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

Alford, Aaron; Kozlovskaya, Veronika; Xue, Bing; Gupta, Nirzari; Higgins, William; Pham-Hua, Dana; He, Lilin; Urban, Volker S.; Tse, Hubert M.; Kharlampieva, Eugenia

doi:10.1021/acs.chemmater.7b03502

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

Journal Article · Mon Dec 18 00:00:00 EST 2017 · Chemistry of Materials

DOI:https://doi.org/10.1021/acs.chemmater.7b03502· OSTI ID:1422484

Alford, Aaron ^[1]; Kozlovskaya, Veronika ^[1]; Xue, Bing ^[1]; Gupta, Nirzari ^[1]; Higgins, William ^[1]; Pham-Hua, Dana ^[2];

^[3];

^[3]; Tse, Hubert M. ^[2];

^[1]

Univ. of Alabama, Birmingham, AL (United States). Dept. of Chemistry
Univ. of Alabama, Birmingham, AL (United States). Dept. of Microbiology
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Neutron Scattering Division

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. In conclusion, 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.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF)

Grant/Contract Number:: AC05-00OR22725; DMR1608728

OSTI ID:: 1422484

Journal Information:: Chemistry of Materials, Vol. 30, Issue 2; ISSN 0897-4756

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 27 works

Citation information provided by
Web of Science

References (74)

