Padua 15 April 20101 Interface Physics Group Biophysics The FluRedox Principle: Biosensors and Sensing Single Enzymes Leiden University Nijmegen U. R.

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Padua 15 April Interface Physics Group Biophysics The FluRedox Principle: Biosensors and Sensing Single Enzymes Leiden University Nijmegen U. R. Nolte A. Rowan H. Engelkamp N. Hatzakis A. Patil Oxford U. J. J. Davis G. Mizzon T. LION, Biophysics J. Aartsma M. Elmalk J. Salverda N. Akkilic Lorentz/EdRox, 1 Nov 2010 S. L. Tabares Zauner LIC, METPROT G. W. Canters G. Kuznetsova A. Tepper D. Heering M. Strianese Newcastle U. C. Dennison D. Kostrzc

2 Förster Resonant Energy Transfer FRET Lorentz/EdRox, 1 Nov 2010

3 Fluorescence detection of redox state No FRET FRET +e - -e - Energy Reduced Oxidized Lorentz/EdRox, 1 Nov 2010

Proof of principle Anal. Biochem. 350 (2006) 52  Now for: Lorentz/EdRox, 1 Nov 2010

5 Single Molecules Lorentz/EdRox, 1 Nov 2010

6 Proc. Natl. Acad. Sci. (1961), Lorentz/EdRox, 1 Nov 2010

7 Oil β-D-Galactosidase B. Rotman, P.N.A.S. 1961, 47, Oil H2OH2O The first single enzyme experiment (1961) + Lorentz/EdRox, 1 Nov 2010

8 H. P. Lu, L. Xun, X. S. Xie, Science, 1998, 282, H 2 O 2 O 2 Fluorescent Cholesteroloxidase Cox in oxidized form Lorentz/EdRox, 1 Nov 2010

9 FRET & Electrochemistry: Fluorescent CV The quest for single molecules Lorentz/EdRox, 1 Nov 2010

10 Fluorescence detection with Potentiostatic control Potentiostat Protein with attached dye CCD camera Fluorescence microscope Reference electrode Work electrode Counter electrode Gold with C8 monolayer and wt-azurin Lorentz/EdRox, 1 Nov 2010

11 Fluorescence image (32x32 μm) of WT azurin 200 mV/s Cyclic Voltammetry Lorentz/EdRox, 1 Nov 2010

12 37 μm 16 μm Fluorescence traces show cyclic redox switching Widefield (Leiden): near-monolayer w. variable brightness TIRF (Oxford): very low coverage in clusters Results – fluorescence switching Lorentz/EdRox, 1 Nov 2010

13 10 mV/s 100 mV/s 1 V/s FCV and CV: increase of separation to ~40 mV at 1V/s (widefield (Leiden) data example, FCVs from full images) Scan rate dependence Scan rate (V/s) Potential (mV, vs. SCE) Lorentz/EdRox, 1 Nov 2010

14 E 0 dispersion much larger in more dilute TIRF sample! TIRF (N42C) (Oxford) Widefield (wt azurin) (Leiden) Thermodynamic (E 0 ) dispersion E 0 vs. SCE (mV) Frequency Lorentz/EdRox, 1 Nov 2010

15 * Large k 0 dispersion in both datasets! * Factor 100 difference within 10 micron on surface possible Kinetic (k 0 ) dispersion TIRF (N42C) (Oxford) Widefield (wt azurin) (Leiden) Angew. Chemie 2010, in press Frequency Lorentz/EdRox, 1 Nov 2010

16 Dispersion E 0  Protein-protein complexes  Effect of charges  Dielectric between partners  Protein-surface interaction  El. Fields of 3-30mV/Å ΔE 0 : mV Batie & Kamin, JBC 256(1981)7756 Knaff cs BBA 635(1981)405 Davidson cs JBC 263(1988)13987 Haehnel cs Biochem 35(1996)1282 Murgida & Hildebrandt Chem S Rev 37(2008)937 Lorentz/EdRox, 1 Nov 2010

