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1 SUPPLEMENTARY INFORMATION Solvent-free protein function - reversible dioxygen binding in liquid myoglobin Adam W. Perriman 1, Alex P. S. Brogan 1, Helmut Cölfen 2, Nikos Tsoureas 3, Gareth R. Owen 3 Mann 1 1 Centre for Organized Matter Chemistry, School of Chemistry, University of Bristol, Bristol BS8 1TS, UK & Stephen 2 Max-Planck-Institute of Colloids and Interfaces, Am Mühlenberg, D Golm, Germany 3 School of Chemistry, University of Bristol, Bristol BS8 1TS, UK Materials and methods General Equine heart met-myoglobin (Mb) was purchased from Sigma-Aldrich and used as received. N,Ndimethyl-1,3-propanediamine (DMPA), N,N-dimethyl-1,6-hexanediamine (DMHA), N-(3- dimethylaminopropyl)-n'-ethylcarbodiimide hydrochloride (EDC), poly(ethylene glycol) 4-nonylphenyl 3- sulfopropyl ether (S 1 = C 9 H 19 -C 6 H 4 -(OCH 2 CH 2 ) n O(CH 2 ) 3 SO - 3 K + ; n = 20) and glycolic acid ethoxylate lauryl ethers (S 2 = CH 3 -(CH 2 ) x -O-(CH 2 CH 2 O) n CH 2 -COOH; x = 11-13, n = 10), (S 3 = CH 3 -(CH 2 ) x -O- (CH 2 CH 2 O) n CH 2 -COOH; x = 11-13, n = 5) and (S 4 = CH 3 -(CH 2 ) x -O-(CH 2 CH 2 O) n CH 2 -COOH; x = 11-13, n = 2) were also used as supplied by Sigma-Aldrich. Protein cationization Coupling of DMPA to aspartic and glutamic acid residues on the external surface of met-mb was undertaken using carbodiimide activation. Briefly, solutions of DMPA were adjusted to ph 6 using 6 M HCl, and added dropwise to a stirred protein solution. The coupling reaction was initiated by adding EDC immediately. The ph was maintained using dilute HCl, and solutions were stirred for 12 h. The solutions were then centrifuged to remove any precipitate and the supernatant dialyzed (Visking dialysis tubing, 7 kda MWCO) extensively against high-purity water to produce stable solutions of the DMPA-cationized protein, C-Mb. Cationization efficiencies were assessed qualitatively using dynamic light scattering (DLS) coupled with zeta potential measurements ([protein] = 1 mg ml -1, Malvern Nano-Z instrument, average number of runs = 100), where the zeta-potential of native myoglobin in Milli-Q water at ph [-10 mv] was used for a point calibration. MALDI-TOF mass spectroscopy (Applied Biosystems, 4700 Proteomics analyser) was used to calculate the average number of DMPA molecules bound per protein molecule where native protein samples were run as blanks and the instrument settings were retained for the subsequent cationized protein measurements. nature chemistry 1
2 2 Protein-polymer surfactant nanoconjugates Complexation of the anionic polymer surfactants S 1, S 2, S 3 or S 4 to C-Mb was undertaken by adding an aqueous solution of the cationized protein (4 mg ml -1 ) to a stirred viscous liquid of the pure surfactant to give a protein : surfactant ratio of 1:3 w/w. The solution was then stirred for 12 h, centrifuged to remove any precipitate, and the supernatant dialyzed (Visking dialysis tubing 7 kda MWCO) extensively against Milli-Q quality water for 48 hours to produce aqueous solutions of the nanoconjugates, designated as [C-Mb][S x ] (x = 1-4). Nuclear Magnetic Resonance (NMR) spectroscopy (Bruker BioSpin GmbH 400) was used to study the effect of surfactant binding to [C-Mb] on the 1 H-NMR spectrum of S 2. Spectra were run at room temperature using D 2 O as a solvent at a concentration of 1 mg ml -1. The stability and stoichiometry of the dispersed Mbsurfactant (S 1 and S 2 ) nanostructures were investigated using analytical ultracentrifugation (AUC) at 25 C (Optima XL-I Beckman-Coulter). Sedimentation velocity experiments were performed on Mb-surfactant conjugates produced using cationized proteins