Fabricated catecholic films are capable of redox-cycling and H2O2-generation in the absence of enzymes

Authors: KIM, EUNKYOUNG - University Of Maryland; XIAO, YI LIU - University Of Maryland; Baker, Con; Owens, Robert; BENTLEY, WILLIAM - University Of Maryland; PAYNE, GREGORY - University Of Maryland

Submitted to: Biomacromolecules
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/25/2011
Publication Date: 2/14/2011
Citation: Kim, E., Xiao, Y., Baker, C.J., Owens, R.A., Bentley, W.E., Payne, G.F. 2011. Fabricated catecholic films are capable of redox-cycling and H2O2-generation in the absence of enzymes. Biomacromolecules. 12:880-888.

Interpretive Summary: Polyphenols are key structural components of plant cell walls and are also generated by plants and animals in response to pathogen attack or adverse conditions. While these polymers function as physical barriers between the host and pathogen, they also retain a potent oxidative reactivity that offers additional defense functions against adversity. Their complex structures and the difficulty in isolating them from biological tissue have hampered investigation of their oxidative reactivity. To overcome these problems we have fabricated a synthetic polyphenolic matrix that has many properties in common with the biological matrix. One advantage of this approach is that the same electrochemical techniques used in the synthesis of this abiotic matrix can also be used to investigate its oxidative reactivity. Using this synthetic matrix, we have demonstrated that phenolic matrices possess catalytic activities in the absence of enzymes. Our results could have important implications/analogies for many diverse phenomena: the role of lignin and melanin in host-pathogen warfare; the involvement of neuromelanins in degenerative animal diseases; the possible non-enzymatic generation of reactive oxygen signaling molecules in plants and animals; and the importance of soluble and insoluble humus for controlling the oxidative environment in the soil.

Technical Abstract: The redox activity of quinones is integral to their physiological function in the electron transfer pathways of respiration and photosynthesis. Quinones and phenolic radicals are also intermediates in the biosynthesis of macromolecular structures (lignins and melanins) generated by plants and insects in response to pathogen attack. While these macromolecular phenols are believed to function as physical barriers between the host and pathogen, there are suggestions that these structures retain redox activity that offer additional defense functions. Evaluating these suggestions is complicated by the fact that these macromolecular phenols are positioned spatiotemporally at sites of substantial redox activity (e.g., an oxidative burst). Here we employed controllable electrochemical reactions both to fabricate a catechol-modified polysaccharide matrix and to probe the redox activity of this abiotic matrix. We demonstrate that this matrix can donate or accept electrons with common biological oxidizing/reducing systems. Further, these catechol-modified films were shown to possess context-dependent activities for redox cycling and reactive oxygen species (ROS) generation. The demonstration that these phenolic matrices possess catalytic activities in the absence of enzymes could have important implications/analogies for such diverse phenomena as: the role of phenolic matrices (e.g., lignin and melanin) in host-pathogen warfare; the participation of neuromelanins in degenerative diseases; the potential for ROS-generation by bactericidal antibiotics [7, 8]; the possible non-enzymatic generation of ROS signaling molecules; and the importance of soluble and insoluble humics for electron transfer in the environment.