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Bioinspired Melanin‐Based Optically Active Materials

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Bioinspired Melanin‐Based Optically Active Materials PROGRESS REPORT www.advopticalmat.de Bioinspired Melanin-Based Optically Active Materials Ming Xiao,* Matthew D. Shawkey, and Ali Dhinojwala the properties and functions of melanin, Melanin is a widespread multifunctional biological pigment that has emerged the synthesis of melanin-like nanopar- as a promising platform for applications in coating, catalysis, energy, drug ticles, and its versatile applications in delivery, and medical therapy. Melanin is also a compelling material for catalysis, energy, and biomedical fields. Over the last 5 years, more than 1000 photonic applications because of its favorable material characteristics, papers on melanin have been published including broadband absorption, high refractive index, tunable fluorescence, annually, based on data from the Web and UV blocking capabilities. However, there is not yet a critical review of Science. Quite a few of these papers focusing on optical functions of melanin. This review summarizes current have reviewed melanin’s chemical struc- advances in bioinspired melanin-based optically active materials, covering ture, physiochemical properties, and biomedical applications.[4–6] However, a melanin’s inherent optical properties and functions both in nature and in critical review focusing on optical func- optics-related applications. It is envisioned that this work will provide a better tions of melanin is still lacking, despite understanding of melanin’s photonic functions and insights into the future tremendous emerging work on melanin- development of melanin-based or melanin-inspired optically active materials based photonic materials. The purpose for wide applications. of this review is to summarize current advances in bioinspired melanin-based optically active materials. Specifically, we will cover inherent optical properties of 1. Introduction melanin, and then summarize melanin’s optical functions in nature and its optics-related applications. Melanin is a group of black or dark pigments ubiquitous in nature, and found in bacteria, fungi, plants, animals, and even prehistoric organisms. Melanin has excellent phys- 2. Melanin Structure and Optical Properties icochemical properties including broadband UV–vis absorp- tion, antioxidant capability, binding affinity for metal ions, Melanin has complex chemical structures that is not yet fully mechanical strength enhancement, and humidity-sensitive understood, however, it does not hinder the exploration of their semi-conductivity.[1,2] optical properties. In this section, we will first discuss classifica- Research on melanin began 400 years ago with the studies tions of melanin and then summarize unique optical properties of Santorio Santorius on pigmentation in human skins.[3] A of melanin, which will be important for both understanding its better molecular understanding of melanin and its biosyn- biological function in nature and synthetic applications. thesis in cells was mostly revealed in the last century. Due to advances in characterization, synthesis, and fabrication that offered tools to more efficiently address old problems, the 2.1. Classification and Structure last decade has seen huge improvements in understanding Conventionally, all black pigments are called melanin. Recently, d’Ischia et al. suggested that any phenolic polymers that have Dr. M. Xiao, Prof. A. Dhinojwala Department of Polymer Science broadband light absorption, antioxidant, and intrinsic free The University of Akron radical character should be characterized as melanin.[5] Exact Akron, OH 44325, USA chemical structures of melanin remain elusive, mainly due to E-mail: [email protected] their insolubility in solvents, close binding with other cellular Dr. M. Xiao tissues, and an amorphous structure. Here, we do not elabo- John A. Paulson School of Engineering and Applied Sciences [7] Harvard University rate on the complexities of melanin’s chemical structures, but Cambridge, MA 02138, USA rather focus on its classification. Melanin can be categorized as Prof. M. D. Shawkey either natural or synthetic depending on whether it was synthe- Department of Biology sized in vivo or in vitro. Both have similar macroscopic proper- Evolution and Optics of Nanostructures Group ties, but their structures are likely quite different. University of Ghent Natural melanin, including eumelanin, pheomelanin, and Ghent 9000, Belgium neuromelanin, is produced from a series of enzymatic reac- The ORCID identification number(s) for the author(s) of this article tions starting from L-tyrosine in biological systems (Figure 1).[1] can be found under https://doi.org/10.1002/adom.202000932. In cells (commonly melanocytes), the tyrosinase oxidizes DOI: 10.1002/adom.202000932 L-tyrosine to dopaquinone (DQ). If cysteine concentration in Adv. Optical Mater. 