with c < 0.04 mg ml -1 at a NaCl concentrations of 0.1 M. Protein melts Aqueous samples of the protein-surfactant nanoconjugates were lyophilized for 48 h and the resulting nanostructured ionic solids stored in a desiccator under vacuum. Solvent-free protein melts were prepared by heating the lyophilized/desiccated protein-surfactant nanoconjugates to temperatures of around 40ºC to produce clear viscous liquids of [C-Mb][S x ] (S x = S 1 or S 2 ). The decomposition temperature and residual water content of the protein melts were determined by thermogravimetric analysis (TGA) (TA Instruments Q500), and differential scanning calorimetry (DSC) (TA Instruments Q100) was used to map the enthalpic phase transitions between -70 and 70. Samples for DSC were heated/cooled at a rate of 10 C min -1, and isothermal cycles repeated to examine the level of reversibility and thermal hysteresis. Attenuated total reflectance FTIR (ATR-FTIR) (PerkinElmer 100 with a universal ATR accessory), diffuse reflectance UV- Vis (DR-UV-Vis) (Perkin-Elmer lambda 35 with a Labsphere RSA-PE-20 diffuse reflectance detector) and CD spectroscopies (Jasco J-810) were used to assess the level of secondary structure in the viscous Mb melts. Spectra were recorded from 260 to 190 nm at 200 nm min -1 with at least 32 accumulations at 20 C. In general, the CD spectra exhibited relatively low optical transparencies due to the high protein concentrations associated with the solvent-free liquids. Deoxy-Mb-containing nanoconjugates were produced by dialysing cationised met-myoglobin exhaustively against degassed Milli-Q water containing 0.06M Na 2 S 2 O 4 for 24 hours under a continuous nitrogen purge. After complexation of deoxy-[c-mb] with surfactant (S 1 ), the resultant conjugates were dialysed against degassed Milli-Q water containing 0.08M Na 2 S under a nitrogen atmosphere for 24 hours. The solution was then lyophilized for 48 hours and heated to 60 C in a dry environment under nitrogen to 2 nature chemistry
3 yield the corresponding deoxy-[c-mb][s 1 ] melt. The resultant material was stored in a sealed vial under a dry nitrogen atmosphere. Ligand binding assays Ligand binding experiments were undertaken by first applying a film of the deoxy-[c-mb][s 1 ] to the inside of a glass tube fitted with a Youngs tap under a nitrogen environment (see Figure overleaf). For SO 2 and CO binding studies, the modified Youngs tube was placed under vacuum overnight, and then connected to the corresponding cylinder and exposed to the appropriate gas. For SO 2 the pressure was controlled by means of an oil-bubbler, while for the CO experiment the sample was exposed to 1.5 bar of CO. For O 2 kinetic and equilibrium experiments, a purpose-built pressure apparatus was assembled, which allowed accurate control of the partial pressures of O 2, which were measured using the interfaced Pirani gauge. Figure. Pressure apparatus for the quantitative control of gas pressure. a) Gas inlet value connect to a drying column. b) Sample tube fitted with a Youngs tap immersed in a temperature-controlled oil bath. c) Parani gauge. d) Vacuum pump inlet. For kinetic and equilibrium dioxygen binding studies, a Gaussian function was fitted to the Soret band from each successive DR-UV-Vis spectrum, and the resulting wavelength ( ) used as an order parameter to define the fraction of oxygen saturation, Y, such that: obs Y sat U free (1) where obs is the observed Soret band peak wavelength, sat is the Soret band peak wavelength at full oxygen saturation, free is the Soret band peak wavelength for deoxy-mb, and U is the fraction of deoxy-mb molecules where: Y U 1 (2) nature chemistry 3
