Quantum Dot-Peptide-Fullerene Bioconjugates for Visualization of In Vitro and In Vivo Cellular Membrane Potential
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1 Quantum Dot-Peptide-Fullerene Bioconjugates for Visualization of In Vitro and In Vivo Cellular Membrane Potential Okhil K. Nag, Michael H. Stewart, Jeffrey R. Deschamps, Kimihiro Susumu, Eunkeu Oh, Vassiliy Tystsarev, Qinggong Tang, Alexander L. Efros, Roman Vaxenburg, Bryan J. Black, YungChia Chen, Thomas J. O Shaughnessy, Stella H. North, Lauren D. Field, Philip E. Dawson, Joseph J. Pancrazio, Igor L. Medintz, Yu Chen, Reha S. Erzurumlu, Alan L. Huston, and James B. Delehanty Table of Contents I. Supporting Information Tables a) Table S1. Physicochemical properties of peptides used in this study b) Table S2. Average hydrodynamic diameter of 605 nm DHLA-capped QDs and peptide-c 60 complexes. II. Supporting Information Figures a) Figure S1. Spectroscopic characterization of QD-peptide-C60 bioconjugates. b) Figure S2. Transmission electron micrographs (TEM) QD samples used in this study. c) Figure S3. Steady-state PL analysis of 605 nm QD-peptide-C 60 conjugates. d) Figure S4. Steady-state PL analysis of 625 nm QD-peptide-C 60 conjugates. e) Figure S5. Wavelength-dependent quenching analysis. f) Figure S6. Circular dichroism (CD) analysis of peptide JBD2 interaction with liposomal membranes. g) Figure S7. Circular dichroism (CD) analysis of peptide JBD3 interaction with liposomal membranes. h) Figure S8. Imaging of membrane potential changes in cells labeled with QD-DHLA-JBD1 peptide-(no C 60 ) bioconjugates. 1
2 i) Figure S9. Quantification of cytotoxicity of QD-peptide-C 60 bioconjugates in HeLa cells. j) Figure S10. QD-JBD1-C 60 labeling of networks of mouse cortical neurons. k) Figure S11. Dual-channel imaging of cellular membrane potential in PC12 pheochromocytoma cells. l) Figure S12. Spectral profiles of QD and dye probes used in this study. m) Figure S13. In vivo optical imaging of cortical electrical stimulation using QD-JBD1 peptide- C 60 bioconjugates. n) Figure S14. In vivo optical imaging of cortical electrical stimulation using QD-JBD1 peptide- C 60 bioconjugates (multiple mice data). o) Theoretical estimations of steady state quenching of QD PL by peptide-c 60 and its modulation by plasma membrane depolarization a) Estimation of steady state QD PL quenching of by peptide-c 60. b) Effect of the membrane electric field on electron transfer rate from QD to C 60. c) The modulation of QD quenching efficiency in response to changes in plasma membrane potential. 2
3 Table S1. Physicochemical properties of peptides used in this study Properties\Sample JBD1 JBD2 JBD3 Molecular weight 1 without C with C pi 1 Native peptide Leu substituted for Lys Peptide charge at ph Native peptide Leu substituted for Lys Hydrophobicity index 1 Native peptide Leu substituted for Lys Determined using GPMAW protein bioinformatics tool ( 2 Determined using PepCalc peptide calculator ( 3 Leucine (Leu) substituted for lysine (Lys) to emulate removal of Lys charge after peptide conjugation to C 60 Table S2. Average hydrodynamic diameter of 605 nm DHLA-capped QDs and peptide-c 60 complexes with increasing ratios of peptides as determined by dynamic light scattering (DLS) H-diameter Standard-Deviation Diffusion Coefficient Standard-Deviation Sample (nm) (nm) (um 2 /s) (um 2 /s) DHLA QD JBD1-C JBD2-C JBD3-C
4 Figure S1. Spectroscopic characterization of QD-peptide-C60 bioconjugates. Shown are the baseline-corrected UV-visible absorbance spectra of free peptides JBD1, JBD2, and JBD3 and their corresponding C 60 bioconjugates. The spectra show significantly greater absorbance in the nm spectral window for the C 60 peptide conjugates indicating the presence of the C 60 moiety on the peptide. 4
5 Supporting Information Nag et al. Figure S2. Transmission electron micrographs (TEM) QD samples used in this study. TEM analysis of A) 605 nm-emitting and B) 625 nm-emitting QDs. The average diameter of the 605 and 625 QDs were 8.2 ± 0.5 nm and 9.4 ± 0.7 nm, respectively. 5