Oxidative stress and metabolic syndrome Roberts, Christian K.; Sindhu, Kunal K. Life Sciences, Vol. 84, Issue 21-22 https://doi.org/10.1016/j.lfs.2009.02.026	journal	May 2009
Superoxide Production by Macrophages and T Cells Is Critical for the Induction of Autoreactivity and Type 1 Diabetes Thayer, T. C.; Delano, M.; Liu, C. Diabetes, Vol. 60, Issue 8 https://doi.org/10.2337/db10-1222	journal	June 2011
Effects of Metalloporphyrins on Reducing Inflammation and Autoimmunity Delmastro-Greenwood, Meghan M.; Tse, Hubert M.; Piganelli, Jon D. Antioxidants & Redox Signaling, Vol. 20, Issue 15 https://doi.org/10.1089/ars.2013.5257	journal	May 2014
Free radicals, natural antioxidants, and their reaction mechanisms Nimse, Satish Balasaheb; Pal, Dilipkumar RSC Advances, Vol. 5, Issue 35 https://doi.org/10.1039/C4RA13315C	journal	January 2015
The role of antioxidants and antioxidant-related enzymes in protective responses to environmentally induced oxidative stress Limón-Pacheco, Jorge; Gonsebatt, María E. Mutation Research/Genetic Toxicology and Environmental Mutagenesis, Vol. 674, Issue 1-2 https://doi.org/10.1016/j.mrgentox.2008.09.015	journal	March 2009
Manganic Porphyrins Possess Catalase Activity and Protect Endothelial Cells against Hydrogen Peroxide-Mediated Injury Day, Brian J.; Fridovich, Irwin; Crapo, James D. Archives of Biochemistry and Biophysics, Vol. 347, Issue 2 https://doi.org/10.1006/abbi.1997.0341	journal	November 1997
Design of the Complex between Manganese Porphyrins and Catalase−Poly(ethylene glycol) Conjugates for a New Antioxidant Asayama, Shoichiro; Hanawa, Tomochika; Nagaoka, Shoji Molecular Pharmaceutics, Vol. 4, Issue 3 https://doi.org/10.1021/mp060093c	journal	March 2007
Mechanistic analysis of the immunomodulatory effects of a catalytic antioxidant on antigen-presenting cells: implication for their use in targeting oxidation–reduction reactions in innate immunity Tse, H. Free Radical Biology and Medicine, Vol. 36, Issue 2 https://doi.org/10.1016/j.freeradbiomed.2003.10.029	journal	January 2004
Increased Manganese Superoxide Dismutase Expression or Treatment with Manganese Porphyrin Potentiates Dexamethasone-Induced Apoptosis in Lymphoma Cells Jaramillo, Melba C.; Frye, Jennifer B.; Crapo, James D. Cancer Research, Vol. 69, Issue 13 https://doi.org/10.1158/0008-5472.CAN-08-4031	journal	June 2009
Cytotoxic effects of Mn(III) N -alkylpyridylporphyrins in the presence of cellular reductant, ascorbate Ye, Xiaodong; Fels, Diane; Tovmasyan, Artak Free Radical Research, Vol. 45, Issue 11-12 https://doi.org/10.3109/10715762.2011.616199	journal	September 2011
New approach to the activation of anti-cancer pro-drugs by metalloporphyrin-based cytochrome P450 mimics in all-aqueous biologically relevant system Spasojević, Ivan; Colvin, O. Michael; Warshany, Keith R. Journal of Inorganic Biochemistry, Vol. 100, Issue 11 https://doi.org/10.1016/j.jinorgbio.2006.07.013	journal	November 2006
Reactions of Manganese Porphyrins with Peroxynitrite and Carbonate Radical Anion Ferrer-Sueta, Gerardo; Vitturi, Darío; Batinić-Haberle, Ines Journal of Biological Chemistry, Vol. 278, Issue 30 https://doi.org/10.1074/jbc.M213302200	journal	July 2003
Metalloporphyrins are potent inhibitors of lipid peroxidation Day, Brian J.; Batinic-Haberle, Ines; Crapo, James D. Free Radical Biology and Medicine, Vol. 26, Issue 5-6 https://doi.org/10.1016/S0891-5849(98)00261-5	journal	March 1999
A Metalloporphyrin-Based Superoxide Dismutase Mimic Inhibits Adoptive Transfer of Autoimmune Diabetes by a Diabetogenic T-Cell Clone Piganelli, J. D.; Flores, S. C.; Cruz, C. Diabetes, Vol. 51, Issue 2 https://doi.org/10.2337/diabetes.51.2.347	journal	February 2002
The potential role of peroxynitrite in the vascular contractile and cellular energetic failure in endotoxic shock: The role of superoxide or peroxynitrite in endotoxemia Zingarelli, Basilia; Day, Brian J.; Crapo, James D. British Journal of Pharmacology, Vol. 120, Issue 2 https://doi.org/10.1038/sj.bjp.0700872	journal	January 1997
Inhibition of Neuronal Apoptosis by a Metalloporphyrin Superoxide Dismutase Mimic Patel, Manisha Journal of Neurochemistry, Vol. 71, Issue 3 https://doi.org/10.1046/j.1471-4159.1998.71031068.x	journal	September 1998
A catalytic antioxidant metalloporphyrin blocks hydrogen peroxide-induced mitochondrial DNA damage Milano, J. Nucleic Acids Research, Vol. 28, Issue 4 https://doi.org/10.1093/nar/28.4.968	journal	February 2000
Scavenging ROS: Superoxide Dismutase/Catalase Mimetics by the Use of an Oxidation-Sensitive Nanocarrier/Enzyme Conjugate Hu, Ping; Tirelli, Nicola Bioconjugate Chemistry, Vol. 23, Issue 3 https://doi.org/10.1021/bc200449k	journal	February 2012
