Specific nanotoxicity of graphene oxide during zebrafish embryogenesis

Abstract Graphene oxide (GO) has shown great potential for biological, medical, energy and electronic applications. As a consequence of these diverse applications, GO release into the ecosystem is inevitable; however, the corresponding risks are largely unknown, particularly with respect to the critical period of embryogenesis. This study revealed that GO adhered to and enveloped the chorion of zebrafish embryos mainly via hydroxyl group interactions, blocked the pore canals of the chorionic membrane, and caused marked hypoxia and hatching delay. Furthermore, GO spontaneously penetrated the chorion, entered the embryo via endocytosis, damaged the mitochondria and primarily translocated to the eye, heart and yolk sac regions, which are involved in the circulatory system of zebrafish. In these organs, GO induced excessive generation of reactive oxygen species and increased oxidative stress, DNA damage and apoptosis. Graphene oxide also induced developmental malformation of the eye, cardiac/yolk sac edema, tail flexure and heart rate reduction. In contrast to the common dose-effect relationships of nanoparticles, the adverse effects of GO on heart rate and tail/spinal cord flexure increased and then decreased as the GO concentration increased. These findings emphasize the specific adverse effects of GO on embryogenesis and highlight the potential ecological and health risks of GO.

[1]  K. Wu,et al.  The zerovalent iron nanoparticle causes higher developmental toxicity than its oxidation products in early life stages of medaka fish. , 2013, Water research.

[2]  L. Fan,et al.  The uptake mechanism and biocompatibility of graphene quantum dots with human neural stem cells. , 2014, Nanoscale.

[3]  S. Hua,et al.  Natrium fluoride influences methylation modifications and induces apoptosis in mouse early embryos. , 2014, Environmental science & technology.

[4]  E. Durand,et al.  Impact of dietary cadmium sulphide nanoparticles on Danio rerio zebrafish at very low contamination pressure , 2014, Nanotoxicology.

[5]  V. Maheshwari,et al.  Adsorption and desorption of DNA on graphene oxide studied by fluorescently labeled oligonucleotides. , 2011, Langmuir : the ACS journal of surfaces and colloids.

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

[7]  M. Mahmoudi,et al.  Graphene oxide strongly inhibits amyloid beta fibrillation. , 2012, Nanoscale.

[8]  Si-Shen Feng,et al.  Effects of particle size and surface coating on cellular uptake of polymeric nanoparticles for oral delivery of anticancer drugs. , 2005, Biomaterials.

[9]  C. Liao,et al.  Assessing the potential risks to zebrafish posed by environmentally relevant copper and silver nanoparticles. , 2012, The Science of the total environment.

[10]  C. Fan,et al.  Protein corona-mediated mitigation of cytotoxicity of graphene oxide. , 2011, ACS nano.

[11]  Omid Akhavan,et al.  Toxicity of graphene and graphene oxide nanowalls against bacteria. , 2010, ACS nano.

[12]  L. Fraceto,et al.  Toxicity assessment of TiO₂ nanoparticles in zebrafish embryos under different exposure conditions. , 2014, Aquatic toxicology.

[13]  H. Zhen,et al.  Effects of graphene/silver nanohybrid additives on electrochemical properties of magnesium-based amorphous alloy , 2014 .

[14]  W. Heideman,et al.  TiO2 nanoparticle exposure and illumination during zebrafish development: mortality at parts per billion concentrations. , 2013, Environmental science & technology.

[15]  H. Stapleton,et al.  Early Zebrafish Embryogenesis Is Susceptible to Developmental TDCPP Exposure , 2012, Environmental health perspectives.

[16]  V. W. Y. C H O I,et al.  Radioadaptive Response Induced by Alpha-Particle-Induced Stress Communicated in Vivo between Zebrafish Embryos , 2010 .

[17]  Ying Liu,et al.  The triggering of apoptosis in macrophages by pristine graphene through the MAPK and TGF-beta signaling pathways. , 2012, Biomaterials.