6 Figure S3. Steady-state PL analysis of 605 nm QD-peptide-C 60 conjugates. Representative PL spectra collected from 605 nm-emitting QDs capped with DHLA-PEG 750 -OMe ligands. Shown are spectra for QDs assembled with increasing ratios of (A) JBD1-C 60, (B) JBD2-C 60, and (C) JBD3-C 60. 6
7 Figure S4. Steady-state PL analysis of 625 nm QD-peptide-C 60 conjugates. Representative PL spectra collected from 625 nm-emitting QDs capped with DHLA (A through C) or DHLA- PEG 750 -OMe ligands (D through F) assembled with increasing ratios of JBD peptide-c 60 conjugates. The data correspond to JBD1-C 60 (A, D), JBD2-C 60 (B, E) and JBD3-C 60 (C, F). The 7
8 normalized quenching data for all six samples at the various peptide-c 60 ratios are shown in panel G. Figure S5. Wavelength-dependent quenching analysis. Shown are the PL spectra for 605 nmemitting QDs capped with DHLA (left column) or DHLA-PEG 750- OMe (right column) ligands when assembled with 30 JBD peptide-c 60 acceptors. Results of the wavelength-dependent quenching analysis are also shown as the horizontal line in each plot. In each column, the plots correspond to conjugates of QDs with peptide JBD1-C 60 (top), JBD2-C 60 (middle), and JBD3- C 60 (bottom). 8
9 Figure S6. Circular dichroism (CD) analysis of peptide JBD2 interaction with liposomal membranes. (A) CD spectra of 10 µm peptide JBD2 in PBS or in the presence of DMPC liposomes showing increased helical content by the dip in the CD spectra between nm. (B) Tabulation of the relative quantification of the secondary structure analysis of peptide JBD2. The only peptide secondary structure that increases upon incubation with liposomal membranes is α helix. 9
10 Figure S7. Circular dichroism (CD) analysis of peptide JBD3 interaction with liposomal membranes. (A) CD spectra of 10 µm peptide JBD3 in PBS or in the presence of DMPC liposomes showing the increased helical content evidenced by the dip in the CD spectra between nm. The inflection in the spectra for JBD3 + liposomes is indicative of Type II proline helix formation. (B) Tabulation of the relative quantification of the secondary structure analysis of peptide JBD3. Helix formation is the only peptide secondary structure that increases upon incubation with liposomal membranes. 10
11 Figure S8. Imaging of membrane potential changes in HeLa cells labeled with QD-DHLA- JBD1 peptide-(no C 60 ) bioconjugates. HeLa cells labeled with 20 nm QD-DHLA-JBD1 peptide (no C 60 ; 20 peptides per QD) before (resting) and after (depolarized) addition of KCl solution. The data show less than 3% decrease in QD PL. 11
12 Figure S9. Quantification of cytotoxicity of QD-peptide-C 60 bioconjugates in HeLa cells. Cell viability was determined using an MTS-based cellular proliferation assay. The bar graphs show the normalized cell viability (n = 5 ± SEM) for QD-DHLA alone (20 nm), JBD1-C 60 peptide alone (400 nm) and QD-JBD1-C 60 conjugates (20 nm QD/400 nm peptide-c 60 ). Also shown are the cell viabilities for oxonol B438 and FluoVolt TM. The results were normalized to the signal corresponding to incubation buffer alone (DPBS). 12
13 Figure S10. QD-JBD1-C 60 labeling of networks of mouse cortical neurons. (A) DIC (top) and fluorescence (bottom) images of cultured cortical neuronal networks labeled with QD-JBD1-C 60 conjugates. Scale bar 50 µm. (B) Live cell staining of QD-JBD1-C 60 -labeled neuronal networks with Calcein AM confirmed cellular viability. In A and B, arrows highlight regions of membranous QD labeling. (C) Cellular viability data as determined by live/dead staining. Data shown are average ± S.D. of 5 separate networks (8 regions of interest interrogated in each network). 13