Polymerizable superoxide dismutase mimetic protects cells encapsulated in poly(ethylene glycol) hydrogels from reactive oxygen species-mediated damage Hume, Patrick S.; Anseth, Kristi S. Journal of Biomedical Materials Research Part A, Vol. 99A, Issue 1 https://doi.org/10.1002/jbm.a.33160	journal	July 2011
Porphyrin-Containing Electrospun Nanofibers: Positional Control of Porphyrin Molecules in Nanofibers and Their Catalytic Application Arai, Takuma; Tanaka, Manabu; Kawakami, Hiroyoshi ACS Applied Materials & Interfaces, Vol. 4, Issue 10 https://doi.org/10.1021/am3013664	journal	September 2012
Synthesis of Polymerizable Superoxide Dismutase Mimetics to Reduce Reactive Oxygen Species Damage in Transplanted Biomedical Devices Cheung, Charles Y.; McCartney, Suzanne J.; Anseth, Kristi S. Advanced Functional Materials, Vol. 18, Issue 20 https://doi.org/10.1002/adfm.200800566	journal	October 2008
Manganese porphyrin reduces renal injury and mitochondrial damage during ischemia/reperfusion Saba, Hamida; Batinic-Haberle, Ines; Munusamy, Shankar Free Radical Biology and Medicine, Vol. 42, Issue 10 https://doi.org/10.1016/j.freeradbiomed.2007.02.016	journal	May 2007
Release of Polyphenolic Drugs from Dynamically Bonded Layer-by-Layer Films Zhou, Lin; Chen, Mao; Tian, Lili ACS Applied Materials & Interfaces, Vol. 5, Issue 9 https://doi.org/10.1021/am4008787	journal	March 2013
Modified Polyelectrolyte Microcapsules as Smart Defense Systems Shchukin, Dmitry G.; Shutava, Tatsiana; Shchukina, Elena Chemistry of Materials, Vol. 16, Issue 18 https://doi.org/10.1021/cm049506x	journal	September 2004
Polyelectrolyte complex optimization for macrophage delivery of redox enzyme nanoparticles Zhao, Yuling; Haney, Matthew J.; Klyachko, Natalia L. Nanomedicine, Vol. 6, Issue 1 https://doi.org/10.2217/nnm.10.129	journal	January 2011
pH Responsive Decomposable Layer-by-Layer Nanofilms and Capsules on the Basis of Tannic Acid Shutava, Tatsiana; Prouty, Malcolm; Kommireddy, Dinesh Macromolecules, Vol. 38, Issue 7 https://doi.org/10.1021/ma047629x	journal	April 2005
Hydrogen-Bonded Multilayers of a Neutral Polymer and a Polyphenol Erel-Unal, Irem; Sukhishvili, Svetlana A. Macromolecules, Vol. 41, Issue 11 https://doi.org/10.1021/ma800186q	journal	May 2008
Responsive microcapsule reactors based on hydrogen-bonded tannic acid layer-by-layer assemblies Kozlovskaya, Veronika; Kharlampieva, Eugenia; Drachuk, Irina Soft Matter, Vol. 6, Issue 15 https://doi.org/10.1039/b927369g	journal	January 2010
One-Step Assembly of Coordination Complexes for Versatile Film and Particle Engineering Ejima, H.; Richardson, J. J.; Liang, K. Science, Vol. 341, Issue 6142 https://doi.org/10.1126/science.1237265	journal	July 2013
Metal-Phenolic Supramolecular Gelation Rahim, Md. Arifur; Björnmalm, Mattias; Suma, Tomoya Angewandte Chemie International Edition, Vol. 55, Issue 44 https://doi.org/10.1002/anie.201608413	journal	September 2016
Modular assembly of superstructures from polyphenol-functionalized building blocks Guo, Junling; Tardy, Blaise L.; Christofferson, Andrew J. Nature Nanotechnology, Vol. 11, Issue 12 https://doi.org/10.1038/nnano.2016.172	journal	October 2016
Ultrathin Polymeric Coatings Based on Hydrogen-Bonded Polyphenol for Protection of Pancreatic Islet Cells Kozlovskaya, Veronika; Zavgorodnya, Oleksandra; Chen, Yi Advanced Functional Materials, Vol. 22, Issue 16 https://doi.org/10.1002/adfm.201200138	journal	April 2012
Biocompatible Shaped Particles from Dried Multilayer Polymer Capsules Chen, Jun; Kozlovskaya, Veronika; Goins, Allison Biomacromolecules, Vol. 14, Issue 11 https://doi.org/10.1021/bm4008666	journal	October 2013
Nanoporous Hydrogen Bonded Polymeric Microparticles: Facile and Economic Production of Cross Presentation Promoting Vaccine Carriers Dierendonck, Marijke; Fierens, Kaat; De Rycke, Riet Advanced Functional Materials, Vol. 24, Issue 29 https://doi.org/10.1002/adfm.201400763	journal	April 2014
Self-Defensive Layer-by-Layer Films with Bacteria-Triggered Antibiotic Release Zhuk, Iryna; Jariwala, Freneil; Attygalle, Athula B. ACS Nano, Vol. 8, Issue 8 https://doi.org/10.1021/nn500674g	journal	July 2014
Hollow capsules formed in a single stage via interfacial hydrogen-bonded complexation of methylcellulose with poly(acrylic acid) and tannic acid Driver, Krystie; Baco, Sara; Khutoryanskiy, Vitaliy V. European Polymer Journal, Vol. 49, Issue 12 https://doi.org/10.1016/j.eurpolymj.2013.10.004	journal	December 2013
