Dispersibility-Dependent Biodegradation of Graphene Oxide by Myeloperoxidase.

Understanding human health risk associated with the rapidly emerging graphene-based nanomaterials represents a great challenge because of the diversity of applications and the wide range of possible ways of exposure to this type of materials. Herein, the biodegradation of graphene oxide (GO) sheets is reported by using myeloperoxidase (hMPO) derived from human neutrophils in the presence of a low concentration of hydrogen peroxide. The degradation capability of the enzyme on three different GO samples containing different degree of oxidation on their graphenic lattice, leading to a variable dispersibility in aqueous media is compared. hMPO fails in degrading the most aggregated GO, but succeeds to completely metabolize highly dispersed GO samples. The spectroscopy and microscopy analyses provide unambiguous evidence for the key roles played by hydrophilicity, negative surface charge, and colloidal stability of the aqueous GO in their biodegradation by hMPO catalysis.

[1]  Martin Fischlechner,et al.  Myeloperoxidase binds to non-vital spermatozoa on phosphatidylserine epitopes , 2007, Apoptosis.

[2]  A. Sokolov,et al.  Myeloperoxidase-induced biodegradation of single-walled carbon nanotubes is mediated by hypochlorite , 2011, Russian Journal of Bioorganic Chemistry.

[3]  M. Davies,et al.  Hypochlorite-mediated fragmentation of hyaluronan, chondroitin sulfates, and related N-acetyl glycosamines: evidence for chloramide intermediates, free radical transfer reactions, and site-specific fragmentation. , 2003, Journal of the American Chemical Society.

[4]  M. Prato,et al.  In vivo degradation of functionalized carbon nanotubes after stereotactic administration in the brain cortex. , 2012, Nanomedicine.

[5]  A. Star,et al.  Insight into the Mechanism of Graphene Oxide Degradation via the Photo-Fenton Reaction , 2014, The journal of physical chemistry. C, Nanomaterials and interfaces.

[6]  J. Eaton,et al.  Degradation of biomaterials by phagocyte-derived oxidants. , 1993, The Journal of clinical investigation.

[7]  Yong Zhao,et al.  Nano-Gold Corking and Enzymatic Uncorking of Carbon Nanotube Cups , 2014, Journal of the American Chemical Society.

[8]  T. Filley,et al.  Oxidative enzymatic response of white-rot fungi to single-walled carbon nanotubes. , 2014, Environmental pollution.

[9]  Y. Liu,et al.  Understanding the toxicity of carbon nanotubes. , 2013, Accounts of chemical research.

[10]  A. Ferrari,et al.  Raman spectroscopy of graphene and graphite: Disorder, electron phonon coupling, doping and nonadiabatic effects , 2007 .

[11]  A. Benayad,et al.  Selective oxidation on metallic carbon nanotubes by halogen oxoanions. , 2008, Journal of the American Chemical Society.

[12]  C. Weber,et al.  Mechanisms underlying neutrophil-mediated monocyte recruitment. , 2009, Blood.

[13]  Kai Yang,et al.  Nano-graphene in biomedicine: theranostic applications. , 2013, Chemical Society reviews.

[14]  Prashant V. Kamat,et al.  Is Graphene a Stable Platform for Photocatalysis? Mineralization of Reduced Graphene Oxide With UV-Irradiated TiO2 Nanoparticles , 2014 .

[15]  M. Sperandio,et al.  Myeloperoxidase attracts neutrophils by physical forces. , 2011, Blood.

[16]  P. Rieu,et al.  Neutrophils: Molecules, Functions and Pathophysiological Aspects , 2000, Laboratory Investigation.

[17]  Jingyan Zhang,et al.  Photo-Fenton reaction of graphene oxide: a new strategy to prepare graphene quantum dots for DNA cleavage. , 2012, ACS nano.

[18]  Alberto Bianco,et al.  Graphene: safe or toxic? The two faces of the medal. , 2013, Angewandte Chemie.

[19]  J. Klein-Seetharaman,et al.  The enzymatic oxidation of graphene oxide. , 2011, ACS nano.

[20]  Moreno Meneghetti,et al.  Evidencing the mask effect of graphene oxide: a comparative study on primary human and murine phagocytic cells. , 2013, Nanoscale.

[21]  Valerian E. Kagan,et al.  Lung Macrophages “Digest” Carbon Nanotubes Using a Superoxide/Peroxynitrite Oxidative Pathway , 2014, ACS nano.

[22]  H. Ploehn,et al.  Quantitative Analysis of Montmorillonite Platelet Size by Atomic Force Microscopy , 2006 .

[23]  Bengt Fadeel,et al.  Impaired Clearance and Enhanced Pulmonary Inflammatory/Fibrotic Response to Carbon Nanotubes in Myeloperoxidase-Deficient Mice , 2012, PloS one.

[24]  Bengt Fadeel,et al.  Enzymatic 'stripping' and degradation of PEGylated carbon nanotubes. , 2014, Nanoscale.

[25]  W. Lu,et al.  Improved synthesis of graphene oxide. , 2010, ACS nano.

[26]  Kai Yang,et al.  Surface coating-dependent cytotoxicity and degradation of graphene derivatives: towards the design of non-toxic, degradable nano-graphene. , 2014, Small.

[27]  G. Wallace,et al.  Processable aqueous dispersions of graphene nanosheets. , 2008, Nature nanotechnology.

[28]  Kai Yang,et al.  Behavior and toxicity of graphene and its functionalized derivatives in biological systems. , 2013, Small.