2020, 2000932 2000932 (1 of 15) © 2020 Wiley-VCH GmbH www.advancedsciencenews.com www.advopticalmat.de Figure 1. Classifications of melanin. The left side shows schematic of biosynthetic pathways for four types of natural melanin. The right orange boxes show some reported synthetic versions for different types of melanin. the cells is low, DQ is then converted to eumelanin catalyzed by into the mysterious structure of natural melanin. Even though different types of enzymes; otherwise it incorporates cysteine the structure of eumelanin is not fully resolved,[22] the preva- to form pheomelanin. It is widely accepted that eumelanin lent hypothesis is that polydopamine is made of linear polymer is made of two major blocks, namely, 5,6-dihydroxyindole chains formed via strong physical intermolecular interactions (DHI) and 5,6-dihydroxyindole-2-carboxylic acid (DHICA); and such as hydrogen bounding and π–π interactions.[23] These pheomelanin consists of two types of benzothiazine intermedi- physical interactions drive polydopamine chains to form pri- ates. Pheomelanin is often combined with eumelanin and pure mary nanoparticles (≈10 nm), and then primary nanoparticles pheomelanin has rarely been reported.[3,8] The ratio of these aggregate to a larger size (hundreds of nanometers). Such a two types of melanin is related to photo-reactivity and likely hierarchical structure is universal for different natural melanin associated with skin cancer susceptibility.[9] Neuromelanin is particles across different phylogenetically distant species.[24] produced in the brain to reduce oxidative stress on brain dis- In the following sections, we will use melanin as a general eases and often mixed with both indole and benzothiazine term to represent both natural and synthetic melanin. Where units. Neuromelanin is related to neurodegenerative disorders it is necessary to avoid confusion or emphasize differences, we such as Parkinson and Alzheimer disease.[10] A fourth type will specify the type of melanin. of natural melanin, called allomelanin, has recently drawn attention.[11] It is a heterogeneous group of polymers without nitrogen mostly found in bacteria, fungi, and plants;[12] and 2.2. Optical Properties it is derived from 1,8-dihydroxynaphthalene (DHN), 1,3,6,8-tetra hydroxynaphthalene, and catechols. Melanin can interact with light in different ways, including Synthetic melanin is melanin-like material made either absorption, elastic scattering, and Raman scattering (inelastic), by enzymatic oxidation or by chemical oxidation of different of which absorption can lead to the generation of heat, fluores- monomers (Figure 1). Synthetic melanin has similar proper- cence, or even degradation in chemical structures (Figure 2A). ties to natural melanin, such as high absorption of light and In this section, we summarize the main studies on melanin- free radical quenching capability.[7] Synthetic eumelanin can be light interactions. made from dopamine,[13,14] dopa,[15] DHI,[16] or DHICA;[17] syn- thetic pheomelanin can be made from a mixture of dopa and cysteine;[18] synthetic neuromelanin may be made from either 2.2.1. Optical Absorption a mixture of polydopamine and cysteine or a mixture of dopa- mine and lysine;[19,20] and finally, synthetic allomelanin can be Three quantities describe how much a material absorbs light, made from DHN.[21] Synthetic melanin made from dopamine including mass specific absorptivity ε( , [cm2 mg−1]), absorp- (polydopamine) is most easily prepared, with good control of tion coefficientα ( , [cm−1]), and imaginary refractive index (k, the particle size, monodispersity, and ease of dispersal in solu- [unitless quantity]). These three quantities have been used to tion. In a typical synthesis process, dopamine hydrochloride is quantify melanin’s absorption and thus it is important to know oxidized and polymerized in NaOH aqueous solution.[13] Mono- the relationships between ε, α, and k to compare results from dispersity of polydopamine nanoparticles can be achieved by different studies. The imaginary refractive index defines the use of ammonium as the base source and a mixture of water bulk absorption property, while the mass specific absorptivity and short-chain alcohol as the reaction medium.[14] describes the absorption property of a material when it is dis- Polydopamine is one of the most widely studied synthetic solved in a solution. The absorption coefficient can be used in eumelanins,[6] and serves as a model eumelanin system to probe both cases and helps bridge the imaginary index to absorptivity. Adv. Optical Mater. 2020, 2000932 2000932 (2 of 15) © 2020 Wiley-VCH GmbH www.advancedsciencenews.com www.advopticalmat.de Figure 2. The interactions of melanin with light. A) Schematic to show melanin-light
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