[18]  Huajian Gao,et al.  Graphene microsheets enter cells through spontaneous membrane penetration at edge asperities and corner sites , 2013, Proceedings of the National Academy of Sciences.

[19]  T. Yen,et al.  Biodistribution of PEGylated graphene oxide nanoribbons and their application in cancer chemo-photothermal therapy , 2014 .

[20]  Xiangang Hu,et al.  Health and ecosystem risks of graphene. , 2013, Chemical reviews.

[21]  Ganesh Gollavelli,et al.  Multi-functional graphene as an in vitro and in vivo imaging probe. , 2012, Biomaterials.

[22]  Booth Oxygen availability and embryonic development in sand snail (Polinices sordidus) egg masses , 1995, The Journal of experimental biology.

[23]  W. Heideman,et al.  Toxicity of oxidatively degraded quantum dots to developing zebrafish (Danio rerio). , 2013, Environmental science & technology.

[24]  Shuk Han Cheng,et al.  Effect of carbon nanotubes on developing zebrafish (Danio Rerio) embryos , 2007, Environmental toxicology and chemistry.

[25]  Suresh Valiyaveettil,et al.  Differential effect of solar light in increasing the toxicity of silver and titanium dioxide nanoparticles to a fish cell line and zebrafish embryos. , 2014, Environmental science & technology.

[26]  Agnes B Kane,et al.  Biological interactions of graphene-family nanomaterials: an interdisciplinary review. , 2012, Chemical research in toxicology.

[27]  Arnaud Magrez,et al.  Are carbon nanotube effects on green algae caused by shading and agglomeration? , 2011, Environmental science & technology.

[28]  D. Furgeson,et al.  Zebrafish as a correlative and predictive model for assessing biomaterial nanotoxicity. , 2009, Advanced drug delivery reviews.

[29]  Jing Kong,et al.  Antibacterial activity of graphite, graphite oxide, graphene oxide, and reduced graphene oxide: membrane and oxidative stress. , 2011, ACS nano.

[30]  Lei Jiang,et al.  Bio-inspired soft polystyrene nanotube substrate for rapid and highly efficient breast cancer-cell capture , 2013 .

[31]  Prakash D Nallathamby,et al.  In vivo imaging of transport and biocompatibility of single silver nanoparticles in early development of zebrafish embryos. , 2007, ACS nano.

[32]  C. Fan,et al.  Uniform ultrasmall graphene oxide nanosheets with low cytotoxicity and high cellular uptake. , 2013, ACS applied materials & interfaces.

[33]  S. S. Smith,et al.  DNA adduct 8-hydroxyl-2'-deoxyguanosine (8-hydroxyguanine) affects function of human DNA methyltransferase. , 1995, Carcinogenesis.

[34]  B. Ramsahoye,et al.  Measurement of genome wide DNA methylation by reversed-phase high-performance liquid chromatography. , 2002, Methods.

[35]  P. Stroeve,et al.  Bacterial effects and protein corona evaluations: crucial ignored factors in the prediction of bio-efficacy of various forms of silver nanoparticles. , 2012, Chemical research in toxicology.

[36]  Yuliang Zhao,et al.  Chemical mechanisms of the toxicological properties of nanomaterials: generation of intracellular reactive oxygen species. , 2013, Chemistry, an Asian journal.

[37]  Shuk Han Cheng,et al.  Influence of carbon nanotube length on toxicity to zebrafish embryos , 2012, International journal of nanomedicine.

[38]  D. Nugegoda,et al.  Hypoxia impairs embryo development and survival in black bream (Acanthopagrus butcheri). , 2008, Marine pollution bulletin.

[39]  Junchao Duan,et al.  Cardiovascular toxicity evaluation of silica nanoparticles in endothelial cells and zebrafish model. , 2013, Biomaterials.

[40]  Hongzheng Chen,et al.  Graphene-like two-dimensional materials. , 2013, Chemical reviews.

