Size-Dependent Endocytosis of Single Gold Nanoparticle
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1 ESI Size-Dependent Endocytosis of Single Gold Nanoparticle Yuping Shan a,d#, Suyong Ma b#, Liya Nie b#, Xin Shang a, Xian Hao a,d, Zhiyong Tang c * Hongda Wang a * a State Key Laboratory of Electroanalytical Chemistry, Changchun Institute of Applied Chemistry, Chinese Academy of Sciences, Changchun, Jilin , P.R. China b School of Chemical Engineering and Technology, Tianjin University. Tianjin , P.R. China c National Center for Nanoscience and Technology, Beijing , P.R.China d Graduate School of Chinese Academy of Sciences, Beijing , P.R. China # Y.Shan, S.Ma, L.Nie contribute equally to this paper. hdwang@ciac.jl.cn or zytang@nanoctr.cn S1
2 Measuring the Sizes of Gold Nanoparticles by Transmission Electron Microscopy In our experiments the Au NPs with different diameters were synthesized respectively as report 1. AuNPs with a diameter of 4 nm were obtained using NaBH 4 as reductant and sodium citrate as stabilizing agent. For the synthesis of 12 nm Au NPs we added HAuCl 4 solution to a boiled solution of sodium citrate under stirring. The 17 nm Au NPs were prepared by the citrate reduction method. In this method, the negative charge citrate ions act as both a reducing agent, and a capping agent, which make the Au NPs load negative charge. The ESI Figure S1 shows the well-dispersed Au NPs, and it has been documented that the sulfur-containing groups tend to exhibit a high affinity toward gold surface, therefore such-prepared Au NPs are easily to be functionalized by the L-cysteine in our following experiments. ESI Figure S1. Transmission electron microscopy images of colloidal Au NPs with diameters of (a) 4, (b) 12, and (c) 17 nm. All the scale bars are 20 nm. S2
3 Control Experiments 1. The blocking experiments with cytochalasin B. ESI Figure S2. Blocking experiments by cytochalasin B. The interactions (force curves) between the HeLa cell and (a) 4 nm, (b) 12 nm, and (c) 17 nm single Au NPs after blocking with cytochalasin B. (d-f) The corresponding histograms of uptaking forces. (g-i) The corresponding histograms of unbinding forces. The histograms were obtained from about 400 randomly chosen force curves after blocking with cytochalasin B. 2. The block experiments by extracting cholesterols from cell membranes S3
4 To identify the pathway of endocytosis for HeLa cells uptaking single Au NP, we further performed block experiments by other reagents. As known, cholesterol-dependent and clathrin-dependent endocytosises are two main pathways of NPs uptake. Previous reports showed that lipid rafts, as cell membrane microdomains enriched with sphingolipids and cholesterol, mediated the endocytosis (i.e. cholesterol-dependent endocytosis), and this pathway of endocytosis was often confirmed by removing cholesterol from the raft regions with methyl-β-cyclodextrin 2. Hypertonic sucrose, chlorpromazine, and monodansylcadaverine are three main blocking reagents for clathrin-mediated endocytosis 3. In our experiments, after the treatment with 5 mm methyl-β-cyclodextrin for 20 minutes at 37 C to remove the cholesterol in lipid raft regions, there was scarcely force signal fi or fu in thousands of recorded force curves, as shown in ESI Figure S3, which indicated that the endocytosises for 4, 12, and 17 nm Au NPs were successfully inhibited by methyl-β-cyclodextrin. We also observed the cellular uptake of Au NPs by confocal fluorescence microscopy, and the results pointed to the excellent blocking effect of methyl-β-cyclodextrin rather than hypertonic sucrose (unpublished data), which further verified the pathway of endocytosis. These results demonstrate that the specific interaction between the single Au NP and the living HeLa cell is lipid raft-mediated endocytosis. S4
5 ESI Figure S3. Blocking the endocytosis by methyl-β-cyclodextrin. The histograms of uptaking forces for (a) 4 nm, (b) 12 nm, and (c) 17 nm single Au NPs after blocking with methyl-β-cyclodextrin. (d-f) The corresponding histograms of unbinding forces. The histograms were obtained from about 400 freely chosen force curves after blocking with methyl-β-cyclodextrin. 3. The force spectroscopy performed by the clean AFM tip and Poly (ethylene glycol) (PEG)-functionalized AFM tip at 37 C. To eradicate the possibility that the force signals might be related to the PEG (Poly (ethylene glycol)) molecules on AFM tip or the bare AFM tip itself, we first applied a clean AFM tip to engage force spectroscopy on living HeLa cells, and found that there was no force signal observed in many thousands of force curves, as shown in ESI Figure S4a. PEG functionalized AFM tip was also tested and no force signal was observed as shown in ESI Figure S4b. These control experiments indicate that the S5
6 force signals in Figures 2a-2c definitely result from the interactions between the HeLa cell and the Au NP attached on AFM tip, rather than the penetration of the AFM tip or the interference of other molecules on the AFM tip. ESI Figure S4. Control experiments. (a) A typical force curve in many thousands of force curves by a clean AFM tip on the living HeLa cell. (b) A typical force curve in many thousands of force curves by the PEG (Poly (ethylene glycol)) attached AFM tip on the living HeLa cell. S6