[29]  Judith Klein-Seetharaman,et al.  Mechanistic investigations of horseradish peroxidase-catalyzed degradation of single-walled carbon nanotubes. , 2009, Journal of the American Chemical Society.

[30]  G. Cox,et al.  Macrophage engulfment of apoptotic neutrophils contributes to the resolution of acute pulmonary inflammation in vivo. , 1995, American journal of respiratory cell and molecular biology.

[31]  M. Davies.  Myeloperoxidase-derived oxidation: mechanisms of biological damage and its prevention , 2010, Journal of clinical biochemistry and nutrition.

[32]  W. Liles,et al.  The phagocytes: neutrophils and monocytes. , 2008, Blood.

[33]  Abhilash Sasidharan,et al.  Confocal Raman Imaging Study Showing Macrophage Mediated Biodegradation of Graphene In Vivo , 2013, Advanced healthcare materials.

[34]  K. Novoselov,et al.  Exploring the Interface of Graphene and Biology , 2014, Science.

[35]  A. Sokolov,et al.  PEGylated single-walled carbon nanotubes activate neutrophils to increase production of hypochlorous acid, the oxidant capable of degrading nanotubes. , 2012, Toxicology and applied pharmacology.

[36]  M. Dresselhaus,et al.  Perspectives on carbon nanotubes and graphene Raman spectroscopy. , 2010, Nano letters.

[37]  M. Melucci,et al.  High-contrast visualization of graphene oxide on dye-sensitized glass, quartz, and silicon by fluorescence quenching. , 2009, Journal of the American Chemical Society.

[38]  SUPARNA DUTTASINHA,et al.  Graphene: Status and Prospects , 2009, Science.

[39]  S. A. Hasan,et al.  A natural vanishing act: the enzyme-catalyzed degradation of carbon nanomaterials. , 2012, Accounts of chemical research.

[40]  B. Hong,et al.  Prospects and Challenges of Graphene in Biomedical Applications , 2013, Advanced materials.

[41]  A. Star,et al.  Effect of antioxidants on enzyme-catalysed biodegradation of carbon nanotubes. , 2013, Journal of materials chemistry. B.

[42]  Yong Zhao,et al.  Peroxidase-mediated biodegradation of carbon nanotubes in vitro and in vivo. , 2013, Advanced drug delivery reviews.

[43]  Yong Zhao,et al.  Enzymatic degradation of multiwalled carbon nanotubes. , 2011, The journal of physical chemistry. A.

[44]  Judith Klein-Seetharaman,et al.  Biodegradation of single-walled carbon nanotubes by eosinophil peroxidase. , 2013, Small.

[45]  H. Schoemaker,et al.  Enantioselective Epoxidation and Carbon–Carbon Bond Cleavage Catalyzed by Coprinus cinereus Peroxidase and Myeloperoxidase* , 2000, The Journal of Biological Chemistry.

[46]  Judith Klein-Seetharaman,et al.  Carbon nanotubes degraded by neutrophil myeloperoxidase induce less pulmonary inflammation. , 2010, Nature nanotechnology.

[47]  P. Kamat,et al.  Making graphene holey. Gold-nanoparticle-mediated hydroxyl radical attack on reduced graphene oxide. , 2013, ACS nano.

[48]  U. Meyer-Hoffert,et al.  Neutrophil serine proteases: mediators of innate immune responses , 2011, Current opinion in hematology.

[49]  A. Raichur,et al.  Graphene oxide based multilayer capsules with unique permeability properties: facile encapsulation of multiple drugs. , 2012, Chemical communications.

[50]  Alexander Star,et al.  Biodegradation of single-walled carbon nanotubes through enzymatic catalysis. , 2008, Nano letters.

[51]  B. Hong,et al.  Biomedical applications of graphene and graphene oxide. , 2013, Accounts of chemical research.

[52]  P. Baron,et al.  Inhalation vs. aspiration of single-walled carbon nanotubes in C57BL/6 mice: inflammation, fibrosis, oxidative stress, and mutagenesis. , 2008, American journal of physiology. Lung cellular and molecular physiology.

[53]  Nelson Durán,et al.  Nanotoxicity of graphene and graphene oxide. , 2014, Chemical research in toxicology.

[54]  Sang-Jae Kim,et al.  The chemical and structural analysis of graphene oxide with different degrees of oxidation , 2013 .

[55]  Balaji Sitharaman,et al.  Enzymatic Degradation of Oxidized and Reduced Graphene Nanoribbons by Lignin Peroxidase. , 2014, Journal of materials chemistry. B.

[56]  Kostas Kostarelos,et al.  Safety considerations for graphene: lessons learnt from carbon nanotubes. , 2013, Accounts of chemical research.

[57]  Jiayu Li,et al.  Binding of human serum albumin to single-walled carbon nanotubes activated neutrophils to increase production of hypochlorous acid, the oxidant capable of degrading nanotubes. , 2014, Chemical research in toxicology.

[58]  Ken Donaldson,et al.  Graphene-based nanoplatelets: a new risk to the respiratory system as a consequence of their unusual aerodynamic properties. , 2012, ACS nano.

[59]  Cheol-Woong Yang,et al.  Evidence of graphitic AB stacking order of graphite oxides. , 2008, Journal of the American Chemical Society.

[60]  M. M. Lucchese,et al.  Quantifying ion-induced defects and Raman relaxation length in graphene , 2010 .

[61]  M. Davies,et al.  Heparan sulfate degradation via reductive homolysis of its N-chloro derivatives. , 2006, Journal of the American Chemical Society.

[62]  Richard Beanland,et al.  Graphene oxide: structural analysis and application as a highly transparent support for electron microscopy. , 2009, ACS nano.