Graphene Microsheets Enter Cells through Spontaneous Membrane Penetration at Edge Asperities and Corner Sites*
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1 Graphene Microsheets Enter Cells through Spontaneous Membrane Penetration at Edge Asperities and Corner Sites* Yinfeng Li, Hongyan Yuan, Annette von dem Bussche, Megan Creighton, Robert H. Hurt, Agnes B. Kane and Huajian Gao School of Engineering, Department of Pathology and Laboratory Medicine, Institute for Molecular and Nanoscale Innovation Brown University, Providence, RI, 02912, USA. Department of Engineering Mechanics, Shanghai Jiao Tong University, Shanghai , China * Based on Li et al., Proc. Nat. Academy of Sci., 110 (30) (2013) presented at SNO in Southern California, November, 2013
2 Graphene calling all researchers in sustainable nanotechnology benzene, naphthalene, phenanthrene, higher PAH,... graph -ene isolated in molecular weight > [Boehm et al., Carbon, 1986] We now have a family of two-dimensional graphene-based materials H 2 SO 4 (intercalant) oxidizing agent(s) Rapid thermal annealing Natural flake graphite Graphite bisulfate or Graphite oxide Wet sonication Expanded graphite few-layer graphene; multilayer graphene; graphite nanoplates* graphene oxide * All in the graphene family A recommended nomenclature for two-dimensional carbon materials, Carbon, 2013
3 Some emerging applications of graphene materials Low-percolation-threshold composite fillers (for e-conductivity, strength, barrier properties) Thin conductive films; conducting inks Guo et al., ES&T, 2012 Ultrathin coatings as molecular barriers Electrode materials (e-conductivity, intercalation) Emulsion stabilizers with 100% atom efficiency Catalyst supports - ultrahigh surface area (2600/N m 2 /g) Materials with engineered folds and wrinkles Ruga materials actuators, crumpled particles, filled sacks
4 Biological interactions and safety of graphene materials Sanchez, Jachak, Hurt, Kane, Biological Interactions of Graphene-Family Nanomaterials An Interdisciplinary Review Chemical Research in Toxicology, 25 (1) (2012). Unique modes of biological coupling for atomically thin plates
5 Graphene Materials Can Produce Artifacts during In Vitro Toxicity Testing GFNs deplete folic acid from cell culture medium GFNs adsorb and quench dyes used in toxicity assays Creighton, Hurt, Kane et al., Graphene-Induced Optical and Adsorptive Artifacts During In Vitro Toxicology Assays Small, 2013
6 Are Graphene-Based Powders an Inhalation Health Risk? Comparisons to carbon nanotubes Differences - graphene materials have fewer impurities; - lie outside the fiber pathogenicity paradigm; - are atomically thin Similarities - graphene materials have range of geometries within the family > thickness range: nm > lateral dimension range: 5 nm 100 um (factor of 20,000!) - have range of surface chemistries Deposition patterns for monolayer graphene in human respiratory tract For commercial multi-layer graphene samples: A = 2600/N (m 2 /g)
7 Can graphene materials penetrate cell membranes and be internalized? Huajian Gao Agnes Kane Robert Hurt Prior work on carbon nanotube uptake Shi, Von dem Bussche, Hurt, Kane, Gao Cell entry of one-dimensional nanomaterials occurs by tip recognition and rotation Nature Nanotechnology, 2011 MWNT entry into liver cells
8 Example Morphologies in Commercial Multi-Layer Graphene 2 um
9 Few-layer graphene microsheets enter cells and localize in the cytoplasm or in vesicles human lung epithelial cells mouse macrophages all FLG microsheets are internalized sheets localize parallel to substrate larger sheets alter cytoskeletal structure
10 High-resolution imaging of the cell entry process human lung epithelial cells mouse macrophages primary human keratinocytes
11 Coarse-Grained and All-Atom Molecular Dynamics Simulations (H. Gao group) Coarse-grained simulations: POPC lipid bilayer with 6.4 nm lateral dimension graphene nanosheet All-atom simulations: POPC lipid bialyer interacting with monolayer graphene sheet corners These simulations are either: Spontaneous (entry initiated by thermal fluctuations) or Steered pulled through membrane by virtual spring to calculate energy barriers
12 Molecular Dynamics Results: Graphene NanoSheets Penetrate Cell Membranes but Graphene MicroSheets do not.? Nanosheet spontaneous entry (CGMD) Microsheets are repelled away by entropic forces, even during edge-on approach calculation of energy barriers for penetration (all-atom MD) only 5kBT energy barrier
13 Resolution: Real graphene samples do not have atomically smooth edges! Reference. Other irregular edge geometries Asperities and corners initiate passive penetration, which propagates along the graphene edge Y Li, H Yuan, A von dem Bussche, M Creighton, RH Hurt, AB Kane, and H Gao, Graphene microsheets enter cells through spontaneous membrane penetration at edge asperities and corner sites, Proceedings of the National Academy of Sciences, 2013.