[41]  Jiye Shi,et al.  Biodistribution and pulmonary toxicity of intratracheally instilled graphene oxide in mice , 2013 .

[42]  R. Albrecht,et al.  Toxicity assessments of multisized gold and silver nanoparticles in zebrafish embryos. , 2009, Small.

[43]  Steven M. L. Smith,et al.  Entrapment of Chlorella vulgaris cells within graphene oxide layers , 2013 .

[44]  Li Mu,et al.  Graphene oxide amplifies the phytotoxicity of arsenic in wheat , 2014, Scientific Reports.

[45]  J. Stafford,et al.  Evaluating the toxicity of hydroxyapatite nanoparticles in catfish cells and zebrafish embryos. , 2013, Small.

[46]  M. Vallet‐Regí,et al.  Endocytic mechanisms of graphene oxide nanosheets in osteoblasts, hepatocytes and macrophages. , 2014, ACS applied materials & interfaces.

[47]  W. Heideman,et al.  Developmental toxicity of low generation PAMAM dendrimers in zebrafish. , 2007, Toxicology and applied pharmacology.

[48]  T. Sanchez-Elsner,et al.  Environmental Oxygen Tension Regulates the Energy Metabolism and Self-Renewal of Human Embryonic Stem Cells , 2013, PloS one.

[49]  Chang-Tang Chang,et al.  Preparation and Characterization of Graphene Oxide , 2014 .

[50]  Y. Martínez-Rubí,et al.  Mechanistic insights into the effect of nanoparticles on zebrafish hatch , 2014, Nanotoxicology.

[51]  Jorge L Gardea-Torresdey,et al.  Ecological nanotoxicology: integrating nanomaterial hazard considerations across the subcellular, population, community, and ecosystems levels. , 2013, Accounts of chemical research.

[52]  José María Navas,et al.  Graphene nanoplatelets spontaneously translocate into the cytosol and physically interact with cellular organelles in the fish cell line PLHC-1. , 2014, Aquatic toxicology.

[53]  O. Akhavan,et al.  Wrapping bacteria by graphene nanosheets for isolation from environment, reactivation by sonication, and inactivation by near-infrared irradiation. , 2011, The journal of physical chemistry. B.

[54]  M. Hersam,et al.  Colloidal properties and stability of graphene oxide nanomaterials in the aquatic environment. , 2013, Environmental science & technology.

[55]  Robert L. Tanguay,et al.  In vivo evaluation of carbon fullerene toxicity using embryonic zebrafish. , 2007, Carbon.

[56]  T. Braunbeck,et al.  Dechorionation as a tool to improve the fish embryo toxicity test (FET) with the zebrafish (Danio rerio). , 2011, Comparative biochemistry and physiology. Toxicology & pharmacology : CBP.

[57]  F. Ahmed,et al.  Investigation of acute effects of graphene oxide on wastewater microbial community: a case study. , 2013, Journal of hazardous materials.

[58]  Chunhai Fan,et al.  The cytotoxicity of CdTe quantum dots and the relative contributions from released cadmium ions and nanoparticle properties. , 2010, Biomaterials.

[59]  Wei Zhang,et al.  Layered manganese oxides-decorated and nickel foam-supported carbon nanotubes as advanced binder-free supercapacitor electrodes , 2014 .

[60]  S. Stankovich,et al.  Preparation and characterization of graphene oxide paper , 2007, Nature.

[61]  Maged F. Serag,et al.  Trafficking and subcellular localization of multiwalled carbon nanotubes in plant cells. , 2011, ACS nano.

[62]  Jose R Peralta-Videa,et al.  Nanomaterials and the environment: a review for the biennium 2008-2010. , 2011, Journal of hazardous materials.

[63]  A. Khademhosseini,et al.  Regulating Cellular Behavior on Few‐Layer Reduced Graphene Oxide Films with Well‐Controlled Reduction States , 2012 .