7 The Schematic Process of Endocytosis of Single Au NP during Engaging the Force Spectroscopy To further understand the event of the living HeLa cell endocytosing the Au NP, it is essential to study the process of endocytosis during the distance-force cycle. As well known, endocytosis is a cargo-specific process by which the materials from the external environment are internalized 4, 5. In this communication, we recorded the endocytosis events by force spectroscopy, and deduced that the process of HeLa cell endocytosing single Au NP is lipid raft-mediated endocytosis. Based on these results, we drew a scheme of the possible endocytosis process during engaging the force spectroscopy, as shown in ESI Figure S5. During the trace process, the AFM tip tethered with Au NPs first moved towards the surface of cells (shown in ESI Figure S5a). As the cysteine capped Au NP on the AFM tip encountered lipid raft regions in cell membranes, the Au NP would interact with the cell membranes, and then the cell membranes began to invaginate around the AFM tip (ESI Figure S5b). Subsequently, with the trace process of force spectroscopy, the Au NP was fully wrapped and endocytosed via the lipid rafts in cell membranes (ESI Figure S5c), which resulted in the uptake force signal due to the sudden bending of the AFM cantilever downwards. With the retrace process, the Au NP tethered on AFM tip was pulled from the inside of the cell (ESI Figure S5d), and then the endocytic Au NP withdrew away from the cell membranes as shown in ESI Figure S5e, which induced the unbinding force signal due to the dissociation between the Au NP and the cell membranes. The hypothesis indicates the possible process of the endocytosis for single NP with the S7
8 Electronic Supplementary Material (ESI) for Chemical Communications diameter of several nanometers, which is absolutely different from the unbinding process between the antigen and antibody. ESI Figure S5. Scheme of the endocytosis of single Au NP attached on AFM tip during force-distance cycle. (a) The AFM tip tethered with Au NP moves towards the cell membrane surface. (b) The cell membranes with lipid raft regions begin to invaginate around the AFM tip. (c) The Au NP is endocytosed via the lipid rafts. (d) The Au NP withdraws from the inside of the cell. (e) The Au NP is pulled away from the cell membranes. S8
9 Experimental Section Cell Culture: Parental HeLa cells were obtained from Shanghai Institute of Biological Sciences. Aminopropyltriethoxysilane (APTES) functionalized glass slides were prepared as previously reported 6. The cells were cultured on APTES-glass slides in Dulbecco s modified Eagle s medium (DMEM) containing 10 % fetal bovine serum, 100 U/mL penicillin, and 100 μg/ml streptomycin at 37 C with 5 % CO 2. Usually, the cells needed to be cultured for 2 or 3 days to achieve 75 % confluence on the glass slide. Before performing force spectroscopy experiments, the HeLa cells were rinsed with fresh DMEM three times to remove the metabolite of cells. Conjugation of Au NPs on AFM Tips Water-solubility Au NPs were obtained following the previous synthetic routes 1. 1 μl L-cysteine solution was added to 500 μl Au NPs (10 nm) aqueous solution at room temperature for 3 hours. Then the Au-cysteine conjugate was purified through a 10k Molecular Weight Cutoff (MWCO) Microcon centrifugal filter device (Millipore, Inc.). Lastly, the purified Au-cysteine NPs were redispersed into 500 μl aqueous solution. Functionalization of AFM tips (Microlever, Veeco, Santa Barbara, CA, coated for MacMode AFM by Agilent Technologies, Chandler, AZ) with APTES was just the same as preparing APTES-glass slides described above. The tips were cleaned with O 3 for 20 minutes to get rid of any organic contamination and placed in a petri dish at the bottom of a dessicator to be modified with APTES. Subsequently, Aldehyde-PEG-NHS linker was conjugated in triethylamine and CHCl 3 as described 7. Then the AFM cantilevers were immersed in a 100 μl cysteine capped Au NP solution for functionalization, and S9
10 2 μl 1M NaCNBH 3 solution was added to the solution and mixed carefully with pipette. After functionalization, 5 μl 1M ethanomine solution was added to the solution in order to passivate the unreacted aldehyde groups. Lastly, the modified AFM tips were rinsed with water for three times and stored at 4 C until use. Force Curve Measurements: Force curve measurements were acquired using AFM 5500 (Agilent Technologies, Chandler, AZ) in DMEM at 37 C. The blocking experiments were performed by the addition of 5 μg/ml cytochalasin B and 5 mm methyl-β-cyclodextrin, respectively. Several thousand force curves were recorded at different positions on the cells. The deflection sensitivity of the photo-detector was determined by the slope of the force-distance curves taken on the bare surface of mica. The AFM cantilevers were calibrated by a reference cantilever (CLFC, Veeco, Santa Barbara, CA) as described M. Liang, I. C. Lin, M. R. Whittaker, R. F. Minchin, M. J. Monteiro and I. Toth, ACS Nano, 2009, 4, U. Ziegler, J. Fernandez-Carneado, E. Giralt, R. Rennert, A. G. Beck-Sickinger and H. P. Merkle, Biochemistry, 2004, 44, S. M. Uriarte, N. R. Jog, G. C. Luerman, S. Bhimani, R. A. Ward and K. R. McLeish, Am J Physiol Cell Physiol, 2009, 296, C S. D. Conner and S. L. Schmid, Nature, 2003, 422, E. M. Schmid and H. T. McMahon, Nature, 2007, 448, D. Lohr, R. Bash, H. Wang, J. Yodh and S. Lindsay, Methods, 2007, 41, C. Stroh, H. Wang, R. Bash, B. Ashcroft, J. Nelson, H. Gruber, D. Lohr, S. M. Lindsay and P. Hinterdorfer, Proc. Natl. Acad. Sci. U. S. A., 2004, 101, B. Ohler, Application note 94. S10
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