Supporting Information. Diffusion Limited Cargo Loading of an Engineered Protein Container Reinhard Zschoche and Donald Hilvert
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1 Supporting Information Diffusion Limited Cargo Loading of an Engineered Protein Container Reinhard Zschoche and Donald Hilvert Laboratory of Organic Chemistry, ETH Zürich, 8093 Zürich, Switzerland Supporting Data Figure S1 ph dependence of TOP36+ fluorescence S2 Figure S2 Size exclusion chromatograms of AaLS 13 capsid containing a mixture of S2 GFP36+/TOP36+ at different ionic strengths Figure S3 Negative staining transmission electron microscopy pictures of AaLS 13 S3 capsids at different ionic strengths Figure S4 FRET between GFP36+ and TOP36+ in absence and presence of AaLS 13 S4 capsids as a function of ionic strength Figure S5 Strategy for obtaining homo and heterogeneously labeled AaLS 13 A85C S5 capsids Figure S6 Exchange of AaLS 13 subunits between assembled capsids S6 Figure S7 Comparison of the dependence of guest encapsulation on ionic strength as S7 measured by FRET and calculated from k on and k off. Figure S8 Encapsulation kinetics and stability of the resulting capsid cargo complex for S8 AaLS neg Figure S9 Semi quantitative analysis of FRET within the AaLS 13 capsid S9 Estimation of AaLS 13 capsid composition from FRET efficiencies References S10 S12 S1
2 Figure S1. ph dependence of TOP36+ fluorescence free in solution (black diamonds) and contained in AaLS 13 capsids (red squares). Figure S2. Size exclusion chromatograms of AaLS 13 capsid containing a 1:4 mixture of GFP36+/TOP36+ at different ionic strengths (50 mm NaPi, 5 mm EDTA, ph 8.0 and varying concentrations of NaCl). (A) Absorption at 280 nm for AaLS 13 and guests. (B) Absorption at 513 nm for GFP36+ and TOP36+. Note: below 400 mm NaCl, free GFP36+ and TOP36+ adhere to the stationary phase (cross linked agarose). S2
3 Figure S3. Negative staining transmission electron microscopy pictures of AaLS 13 capsids at different ionic strengths (50 mm NaPi, 5 mm EDTA, ph 8.0 and varying concentrations of NaCl). S3
4 Figure S4. FRET between GFP36+ and TOP36+ in the absence (empty symbols) or presence of AaLS 13 capsid (full symbols) as a function of ionic strength. (A) Ionic strength modulated by addition of NaCl. (B) Ionic strength modulated by addition of Na2SO4. Note: Ionic strength is calculated by 0.5. As is apparent from the different inflection points for NaCl and Na2SO4, the Coulombic energy does not scale with the ionic strength, but rather the Debye length κ 1 which is given by. or /. /.1 S4
5 Figure S5. Strategy for obtaining homo and heterogeneously labeled AaLS 13 A85C capsids. Purification by metal affinity chromatography from cell lysate at an ionic strength of 250 mm afforded exclusively pentameric capsid fragments. These fragments were covalently labeled with either ATTO495 maleimide or ATTO565 maleimide. Increasing the ionic strength to 750 mm gave homogeneously labeled assembled capsids after one week at room temperature. Incubating a 1:1 mixture of AaLS 13 A85C(ATTO495) and AaLS 13 A85C(ATTO565) yielded capsids containing both fluorescent labels, which served as a positive control for subsequent experiments. S5
6 Figure S6. Exchange of AaLS 13 subunits between assembled capsids. (A) Emission spectra of AaLS 13 capsid labeled with both ATTO495 and ATTO565 (pink) or a mixture of AaLS 13 capsids labeled with either ATTO495 or ATTO565 after 1 min (black), 100 min (dark grey), 1 day (grey) and 4 days (light grey) upon excitation at 450 nm. (B) Time dependence of the ratio of ATTO565 (586 nm) to ATTO495 (524 nm) emission upon excitation at 450 nm after mixing AaLS 13 capsids labeled with either ATTO495 or ATTO565 (black squares). The ratio for AaLS 13 capsids containing both fluorophores is shown as a pink line. S6
7 Figure S7. Comparison of the ionic strength dependence of guest encapsulation by AaLS 13 measured by FRET and calculated from k on and k off. The experimentally determined relative fluorescence at 525 nm and 508 nm for a mixture of GFP36+/TOP36+ indicates the extent of encapsulation as a function of ionic strength (red squares; data are identical to Figure 3B). The fraction of guests encapsulated at 1 µm guest and 5 µm AaLS 13 (concentration with respect to monomer) was calculated from the K D value and is shown as a blue line. The dissociation constant for binding of GFP36+ or TOP36+ to AaLS 13 was estimated using the equation and the rate constants 10 and. The parameters a = 29.1 ± 0.6 and b = 42.5 ± 1.0 M 1/2 were determined by a linear fit of the logarithmized rate of guest exchange versus the square root of ionic strength for an AaLS 13 capsid containing 32 guests per 180 mer capsid (Figure 4D). S7
8 Figure S8. Kinetics of encapsulation and guest exchange for AaLS neg. A) Fluorescence emission at 500±5 nm (green) and >515 nm (orange) after mixing 20 µm empty AaLS neg capsids with 4 µm 1:4 GFP36+/TOP36+ at I = 350 mm in a stopped flow apparatus. B) Time dependent emission at 525 nm upon mixing AaLS neg (red) or AaLS 13 (black) capsids containing GFP36+ with capsids containing TOP36+ (30 guests/180 mer capsid, I = 350 mm). The different endpoints reflect higher FRET efficiencies likely caused by denser loading of the smaller AaLS neg capsids (diameter = 28.6 ± 2.6 nm versus 35.4 ± 3.2 nm for AaLS 13). S8