14 Figure S11. Dual-channel imaging of cellular membrane potential in PC12 pheochromocytoma cells. (A) DIC and fluorescence images of PC12 cells co-labeled with oxonol B438 and QD-DHLA-JBD1-C 60 conjugates. Arrow highlights same cell in Scale bar, 20 µm. (B) Quantification of the relative differential fluorescence response of the QD-DHLA- JBD1-C 60 and oxonol probes upon depolarization with KCl. Fluorescence intensities were obtained by drawing ROIs around individual cell membranes. The graph shows the average fluorescence intensity (±SEM) obtained from 30 to 40 cells from 4 to 6 independent experiments. 14
15 Figure S12. Spectral profiles of QD and dye probes used in this study. Shown are the normalized absorption and emission profiles of the QD and fluorophore dyes used in this study. The emission of the 605 nm-emitting QD is spectrally well-resolved from the emission of the oxonol B438 (Ox) and FluoVolt TM (FV) probes. 15
16 Figure S13 cont d 16
17 Figure S13. In vivo optical imaging of cortical electrical stimulation using QD-JBD1 peptide-c 60 bioconjugates. (A - C) Images and fluorescence response of mouse cortex injected with QD-JBD1 peptide (noc 60 ) conjugates during stimulus onset. (A) Images were captured at 200 Hz frame rate and numbers indicate the acquisition time point. Frame at 575 ms is expanded in (B) and shows the four ROIs corresponding to the fluorescence response traces shown in (C). (D F) Images and fluorescence response of mouse cortex injected with QDs alone during stimulus onset. (D) Images were captured at 200 Hz frame rate and numbers indicate the acquisition time point. Frame at 575 ms is expanded in (E) and shows the four ROIs corresponding to the fluorescence response traces shown in (F). 17
18 Figure S14. In vivo optical imaging of cortical electrical stimulation using QD-JBD1 peptide-c 60 bioconjugates (multiple mice data). Shown are the results of cortical stimulation/optical recording experiments performed on three separate mice. Experiments were performed exactly as described for the data in Figure 7 (main manuscript) and SI Figure S13. The average QD PL response across the three animals (± SEM) was 2.1 ±
19 Theoretical estimations of steady state quenching of QD PL by peptide-c 60 and its modulation by plasma membrane depolarization. a) Estimation of steady state QD PL quenching of by peptide-c 60. In estimating the steady state QD PL quenching of QD PL by the peptide-c 60, it was assumed that (i) in order to quench the QD luminescence the C 60 must be directly at the QD surface, and (ii) only a fraction of all peptide-c 60 conjugates attached to the QD contributes to the PL quenching by bringing C 60 to the QD surface (the rest of the peptides do not contribute to the quenching). The PL intensity can be written as: where τ r and τ nr are the radiative and nonradiative decay times of the exciton, respectively, in the QD, α = σ(ω)i/ħω, wherein σ(ω) is the absorption coefficient at the excitation frequency ω, I is the light intensity, and τ e is the time of the electron transfer from the QD to the C 60 moiety. Finally, p is the number of peptide-c 60 at the QD surface, which is limited by the total number of peptide-c 60 sites at the QD surface, p tot. As a result, the relative PL intensity of the QD assembled with p peptide-c 60 can be expressed as: where QY = 1/[1 + (τ r /τ nr )] and is the PL quantum yield of the QD in the absence of C 60. It can be seen from Eq. (2) that low PL quantum yield reduces the efficiency of quenching, and generally the quenching increases with the number of C 60 at the QD surface. Upon incubation of peptide-c 60 with QDs at peptide-c 60 /QD ratios that are below saturation of the QD surface (in this case peptide-c 60 /QD < ~100 ± 20), eventually all peptide- C 60 get attached to the QD surface. As a result, each QD has on average peptide-c 60 at its surface. Due to hydrophobic forces, some of these peptides will bend, bringing the C 60 directly to 19