14 Graphene lateral size determines macrophage uptake and lung clearance [Sanchez, Jachack, Hurt, Kane, Chemical Research in Toxicology, 2012] 500 nm 800 nm 5 um Uptake 25 um Attachment and multicellular coverage
15 Summary Statement Graphene-based materials are a new material family with varying geometry and chemistry. Materials with lateral dimension < about 5 um can enter mammalian cells initiated by spontaneous penetration of lipid bilayers at atomically-thin corner and rough edge sites. Uptake/ clearance for large lateral dimension (> 5 um) flakes is often incomplete, and this subset of materials may deserve special attention in nanotoxicity studies and risk assessment Financial support was provided by NSF CBET (Barbara Karn, program manager), and NSF CMMI and the NIEHS Superfund Research Program The Hurt Laboratory at Brown
16 Backups
17 Large GFNs and Carbon Nanotubes Induce Macrophage Toxicity
18 2. Ultrathin Barrier Coatings [Guo, Hurt et al., Graphene-based environmental barriers, Envir. Sci. Tech. 2012] See also: [V. Berry, Impermeability of graphene and its applications (Review), Carbon, in press 2013] P comp P polym With GO coating 50 μm Polymer GO Film Thickness (nm) Poisson disk deposition
19 4. Interfacial assembly: high-performance emulsion stabilizers Graphene oxide structure [Cote et al. Pure Appl. Chem. 2011] 50 ppm GO Meg Creighton 200 um Thermodynamic modelling 250 ppm GO -ΔG stabilization = solid-oil solid-water ϒ oil-water GO SDS 200 um oil-in-water emulsions Unique features of graphene-based stabilizers - Up to 100% atom economy - conformal coverage - multilayer tiling - barrier properties? Pickering emulsions
20 Examples of unique features of graphene-based stabilizers 1. Mass potency 2. vdw transparency Stabilization Energy (normalized) atomically thin plates Atomically thin GO sheets show wetting transparency [Koratkar et al] 3. Templating of crumpled microparticles 50 um 10 nm spheres Atomically thin GO sheets crumple if oil phase evaporates
21 5. Folded structures Ruga materials Ruga (pl Rugea) from Latin folds, creases, wrinkles Ruga materials are a new class of engineered structures made by contraction of elastic substrates with stiffer surface films K.S. Kim Brown Univ Critical length for graphene self-folding = (C/ ) 1/2 [Cranford, Sen, Buehler, 2009] C bending stiffness - adhesion energy Multilayers: bending stiffness ~ N 3 (beam theory, no sliding) Nanodroplet Activated and Guided Folding of Graphene Nanostructures [Patra, Wang, Kral, Nano Letters, 2009] 200 nm 21
22 Cargo-Filled Graphene Nanosacks Chen Y, Guo F, Jachak A, Kim S-P, Datta D, Liu J, Kulaots I, Vaslet C, Jang HD, Huang J, Kane A, Shenoy VB, Hurt RH, Nano Letters (2012).? salmon-sperm DNA citrate-stabilized nanosilver as minority phase (Ag:GO 1:16) citrate-stabilized nanosilver as majority phase (Ag:GO 2:1)
23 Filled Graphene Nanosacks as Multifunctional Materials [Y Chen, F Guo, Y Qiu, H Hu, I Kulaots, E Walsh, RH Hurt, ACS Nano, 2013] gold nanoparticles silicon nanoparticles iron oxide NPs Ternary hybrids as MRI / CT dual contrast agents gold / iron oxide barium titanate / iron oxide Full scale, clinical MRI / CT results
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