9 Figure S9. Semi quantitative analysis of FRET within the AaLS 13 capsid. (A) Schematic representation of one GFP36+ donor (green) surrounded by four TOP36+ (orange) as FRET acceptors (purple arrows) and one GFP36+ homo FRET partner (magenta arrows). (B) FRETefficiencies as a function of the guest:capsid protein ratio, measured (diamonds) and calculated upper limit for different oligomeric states given an orientation factor κ 2 of 2/3 and an inner diameter d = 26 nm. S9
10 Estimation of AaLS 13 capsid composition from FRET efficiencies In the absence of structural data for AaLS 13 capsids, the number of subunits can be estimated from 2 dimensional electron microscopy images. The measured diameter would be consistent with icosahedrally symmetric capsids having T=3 or T=4 symmetry (180 or 240 subunits, respectively). 2 Comparing FRET efficiencies between guests encapsulated in AaLS 13 with values estimated for common capsid geometries could potentially provide insights into the capsid s quaternary state. Since the absorption and emission spectra, as well as the quantum yields of GFP36+ and TOP36+, are similar to their uncharged precursors, 3 a Förster distance of 5.6 nm can be approximated, the same value as for GFP YFP assuming rapid randomization of relative fluorophore orientation. 4 The ratio of guest to AaLS 13 subunits is easily determined spectrophotometrically. Placing n points on a sphere such that their mutual distances R are maximized is referred to as the Tammes problem, and the solutions for n = were retrieved from Tables of Spherical Codes, published electronically at NeilSloane.com/packings. 5,6 For n > 130, the angular separation was approximated with Tóth s formula, eq (1) The radius of the sphere on which the chromophores are placed when encapsulated in AaLS 13 was estimated to be 13 nm by subtracting the thickness of the wall (5.0 nm) and the radius of GFP36+ (1.5 nm) from the outer radius of a filled capsid (19.5 nm). 8 The loading capacity of AaLS 13 is about 0.2 GFP36+ per monomer. This ratio corresponds to 12 guests per 60 mer (T=1), 36 guests per 180 mer (T=3) and so on, resulting in higher fluorophore density and thus FRET efficiency if a larger triangular number is assumed for a capsid of defined diameter. FRET efficiency, E 0, between one donor and acceptor is calculated by eq. 2. To account for the presence of multiple acceptors in the vicinity of a FRET donor, we used a model proposed by Fábián et al. to calculate the FRET efficiency, En, for one donor and n acceptors (eq. 3). 9 For an AaLS 13 capsid filled with a 1:4 mixture of GFP36+/TOP36+ we assumed FRET between one GFP36+ donor and four TOP36+ acceptors (Figure S9A). (2) (3) The fluorescence emission was decomposed into contributions from GFP36+ (ID) and TOP36+ (I A ), using a e UV Vis IR Spectral Software 2.0 (FluorTools, Crosstalk (direct excitation of TOP36+) was determined from the emission spectrum of a GFP36+/TOP36+ mixture in the absence of capsid and the correction included in the equation for ratiometric FRET. 10 Since donor and acceptor emission are marginally separated and quantum yields not significantly different, no corresponding corrections were employed to calculate the FRET efficiency with eq. 4. S10
11 (4) Assuming identical capsid diameters and guest:capsid subunit ratios, capsids composed of a higher number of subunits would be more densely loaded and thus exhibit higher FRET (Figure S9B). Although the agreement is imperfect, experimentally observed FRET efficiencies are most compatible with the AaLS 13 capsid being a 240 mer (T=4), a number consistent with geometric constraints. However, a value of 2/3 as orientation factor κ 2 used to determine the Förster distance 4 likely leads to overestimation of the calculated FRET efficiencies because the criterion of fast rotational randomization within the lifetime of the excited state cannot possibly be fulfilled for encapsulated proteins. 11 Consequently, we cannot exclude that the number of subunits is even higher than 240. S11
12 References (1) Israelachvili, J. N. In Intermolecular and Surface Forces (Third Edition); Elsevier, 2011; pp (2) Wörsdörfer, B.; Woycechowsky, K. J.; Hilvert, D. Science 2011, 331, (3) Cubitt, A. B.; Woollenweber, L. A.; Heim, R. Methods Cell Biol. 1999, 58, (4) Patterson, G. H.; Piston, D. W.; Barisas, B. G. Anal. Biochem. 2000, 284, (5) Conway, J. H.; Sloane, N. J. A. Sphere packings, lattices and groups; 3rd ed.; Springer: New York, (6) Rurup, W. F.; Verbij, F.; Koay, M. S. T.; Blum, C.; Subramaniam, V.; Cornelissen, J. J. L. M. Biomacromolecules 2014, 15, (7) Fejes Tóth, L. Jber. dtsch. Math. Ver. 1943, 53, (8) Wörsdörfer, B.; Pianowski, Z.; Hilvert, D. J. Am. Chem. Soc. 2012, 134, (9) Fábián, Á. I.; Rente, T.; SzölloSi, J.; Matyus, L.; Jenei, A. ChemPhysChem 2010, 11, (10) McCann, J. J.; Choi, U. B.; Zheng, L.; Weninger, K.; Bowen, M. E. Biophys. J. 2010, 99, (11) van der Meer, B. W.; van der Meer, D. M.; Vogel, S. S. In FRET Förster Resonance Energy Transfer; Wiley VCH Verlag GmbH & Co. KGaA: Weinheim, Germany, 2013; pp S12
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