Manganoporphyrin-Polyphenol Multilayer Capsules as Radical and Reactive Oxygen Species (ROS) Scavengers

被引:36
作者
Alford, Aaron [1 ]
Kozlovskaya, Veronika [1 ]
Xue, Bing [1 ]
Gupta, Nirzari [1 ]
Higgins, William [1 ]
Dana Pham-Hua [2 ]
He, Lilin [3 ]
Urban, Volker S. [3 ]
Tse, Hubert M. [2 ]
Kharlampieva, Eugenia [1 ]
机构
[1] Univ Alabama Birmingham, Dept Chem, Birmingham, AL 35294 USA
[2] Univ Alabama Birmingham, Dept Microbiol, Birmingham, AL 35294 USA
[3] Oak Ridge Natl Lab, Neutron Scattering Div, Oak Ridge, TN 37831 USA
基金
美国国家科学基金会;
关键词
HYDROGEN-BONDED MULTILAYERS; BY-LAYER FILMS; SUPEROXIDE-DISMUTASE; TANNIC-ACID; POLYELECTROLYTE MICROCAPSULES; CATALYTIC ANTIOXIDANT; MANGANESE PORPHYRINS; OXIDATIVE STRESS; CYTOCHROME-C; DNA-DAMAGE;
D O I
10.1021/acs.chemmater.7b03502
中图分类号
O64 [物理化学(理论化学)、化学物理学];
学科分类号
070304 ; 081704 ;
摘要
Local modulation of oxidative stress is crucial for a variety of biochemical events including cellular differentiation, apoptosis, and defense against pathogens. Currently employed natural and synthetic antioxidants exhibit a lack of biocompatibility, bioavailability, and chemical stability, resulting in limited capability to scavenge reactive oxygen species (ROS). To mediate these drawbacks, we have developed a synergistic manganoporphyrin-polyphenol polymeric nanothin coating and hollow microcapsules with efficient antioxidant activity and controllable ROS modulation. These materials are produced by multilayer assembly of a natural polyphenolic antioxidant, tannic acid (TA), with a synthesized copolymer of polyvinylpyrrolidone containing a manganoporphyrin modality (MnP-PVPON) which mimics the enzymatic antioxidant superoxide dismutase. The redox activity of the copolymer is demonstrated to dramatically increase the antioxidant response of MnP-PVPON/TA capsules versus unmodified PVPON/TA capsules through reduction of a radical cationic dye and to significantly suppress the proliferation of superoxide via cytochrome C competition. Inclusion of MnP-PVPON as an outer layer enhances radical-scavenging activity as compared to localization of the layer in the middle or inner part of the capsule shell. In addition, we demonstrate that TA is crucial for the synergistic radical-scavenging activity of the MnP-PVPON/TA system which exhibits a combined superoxide dismutase-like ability and catalase-like activity in response to the free radical superoxide challenge. The MnP-PVPON/TA capsules exhibit a negligible, 8% loss of shell thickness upon free radical treatment, while PVPON/TA capsules lose 39% of their shell thickness due to the noncatalytic free-radical-scavenging of TA, as demonstrated by small angle neutron scattering (SANS). Finally, we have found the manganoporphyrin-polyphenol capsules to be nontoxic to splenocytes from NOD mice after 48 h incubation. Our study illustrates the strong potential of combining catalytic activity of manganoporphyrins with natural polyphenolic antioxidants to design efficient free-radical-scavenging materials that may eventually be used in antioxidant therapies and as free radical dissipating protective carriers of biomolecules for biomedical or industrial applications.
引用
收藏
页码:344 / 357
页数:14
相关论文
共 74 条
[1]   Decreased material-activation of the complement system using low-energy plasma polymerized poly(vinyl pyrrolidone) coatings [J].
Andersen, Thomas E. ;
Palarasah, Yaseelan ;
Skjodt, Mikkel-Ole ;
Ogaki, Ryosuke ;
Benter, Maike ;
Alei, Mojagan ;
Kolmos, Hans J. ;
Koch, Claus ;
Kingshott, Peter .
BIOMATERIALS, 2011, 32 (20) :4481-4488
[2]   The NOD mouse: A model of immune dysregulation [J].
Anderson, MS ;
Bluestone, JA .
ANNUAL REVIEW OF IMMUNOLOGY, 2005, 23 :447-485
[3]   Porphyrin-Containing Electrospun Nanofibers: Positional Control of Porphyrin Molecules in Nanofibers and Their Catalytic Application [J].
Arai, Takuma ;
Tanaka, Manabu ;
Kawakami, Hiroyoshi .
ACS APPLIED MATERIALS & INTERFACES, 2012, 4 (10) :5453-5457
[4]   Design of metalloporphyrin-carbohydrate conjugates for a new superoxide dismutase mimic with cellular recognition [J].
Asayama, S ;
Mizushima, K ;
Nagaoka, S ;
Kawakami, H .
BIOCONJUGATE CHEMISTRY, 2004, 15 (06) :1360-1363
[5]   Design of the complex between manganese porphyrins and catalase-poly(ethylene glycol) conjugates for a new antioxidant [J].
Asayama, Shoichiro ;
Hanawa, Tomochika ;
Nagaoka, Shoji ;
Kawakami, Hiroyoshi .
MOLECULAR PHARMACEUTICS, 2007, 4 (03) :484-486
[6]   New PEG-ylated Mn(III) porphyrins approaching catalytic activity of SOD enzyme [J].
Batinic-Haberle, I ;
Spasojevic, I ;
Stevens, RD ;
Bondurant, B ;
Okado-Matsumoto, A ;
Fridovich, I ;
Vujaskovic, Z ;
Dewhirst, MW .
DALTON TRANSACTIONS, 2006, (04) :617-624
[7]   Influence of water-soluble polymers on the shear-induced structure formation in lyotropic lamellar phases [J].
Berghausen, J ;
Zipfel, J ;
Lindner, P ;
Richtering, W .
JOURNAL OF PHYSICAL CHEMISTRY B, 2001, 105 (45) :11081-11088
[8]   Kinetics of oxidation of benzyl alcohols by the dication and radical cation of ABTS. Comparison with laccase-ABTS oxidations: an apparent paradox [J].
Branchi, B ;
Galli, C ;
Gentili, P .
ORGANIC & BIOMOLECULAR CHEMISTRY, 2005, 3 (14) :2604-2614
[9]   Theranostic Multilayer Capsules for Ultrasound Imaging and Guided Drug Delivery [J].
Chen, Jun ;
Ratnayaka, Sithira ;
Alford, Aaron ;
Kozlovskaya, Veronika ;
Liu, Fei ;
Xue, Bing ;
Hoyt, Kenneth ;
Kharlampieva, Eugenia .
ACS NANO, 2017, 11 (03) :3135-3146
[10]   Biocompatible Shaped Particles from Dried Multilayer Polymer Capsules [J].
Chen, Jun ;
Kozlovskaya, Veronika ;
Goins, Allison ;
Campos-Gomez, Javier ;
Saeed, Mohammad ;
Kharlampieva, Eugenia .
BIOMACROMOLECULES, 2013, 14 (11) :3830-3841