4 For equilibrium dioxygen binding experiments, the fraction of oxygen saturation (Y) as a function of dioxygen partial pressure (P) was fitted using the Hill equation to yield the Hill coefficient, h, and the oxygen affinity, P 1/2 where: 1 Y 1 P h 1/2 P (3) Figure S1. MALDI mass spectroscopy data confirming covalent conjugation of ca. 17 N,N-dimethyl-1,3- propanediamine (DMPA) molecules to myoglobin. Mass spectra from native myoglobin (black line) giving a molecular weight of Da, and from cationized myoglobin (red line) showing a broader distribution with a molecular weight of approximately Da. 4 nature chemistry
5 5 Figure S2. NMR spectra of S2 showing the effect of surfactant binding to [C-Mb]. a) 1H-NMR spectrum of S2 and assigned protein positions (insert). b) 1H-NMR spectrum of S2 bound to C-Mb showing an upfield chemical shift of 4.14 (F) to 4.00 (F*) ppm for protons on the carbon adjacent to the carboxylate headgroup. Samples were prepared from the [C-Mb][S2] melt after re-dissolution in D2O and recorded on a 400 MHz instrument. Proton signals from the surfactant dominate the spectrum as the relative abundance is high (protein : polymer surfactant ratio = 1 : 42; stoichiometric with respect to charge) and number of environments low (7 proton environments compared with hundreds for the protein). 5 nature chemistry
6 6 Figure S3. Overlay of normalized diffusion-corrected sedimentation coefficient distributions [c(s)] for [C- Mb][S1] in 0.1 M NaCl at 1:50 dilution (black line) and S1 in 0.1 M NaCl at 1:20 dilution (red line). Experiments were run at rpm at 25qC and s-distributions detected using absorbances at 280 nm. No free S1 was detected when interference optics were used (data not shown). The minor peak at 3.4 S indicates a small degree of self-association of [C-Mb][S1] in 0.1 M NaCl. Figure S4. Dynamic light scattering hydrodynamic diameter distributions showing the effect of cationization of Mb and subsequent electrostatic conjugation with S1. a) 0.5 mg ml-1 Mb at 25qC, b) 0.5 mg ml-1 C-Mb at 25qC and c) 0.5 mg ml-1 [C-Mb][S1] at 25qC. Inserts show corresponding correlation coefficient distributions. 6 nature chemistry
7 Figure S5. TGA traces (black lines) and corresponding first derivatives (blue lines) showing water content and decomposition temperature for (a) [C-Mb][S 1 ] and (b) lyophilized Mb. The temperature ramp-rate was 10 C/min and the temperature maintained at 110 C for 120 min. nature chemistry 7
8 Figure S6 Far-UV CD spectra showing minima at 208 and 222 nm for aqueous native myoglobin (black line), aqueous cationized myoglobin (red line), aqueous [C-Mb][S 1 ] conjugate before lyophilization (blue line), and [C-Mb][S 1 ] solvent-less melt (green line). CD traces have been offset in the y-axis for clarity. 8 nature chemistry
9 Figure S7. UV-Vis spectrum of cationized myoglobin showing a red-shifted Soret band (411 nm). Scan was performed at 25 C on a 0.06 mg ml -1 cationized myoglobin solution. Figure S8. Diffuse reflectance UV-Vis spectra showing associated shifts in Soret band for deoxy-[c-mb][s 1 ] (black line), oxy-[c-mb][s 1 ] (red line), CO-[C-Mb][S 1 ] (blue line) and SO 2 -[C-Mb][S 1 ] (green line). nature chemistry 9
10 Figure S9. ATR-FTIR spectrum of SO 2 -bound [C-Mb][S 1 ] (black line) showing the characteristic S=O stretch at 1323 cm -1 (arrow). For comparison the ATR-FTIR spectrum of met-[c-mb][s 1 ] is shown (red line). References 1. Blanco. E, J. M. Ruso, G. Prieto, F. Sarmiento, On relationships between surfactant type and globular proteins interactions in solution, J. Colloid Interface Sci. 316 (1), 37 (2007). 10 nature chemistry
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