Hemostatic Multilayer Coatings Shukla, Anita; Fang, Jean C.; Puranam, Sravanthi Advanced Materials, Vol. 24, Issue 4 https://doi.org/10.1002/adma.201103794	journal	December 2011
Theranostic Multilayer Capsules for Ultrasound Imaging and Guided Drug Delivery Chen, Jun; Ratnayaka, Sithira; Alford, Aaron ACS Nano, Vol. 11, Issue 3 https://doi.org/10.1021/acsnano.7b00151	journal	February 2017
Polyphenolic Polymersomes of Temperature-Sensitive Poly( N -vinylcaprolactam)- block -Poly( N -vinylpyrrolidone) for Anticancer Therapy Kozlovskaya, Veronika; Liu, Fei; Xue, Bing Biomacromolecules, Vol. 18, Issue 8 https://doi.org/10.1021/acs.biomac.7b00687	journal	July 2017
Islet encapsulation with polyphenol coatings decreases pro-inflammatory chemokine synthesis and T cell trafficking Pham-Hua, Dana; Padgett, Lindsey E.; Xue, Bing Biomaterials, Vol. 128 https://doi.org/10.1016/j.biomaterials.2017.03.002	journal	June 2017
Hydrogen-Bonded Multilayers of Tannic Acid as Mediators of T-Cell Immunity Kozlovskaya, Veronika; Xue, Bing; Lei, Weiqi Advanced Healthcare Materials, Vol. 4, Issue 5 https://doi.org/10.1002/adhm.201400657	journal	December 2014
Preparation of Tetracationic Metalloporphyrin−Spermine Conjugates Jakobs, Andreas; Bernadou, Jean; Meunier, Bernard The Journal of Organic Chemistry, Vol. 62, Issue 11 https://doi.org/10.1021/jo9620831	journal	May 1997
Reaction of radical cations with multilayers of tannic acid and polyelectrolytes Shutova, T. G.; Agabekov, V. E.; Lvov, Y. M. Russian Journal of General Chemistry, Vol. 77, Issue 9 https://doi.org/10.1134/S1070363207090034	journal	September 2007
Influence of Water-Soluble Polymers on the Shear-Induced Structure Formation in Lyotropic Lamellar Phases Berghausen, Jörg; Zipfel, Johannes; Lindner, Peter The Journal of Physical Chemistry B, Vol. 105, Issue 45 https://doi.org/10.1021/jp0115897	journal	November 2001
Reduction and analysis of SANS and USANS data using IGOR Pro Kline, Steven R. Journal of Applied Crystallography, Vol. 39, Issue 6, p. 895-900 https://doi.org/10.1107/S0021889806035059	journal	November 2006
Design of Metalloporphyrin−Carbohydrate Conjugates for a New Superoxide Dismutase Mimic with Cellular Recognition Asayama, Shoichiro; Mizushima, Kaori; Nagaoka, Shoji Bioconjugate Chemistry, Vol. 15, Issue 6 https://doi.org/10.1021/bc049865i	journal	November 2004
Magnetic nanoparticles supported manganese(III) tetrapyridylporphyrin catalyst via covalent interaction: A highly efficient and reusable catalyst for the oxidation of hydrocarbons Saeedi, Mohammad Saleh; Tangestaninejad, Shahram; Moghadam, Majid Polyhedron, Vol. 49, Issue 1 https://doi.org/10.1016/j.poly.2012.09.026	journal	January 2013
Vibration and Fluorescence Spectra of Porphyrin- CoredBis(methylol)-propionic Acid Dendrimers Minaev, Boris; Lindgren, Mikael Sensors, Vol. 9, Issue 3 https://doi.org/10.3390/s90301937	journal	March 2009
Encapsulation of anticancer drug by hydrogen-bonded multilayers of tannic acid Liu, Fei; Kozlovskaya, Veronika; Zavgorodnya, Oleksandra Soft Matter, Vol. 10, Issue 46 https://doi.org/10.1039/C4SM01813C	journal	January 2014
Ionization and pH Stability of Multilayers Formed by Self-Assembly of Weak Polyelectrolytes Kharlampieva, Eugenia; Sukhishvili, Svetlana A. Langmuir, Vol. 19, Issue 4 https://doi.org/10.1021/la026546b	journal	February 2003
pH-Responsive Layered Hydrogel Microcapsules as Gold Nanoreactors Kozlovskaya, Veronika; Kharlampieva, Eugenia; Chang, Sehoon Chemistry of Materials, Vol. 21, Issue 10 https://doi.org/10.1021/cm900314p	journal	April 2009
Elasticity of hollow polyelectrolyte capsules prepared by the layer-by-layer technique Gao, C.; Donath, E.; Moya, S. The European Physical Journal E, Vol. 5, Issue 1 https://doi.org/10.1007/s101890170083	journal	May 2001
Single Polyelectrolyte Microcapsules Fabricated By Glutaraldehyde-Mediated Covalent Layer-By-Layer Assembly Tong, Weijun; Gao, Changyou; Möhwald, Helmuth Macromolecular Rapid Communications, Vol. 27, Issue 24 https://doi.org/10.1002/marc.200600533	journal	December 2006
Preparation and application of single polyelectrolyte microcapsules possessing tunable autofluorescent properties Wang, Zhongjun; Zhu, Hui; Li, Dan Colloids and Surfaces A: Physicochemical and Engineering Aspects, Vol. 329, Issue 1-2 https://doi.org/10.1016/j.colsurfa.2008.06.050	journal	October 2008
Hydrophobicity: an ancient damage-associated molecular pattern that initiates innate immune responses Seong, Seung-Yong; Matzinger, Polly Nature Reviews Immunology, Vol. 4, Issue 6 https://doi.org/10.1038/nri1372	journal	June 2004
