 2014, DOI: 10.1002/adfm.201401377.
56. Ambrico, M.; Ambrico, P. F.; Cardone, A.; Della Vecchia, N. F.; Ligonzo, T.; Cicco, S. R.; Talamo, M. M.; Napolitano, A.; Augelli, V.; Farinola, G. M.; d'Ischia, M. Engineering Polydopamine Films with Tailored Behaviour for Next-Generation Eumelanin-Related Hybrid Devices. J. Mater. Chem. C 2013, 1, 1018-1028.
57. Ito, S.; Wakamatsu, K. Chemistry of Mixed Melanogenesis-Pivotal Roles of Dopaquinone. Photochem. Photobiol. 2008, 84, 582-592.
58. Palumbo, A.; d'Ischia, M.; Misuraca, G.; Prota, G.; Schultz, T. M. Structural Modifications in Biosynthetic Melanins Induced by Metal Ions. Biochim. Biophys. Acta 1989, 964, 193-199.
59. Ito, S. A Chemist's View of Melanogenesis. Pigment Cell Res. 2003, 16, 230-236.
60. Della Vecchia, N. F.; Luchini, A.; Napolitano, A.; D'Errico, G.; Vitiello, G.; Szekely, N.; d'Ischia, M.; Paduano, L. Tris Buffer Modulates Polydopamine Growth, Aggregation and Paramagnetic Properties. Langmuir 2014, 30, 9811-9818.
61. Arzillo, M.; Mangiapia, G.; Pezzella, A.; Heenan, R. K.; Radulescu, A.; Paduano, L.; d'Ischia, M. Eumelanin Buildup on the Nanoscale: Aggregate Growth/Assembly and Visible Absorption Development in Biomimetic 5,6-Dihydroxyindole Polymerization. Biomacromolecules 2012, 13, 2379-2390.
62. Kuang, J.; Guo, J. L.; Messersmith, P. B. High Ionic Strength Formation of DOPA-Melanin Coating for Loading and Release of Cationic Antimicrobial Compounds. Adv. Mater. Interfaces 2014, 1, 1400145-1400150.
63. Yu, X.; Fan, H. L.; Wang, L.; Jin, Z. X. Formation of Polydopamine Nanofibers with the Aid of Folic Acid. Angew. Chem., Int. Ed. 2014, 53, 1-6.
64. Cranford, S. W.; Buehler, M. J. Biomateriomics: Springer Series in Materials Science; Springer: New York, 2012; Vol. 165.
65. Knowles, T. P. J.; Buehler, M. J. Nanomechanics of Functional and Pathological Amyloid Materials. Nat. Nanotechnol. 2011, 6, 469-479.
66. Gronau, G.; Krishnaji, S. T.; Kinahan, M. E.; Giesa, T.; Wong, J. Y.; Kaplan, D. L.; Buehler, M. J. A Review of Combined Experimental and Computational Procedures for Assessing Biopolymer Structure-Process-Property Relationships. Biomaterials 2012, 33, 8240-8255.
67. 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.
68. Stark, K. B.; Gallas, J. M.; Zajac, G. W.; Eisner, M.; Golab, J. T. Spectroscopic Study and Simulation from Recent Structural Models for Eumelanin: II. Oligomer. J. Phys. Chem. B 2003, 107, 11558-11562.
69. Kaxiras, E.; Tsolakidis, A.; Zonios, G.; Meng, S. Structural Model of Eumelanin. Phys. Rev. Lett. 2006, 97, 218102.
70. Meng, S.; Kaxiras, E. Theoretical Models of Eumelanin Protomolecules and their Optical Properties. Biophys. J. 2008, 94, 2095-2105.
71. d'Ischia, M.; Crescenzi, O.; Pezzella, A.; Arzillo, M.; Panzella, L.; Napolitano, A.; Barone, V. Structural effects on the electronic absorption of 5,6-dihydroxyindole oligomers: the potential of an integrated experimental and DFT approach to model eumelanin optical properties. Photochem. Photobiol. 2008, 84, 600-607.
72. 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.
73. Okuda, H.; Wakamatsu, K.; Ito, S.; Sota, T. Possible Oxidative Polymerization Mechanism of 5,6-Dihydroxyindole from ab initio Calculations. J. Phys. Chem. A 2008, 112, 11213-11222.
74. Lin, S.; Chen, C. T.; Bdikin, I.; Ball, V.; Grácio, J.; Buehler, M. J. Tuning heterogeneous poly(dopamine) structures and mechanics: in silico covalent cross-linking and thin film nanoindentation. Soft Matter 2014, 10, 457-464.
75. Chen, C.-T.; Ball, V.; de Almeida Gracio, J. J.; Singh, M. K.; Toniazzo, V.; Ruch, D.; Buehler, M. J. Self-assembly of tetramers of 5,6-dihydroxyindole is sufficient to explain the main physical properties of eumelanin. ACS Nano 2013, 7, 1524-1532.
76. Chen, C. T.; Chuang, C.; Cao, J.; Ball, V.; Ruch, D.; Buehler, M. J. Excitonic effects from geometric order and disorder explain broadband optical absorption in eumelanin. Nat. Commun. 2014, 5, 3859.
77. Ball, V.; Del Frari, D. Kinetics of Polydopamine Film Deposition as a Function of pH and Dopamine Concentration: Insights in the Polydopamine Deposition Mechanism. J. Colloid Interface Sci. 2012, 386, 366-372.
78. Ball, V.; Gracio, J.; Villa, M.; Singh, M. K.; Metz-Boutique, M.-H.; Michel, M.; Bour, J.; Toniazzo, V.; Ruch, D.; Buehler, M. J. Comparison of Synthetic Dopamine-Eumelanin Formed in the Presence of Oxygen and Cu2+ Cations as Oxidants. Langmuir 2013, 29, 12754-12761.
79. Bernsmann, F.; Ball, V.; Addiego, F.; Ponche, A.; Michel, M.; de Almeida Gracio, J. J.; Toniazzo, V.; Ruch, D. Dopamine-Melanin Film Deposition Depends on the Used Oxidant and Buffer Solution. Langmuir 2011, 27, 2819-2825.
80. Chassepot, A.; Ball, V. Human Serum Albumin and other Proteins as Templating Agents for the Synthesis of Nanosized Dopamine-Eumelanin. J. Colloid Interface Sci. 2014, 414, 97-102.
81. Bernsmann, F.; Voegel, J. C.; Ball, V. Different Synthesis Methods Allow to Tune the Permeability and Permselectivity of Dopamine-Melanin Films to Electrochemical Probes. Electrochim. Acta 2011, 56, 3914-3919.
82. Ponzio, F.; Payamyar, P.; Schneider, A.; Winterhalter, M.; Bour, J.; Addiego, F.; Krafft, M.-P.; Hemmerle, J.; Ball, V. Polydopamine Films from the Forgotten Air/Water Interface. J. Phys. Chem. Lett. 2014, 5, 3436-3440.
83. Wei, Q.; Zhang, F.; Li, J.; Li, B.; Zhao, C. Oxidant-induced Dopamine Polymerization for Multifunctional Coatings. Polymer Chem. 2010, 1, 1430-1433.
84. Wei, H. L.; Ren, J. .; Han, B.; Xu, L.; Han, L.; Jia, L. Stability of Polydopamine and Poly(DOPA) Melanin-like Films on the Surface of Polymer Membranes under Strongly Acidic and Alkaline Conditions. Colloids Surf., B 2013, 110, 22-28.