17 n Dispersion k 0 k0k0 Feng et al. J.Chem.Soc. Far. Trans , 1367 Lorentz/EdRox, 1 Nov 2010

18 Nitrite Reductase NiR Lorentz/EdRox, 1 Nov 2010

19 Cu-containing Nitrite Reductase - NiR NO 2 - e-e- e-e- X ox NO X red Lorentz/EdRox, 1 Nov 2010

20 What will happen during turnover? e-e- NO 2 - NO Ex Em Ex Em Lorentz/EdRox, 1 Nov 2010

21 NO e - + 2H +  NO + H 2 O Nitrite Reductase J. Biol. Chem. 281 (2006) Lorentz/EdRox, 1 Nov 2010

22 Confocal Fluorescence Spectroscopy of NiR Lorentz/EdRox, 1 Nov 2010

23 Experimental set-up Detection pinhole Single photon detector Objective Sample plane Point laser light source PNAS (2008) 105, Lorentz/EdRox, 1 Nov 2010

24 Measuring single molecules at work Background Inactive and bleaches Turning over and bleaches Turnover! Lorentz/EdRox, 1 Nov 2010

25 Intensity histogram Counts / 10 ms Counts / 10 ms Time, s Number of bins counts/bin Binsize: 10 ms Poissonian distributions Lorentz/EdRox, 1 Nov 2010

26 NiR - ATTO 655 turnovers with asc/PES 20mM HEPES pH7 10mM NO 2 - 3mM ascorbate 0.3 nM PES high Counts / 10 ms Time, s bg low high Counts / 10 ms Time, s bg low Number of events Fluorescence intensity, counts/10 ms Lorentz/EdRox, 1 Nov 2010

27 Autocorrelation: Correlation of a signal with its time-shifted image. Fluorescence time trace: AUTOCORRELATION Fluorescence t 1 t2t2 t Lorentz/EdRox, 1 Nov 2010

28 λ 1, λ 2 : f (k i ) S1S1 S2S2 S3S3 k3k3 k -3 k1k1 k2k2 k -2 k -1 OO RORO OR k3k3 k1k1 k2k2 e NO 2 - NO k -3 Qian & Elson Biophys Chem (2002) 565 Lorentz/EdRox, 1 Nov 2010

29 [NO 2 - ]-dependent autocorrelation decay timing The autocorrelation curves can be fitted to a stretched exponential:  =    ms X Lorentz/EdRox, 1 Nov 2010

30 Single exponential means Single rate: Stretched exponential means Distribution of rates: τ/τ0τ/τ0 ρ Mumbai 4 Nov 2009

31 Why a "stretched" instead of a simple exponential?  In the stretched exponential  is not a single value but a distribution  The distribution of  depends on  : if  =1, there is no distribution in  if  <1, the distribution becomes broader s s s s [NO 2 - ] 5  M 50  M 500  M 5000  M   = 0.6  1 order of magnitude distribution WHY? Mumbai 4 Nov 2009

32 A partial disorder at the catalytic heart of NiR First coordination sphere - Type-1 Cu site: Met150 is partially disordered - Type-2 Cu site: The water ligand is disordered in the reduced state Proton delivery - His255: is partially disordered - Asp98 : has a large B-factor - Network of water molecules PNAS 105 (2008) 3250 Lorentz/EdRox, 1 Nov 2010

33 How can we get the kinetics parameters? Global fit: 1/  [s -1 ] Mumbai 4 Nov 2009

34 How can we get the kinetics parameters? k 1 = 3.5 x10 5 M -1 s -1 k 2 = 9.5 s -1 k 3 = 21 s -1 k -3 = 14 s -1 Electron Transfer Rate between Cu1 and Cu2! K M = k 2 ( k 3 + k -3 ) k 1 ( k 2 + k 3 ) = 31  M V max = k2k3k2k3 ( k 2 + k 3 ) = 6.5 s -1 In good agreement with in-bulk measurements : 50  M and 8.0 s -1 Mumbai 4 Nov 2009