Nanoparticle Hydrophobicity Dictates Immune Response Moyano, Daniel F.; Goldsmith, Meir; Solfiell, David J. Journal of the American Chemical Society, Vol. 134, Issue 9 https://doi.org/10.1021/ja2108905	journal	February 2012
Effect of Poly( N -vinyl-pyrrolidone)- block -poly( d , l -lactide) as Coating Agent on the Opsonization, Phagocytosis, and Pharmacokinetics of Biodegradable Nanoparticles Gaucher, Geneviève; Asahina, Kinji; Wang, Jiaohong Biomacromolecules, Vol. 10, Issue 2 https://doi.org/10.1021/bm801178f	journal	January 2009
Decreased material-activation of the complement system using low-energy plasma polymerized poly(vinyl pyrrolidone) coatings Andersen, Thomas E.; Palarasah, Yaseelan; Skjødt, Mikkel-Ole Biomaterials, Vol. 32, Issue 20 https://doi.org/10.1016/j.biomaterials.2011.03.002	journal	July 2011
Emissive nanoparticles from pyridinium-substituted tetraphenylethylene salts: imaging and selective cytotoxicity towards cancer cells in vitro and in vivo by varying counter anions Huang, Yanyan; Zhang, Guanxin; Hu, Fang Chemical Science, Vol. 7, Issue 12 https://doi.org/10.1039/C6SC02395A	journal	January 2016
Manganese-induced oxidative DNA damage in neuronal SH-SY5Y cells: Attenuation of thymine base lesions by glutathione and N-acetylcysteine Stephenson, Adrienne P.; Schneider, Jeffrey A.; Nelson, Bryant C. Toxicology Letters, Vol. 218, Issue 3 https://doi.org/10.1016/j.toxlet.2012.12.024	journal	April 2013
Protective Effects of Curcumin on Manganese-Induced BV-2 Microglial Cell Death Park, Euteum; Chun, Hong Sung Biological & Pharmaceutical Bulletin, Vol. 40, Issue 8 https://doi.org/10.1248/bpb.b17-00160	journal	January 2017
THE NOD MOUSE: A Model of Immune Dysregulation Anderson, Mark S.; Bluestone, Jeffrey A. Annual Review of Immunology, Vol. 23, Issue 1 https://doi.org/10.1146/annurev.immunol.23.021704.115643	journal	April 2005
Catalytic antioxidant therapy by metallodrugs: lessons from metallocorroles Haber, Adi; Gross, Zeev Chemical Communications, Vol. 51, Issue 27 https://doi.org/10.1039/C4CC08715A	journal	January 2015
Kinetics of oxidation of benzyl alcohols by the dication and radical cation of ABTS. Comparison with laccase–ABTS oxidations: an apparent paradox Branchi, Barbara; Galli, Carlo; Gentili, Patrizia Organic & Biomolecular Chemistry, Vol. 3, Issue 14 https://doi.org/10.1039/b504199f	journal	January 2005
New PEG-ylated Mn( iii ) porphyrins approaching catalytic activity of SOD enzyme Batinić-Haberle, Ines; Spasojević, Ivan; Stevens, Robert D. Dalton Trans., Issue 4 https://doi.org/10.1039/B513761F	journal	January 2006
Oxidation of reduced cytochrome c by hydrogen peroxide: Implications for Superoxide assays Vandewalle, P. L.; Petersen, N. O. FEBS Letters, Vol. 210, Issue 2 https://doi.org/10.1016/0014-5793(87)81336-4	journal	January 1987
One-electron transfer reactions in biochemical systems. VIII. Kinetic study of superoxide dismutase Sawada, Yukiharu; Yamazaki, Isao Biochimica et Biophysica Acta (BBA) - Enzymology, Vol. 327, Issue 2 https://doi.org/10.1016/0005-2744(73)90408-7	journal	December 1973
The extinction coefficient of cytochrome c Van Gelder, B. F.; Slater, E. C. Biochimica et Biophysica Acta, Vol. 58, Issue 3 https://doi.org/10.1016/0006-3002(62)90073-2	journal	April 1962
Microcapsule Modification with Peroxidase-Catalyzed Phenol Polymerization Shutava, Tatsiana; Zheng, Zhiguo; John, Vijay Biomacromolecules, Vol. 5, Issue 3 https://doi.org/10.1021/bm034476x	journal	May 2004
Small Angle Neutron Scattering Investigations (SANS) of Polyelectrolyte Multilayer Capsules Templated on Human Red Blood Cells Estrela-Lopis, Irina; Leporatti, Stefano; Typlt, Elke Langmuir, Vol. 23, Issue 13 https://doi.org/10.1021/la700496c	journal	June 2007
Polyelectrolyte multilayer hollow capsules studied by small-angle neutron scattering (SANS) Estrela-Lopis, Irina; Leporatti, Stefano; Clemens, Daniel Soft Matter, Vol. 5, Issue 1 https://doi.org/10.1039/B810363A	journal	January 2009
Direct Probing of Micromechanical Properties of Hydrogen-Bonded Layer-by-Layer Microcapsule Shells with Different Chemical Compositions Lisunova, Milana O.; Drachuk, Irina; Shchepelina, Olga A. Langmuir, Vol. 27, Issue 17 https://doi.org/10.1021/la202082w	journal	September 2011
Structure of Guar in Solutions of H ₂ O and D ₂ O: An Ultra-Small-Angle Light-Scattering Study Gittings, M. R.; Cipelletti, Luca; Trappe, V. The Journal of Physical Chemistry B, Vol. 104, Issue 18 https://doi.org/10.1021/jp9943833	journal	May 2000
Reaction of Phenols with Peroxy Radicals Ingold, K. U.; Howard, J. A. Nature, Vol. 195, Issue 4838 https://doi.org/10.1038/195280b0	journal	July 1962