20 the QD surface. The dynamical average of C 60 at the QD surface due to adsorption and desorption processes can be written as: where the coefficients A and D are the rate constants describing adsorption and desorption of C 60 to and from the QD surface, respectively, and p tot is the total number of sites available for C 60 at the surface of an individual QD. The steady state solution of Eq. (3) can be written as A(p tot p)( p) D p = 0, from which can be derived: The only one meaningful solution of Eq. (4) is: In the absence of desorption, D/A = 0, and the steady state solution gives the following: That is, all available peptide-c 60 sites on the QD surface should be occupied with the help of all available peptide-c 60. As it was shown above, this would lead to all peptide-c 60 eventually attached to the QDs making p simply equal to the number of peptide-c 60 occupying the QDs. This also requires that the number of available sites is larger than the initial amount of peptide- C 60, which is true because we see reduction of PL all the way to a ratio of peptide-c 60 /QD = 60 (Figure 2D, main manuscript). In this case, Eq. (2) and the data points of the PEG-coated QDs can be used to directly fit the value of QY (τ r /τ e ) (Fig. 2D, main manuscript). This fit gives QY 20
21 (τ r /τ e ) The universal fitting parameter QY (τ r /τ e ) = allows an estimation of the time of the electron escape from the QD to the C 60 moiety. The typical radiative decay time of the studied QDs τ r ns. Using a value of QY = 30 %, τ e = τ r (0.3/0.093) ns. b) Effect of the membrane electric field on the electron transfer rate from QD to C 60. The electron transfer rate from the QD donor sitting on the membrane to the C 60 inserted into the phospholipid bilayer is quite sensitive to modulations in the electric field because changes in the electric field change the tunneling integral responsible for the electron transfer. Consider the effect of changes in the electric field on one QD-peptide-C 60 conjugate with the C 60 moiety in the membrane bilayer. In the case when the C 60 acceptor is located in the middle of the membrane with thickness d we can estimate: where τ se (0) is the tunneling time of the electron from the QD donor to the C 60 acceptor when the C 60 is in the middle of the membrane in the absence of the electric field, m is the free electron mass, R = ħ2/2ma2 0 = 13.6 ev is the electron Rydberg and a 0 = nm is the electron Bohr radius. In the expression: d = 4 nm and we assume that the tunneling barrier is high (U ev) and voltage (Ed) is 50 mv. In this instance a significant (~9%) modulation of QD PL intensity is provided by a single peptide C 60 for a QD with 100% quantum yield. 21
22 c) The modulation of QD quenching efficiency in response to changes in cellular membrane potential. The effect of C 60 -mediated QD quenching, however, is reduced in real QDs due to their lower PL quantum yield and the effect of the other C 60 at the QD surface, which also suppresses the PL intensity. If only one peptide-c 60 (of all of those assembled onto the QD surface) inserts into the membrane and is affected by the electric field, using Eqs. (1) and (7) it can be written: where pꞌ is the number of C 60 at the QD surface brought by peptide-c 60 attached to the QD surface. So the change in QD PL intensity can be expressed as: The relative QD intensity, consequently, is expressed as: This expression allows one to estimate changes in the PL intensity. Using the change in tunneling time (δ = 0.090), the universal fitting parameter QY (τ r /τ e ) = 0.093, pꞌ = 5 and assuming that (0) τ e we obtain IP L(E)/I P L (E) 1.2 % if it is assumed that the tunneling time in the membrane is two times faster than the tunneling time to C 60 at the QD surface: (0) 2τe. It is likely that membrane undulations wrap the plasma membrane around a significant portion of the QD surface resulting in the insertion of multiple peptide C 60 into the membrane bilayer. In this case, to estimate the modulation efficiency, one can multiply the modulation efficiency expected for a QD with a single peptide-c 60 by the total number at the QD surface. In the case of = 20 (as is the case in the cellular depolarization experiments performed herein) modulation of the QD PL by depolarization of membrane potential can reach 24 %. 22
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