Cited By (3)

Layer‐by‐Layer Cerium Oxide Nanoparticle Coating for Antioxidant Protection of Encapsulated Beta Cells Abuid, Nicholas J.; Gattás‐Asfura, Kerim M.; Schofield, Emily A. Advanced Healthcare Materials, Vol. 8, Issue 12 https://doi.org/10.1002/adhm.201801493	journal	October 2018
Phenolische Bausteine für die Assemblierung von Funktionsmaterialien Rahim, Md. Arifur; Kristufek, Samantha L.; Pan, Shuaijun Angewandte Chemie https://doi.org/10.1002/ange.201807804	journal	December 2018
Phenolic Building Blocks for the Assembly of Functional Materials Rahim, Md. Arifur; Kristufek, Samantha L.; Pan, Shuaijun Angewandte Chemie International Edition, Vol. 58, Issue 7 https://doi.org/10.1002/anie.201807804	journal	February 2019

Figures / Tables (10)

Similar Records

Temperature controlled transformations of giant unilamellar vesicles of amphiphilic triblock copolymers synthesized via microfluidic mixing

Journal Article · Wed May 26 00:00:00 EDT 2021 · Applied Surface Science Advances · OSTI ID:1422484

Yang, Yiming; Kozlovskaya, Veronika; Dolmat, Maksim; +5 more

Inhibition of rat liver microsomal lipid peroxidation by N-acyldehydroalanines: An in vitro comparative study

Journal Article · Fri Sep 01 00:00:00 EDT 1989 · Archives of Biochemistry and Biophysics; (USA) · OSTI ID:1422484

Buc-Calderon, P; Roberfroid, M

Oxidative stress is involved in Dasatinib-induced apoptosis in rat primary hepatocytes

Journal Article · Fri Jun 15 00:00:00 EDT 2012 · Toxicology and Applied Pharmacology · OSTI ID:1422484

Xue, Tao; Luo, Peihua; Zhu, Hong; +7 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
60 APPLIED LIFE SCIENCES
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY