Isothermal Titration Calorimetry for Bioinorganic Chemists: Technical Issues, and Applications for New Insight Dean Wilcox
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1 Isothermal Titration Calorimetry for Bioinorganic Chemists: Technical Issues, and Applications for New Insight Dean Wilcox Department of Chemistry Dartmouth University College Hanover, NH
2 Calorimetry Outline 2014 Penn State Workshop Biomolecular Calorimetry Isothermal Titration Calorimetry (ITC) The Method: information, instruments, data, analysis Bioinorganic Applications Issues with metal ions Examples: His (Ni 2+ ), a teaching example Transferrin (Fe 3+ ) Ferritin (Fe 2+ ) Albumin (Cu 2+ ) His-rich sequence (Zn 2+, Fe 3+, Fe 2+, etc.) Metallothionein (Zn 2+, Cd 2+, As 3+, Pb 2+ ) UreE, a urease metallochaperone (Ni 2+, Cu 2+ ) Differential Scanning Calorimetry (DSC) The Method: information, instruments, data Bioinorganic Applications: Insulin (Zn 2+ ), Carbonic Anhydrase (Zn 2+ )
3 Outline 2016 Penn State Workshop Isothermal Titration Calorimetry (ITC) The Method: information, instruments, data, analysis Technical Issues Bioinorganic Chemistry Applications Issues with Metal Ions Examples: Metal-buffer interaction Azurin (Cu 2+, Cu + ) Metallothionein-3 (Pb 2+, Zn 2+ ) Ln 3+ -binding peptides (Dy 3+, Nd 3+ )
4 Thermodynamics of Metal Ions Binding to Proteins M n+ + Protein M n+ Protein - Equilibrium (K) K = [M n+ Protein] / [M n+ ][Protein] - Free Energy (ΔG) ΔG = -R T ln(k) - Enthalpy (ΔH) calorimetry: ΔH = q P - Entropy (ΔS) ΔG = ΔH - TΔS - Heat Capacity (C P ) ΔC P = ΔH 0 / T 0 - ΔH / T = ΔΔH / ΔT
5 Isothermal Titration Calorimetry
6 Isothermal Titration Calorimetry Time µcal/sec Raw Data kcal/mol of injectant Binding Isotherm Molar Ratio [Titrant/Cell] Capabilities - determine binding stoichiometry and K value (3 < log K ITC < 8). c = K [P] - complete thermodynamic profile in one experiment (ΔG, ΔH, ΔS). - determine ΔC p from temperature dependence of ΔH.
7 ITC: Uses 1. Basic Is there binding? What is the binding stoichiometry (n)? Caveat: generally softer number What is the binding affinity (K d )? Caveat: c window limitations 2. Intermediate What is the binding enthalpy (ΔH)? Caveat: measuring net ΔH ITC Is there coupled (de)protonation that accompanies binding (n H+ )? What is the binding entropy (ΔS)? Caveat: from comparable ΔG, ΔH 3. Advanced What is the change in heat capacity (ΔC p )? What are the effects of other perturbations (ionic strength, solvent, etc.)? Kinetics of binding?
8 ITC: What to do with the data? 1. Manipulation of the data. - baseline correction - subtract heat of dilution -integration control titration extended region of experimental data 2. Qualitative analysis of the data (critical evaluation). injection peaks? stoichiometry? c-window? enough heat? (concentration, conditions) (initial data à better data à optimal data à reproducible data) 3. Quantitative analysis of the data. a) Fitting to a model - Single binding site model à n, K, ΔH - Independent binding sites model (2) - Sequential binding sites model - Competition binding model à known K A, ΔH A ; unknown K B, ΔH B b) Post-hoc analysis of K ITC and ΔH ITC values (condition-dependent values à condition-independent values)
9 ITC: Technical Issues Red Flags Noisy data?: precipitate, air bubbles Irreproducible results?: cleanliness, air bubbles, chemistry (!) Low net heat (ΔH ITC )?: use another temperature, other conditions (buffer) Slow kinetics (return to baseline)?: faster stirring, higher temperature Sources of Error Binding stoichiometry (n): depends on two concentrations and volumes Binding enthalpy (ΔH): measuring net heat flow (post-hoc analysis) Binding constant (K): measuring overall equilibrium (post-hoc analysis) competing equilibria compare/confirm with other method(s)
10 ITC of Metal-Protein Interactions: Complications 1. Metal-Buffer Interactions * M(buffer) x +n M +n + X buffer 2. Metal Redox Reactions M +n + [O] 3. Metal Solution Chemistry M +(n+1) + [R] a) Hydrolysis L n M +n -H 2 O L n M +n -OH - + H + b) Precipitation / Dissolution L n M (aq) L n M (s) 4. Proton Displacement * M +n + Protein M +n Protein + n H + n H + + n buffer n bufferh +
11 ITC of Metal-Protein Interactions: Experimental Design 1. ph. - metal ions are Lewis acids and compete with H + - coupled equilibria involving H + are common with metal ions - need to account for heat associated with coupled (de)protonations 2. Buffer. a) interaction with the metal ion - can suppress side reactions of the metal ion (e.g., hydrolysis) - can provide a competing ligand for the metal ion - need to know K M-buff and ΔH M-buff b) interaction with H + - ΔH buff-h+ can be used to quantify H + s in coupled equilibria - use a buffer with larger heat of protonation to amplify signal 3. Other species? - reducing agent, complexing agent, salt, detergent, DMSO, etc.
12 Overall: (1-z)M 2+ + zmb 2+ + (1-x)L + xhl + + (x- z)b ML 2+ + xhb + Buffer- and ph-independent Equilibrium: M 2+ + L ML 2+ Thermodynamic cycles are required to obtain condition-independent values from condition-dependent experimental values (1-z)M 2+ + zmb 2+ + (1-x)L + xhl + + (x- z)b ML 2+ + xhb + ΔH ITC MB 2+ M 2+ + B z -ΔH MB HL + H + + L x -ΔH HL H + + B HB + x ΔH HB M 2+ + L ML ΔH ML
13 Penn State Workshop Tutorial: Cu 2+ à albumin Most abundant circulatory protein (~ 0.6 mm). Binds and transports Cu +2 and Ni +2 at its N-terminal X-X-His- binding site (not resolved in structure). Lys-4 ß HN R 1 CH C H 2 N 2+ M N O (-) N CH C N (-) Human Serum Albumin (PDB file 1UOR(HSA)) C H 2 CH CONHR R 2 O
14 Cu 2+ Binding to Albumin Cu +2 binding to bovine serum albumin (BSA) (reported, ph-independent, and ph 7.4 equilibrium constants Method ph Buffer Competing a log K reported b log K calc.. c log K ph 7.4 Reference Ligand Ultrafiltration 7.5 c MOPS (50 mm) Gly Giroux and Schoun, 1981 Dialysis Ryall d HEPES (30 mm) His Saltman, et al, d HEPPS (30 mm) His Saltman, et al, 1993 Ion-selective electrode 7.3 HEPES (20 mm) Ljones, et al, BisTris (46 mm) Ljones, et al, Acetate (25 mm) Ljones, et al, 1986 a) K reported = [Cu(BSA)]/[Cu 2+ ][BSA]; reported apparent binding constant at the given ph and experimental conditions. b) K calc.. = [Cu(BSA)][H + ] 2 /[Cu 2+ ][BSA]; intrinsic equilibrium constant for the reaction: Cu 2+ + BSA Cu(BSA) + 2H + c) K ph 7.4 = [Cu(BSA)]/[Cu 2+ ][BSA]; apparent binding constant at ph 7.4. Use competition with buffer (e.g. Tris) to measure high affinity Cu 2+ binding.
15 Cu 2+ Binding to Albumin Cu 2+ à BSA 100 mm Tris ph 9.2 (100 mm borate, 20 mm NaCl)
16 Cu 2+ -buffer interaction Time (min) Time (min) µcal/sec µcal/sec kcal mol -1 of injectant kcal mol -1 of injectant [CuSO 4 ]/[TEPA] 1.0 mm TEPA à 0.1 mm CuSO mm bis-tris, 100 mm NaCl [CuSO 4 ]/[DTPA] 1.2 mm DTPAà 0.1 mm CuSO mm bis-tris, 100 mm NaCl 16
17 Cu 2+ -buffer interaction (ph 7.0) TEPA DTPA Average of Both Ligands Buffer Log β n ΔH MB (kcal/mol) Log β n ΔH MB (kcal/mol) Log β n ΔH MB (kcal/mol) bis-tris 12.1 ± ± ± ± ± ± 0.4 TAPSO 13.0 ± ± ± ± ± ± 2 DIPSO 13.0 ± ± ± ± ± ± 0.4 TES 13.3 ± ± ± ± ± ± 0.4 Colette F. Quinn, Margaret C. Carpenter, Molly L. Croteau, Dean E. Wilcox Isothermal Titration Calorimetry of Metal Ions Binding to Proteins, in Methods in Enzymology, Vol. 567, Calorimetry, A. L. Feig, ed; Academic, 2016, pp
18 ITC Studies of Metal Ions Binding to Proteins 1. Cu 2+ and Cu + binding to Azurin 2. Pb 2+ and Zn 2+ binding to Metallothionein-3 3. Ln 3+ binding to peptides
19 Azurin Cu 2+ : Blue (PDB 4AZU) Cu + : Gray (PDB 1E5Y) Apo: Green (PDB 1E65) 19
20 Cu 2+ binding to Azurin: Blasie & Berg ph 7.0 Time (min) µcal/sec kcal mol -1 of injectant ΔH = 10.2 ± 1.6 kcal/mol K = 4.0 x (log K = 13.6) [CuCl 2 ]/[Azurin] 1.0 mm apo-azurin à mm CuCl mm cholamine +, 50 mm NaCl Blasie, C.A.; Berg, J.M. JACS, 2003, 125, Dunitz, J.D. Science, 1994, 264, 670. Amzel, L. Proteins Struct. Funct. Bioinforma. 1997, 28, ΔS = 19.9 cal/mol K ΔS Metal Dehydra.on ΔS Transla.onal ΔS Conforma.onal 20
21 Cu 2+ binding to Azurin ph 7.0 µcal/sec Time (min) Cu 2+ -Buffer Cu 2+ + Buffer ΔH MB Azurin-H m Azurin + m H + ΔH HP Cu 2+ + Azurin Cu 2+ -Azurin ΔH MP m Buffer + m H + m Buffer-H ΔH HB ΔΗ ITC = ΔΗ MP ΔΗ HP ΔΗ MB + m ΔΗ HB kcal mol -1 of injectant [CuSO 4 ]/[Azurin] ΔΗ MP ΔΗ HP = ΔΗ ITC + ΔΗ MB m ΔΗ HB Perform experiment in > 3 buffers: y = mx + b ΔH ITC + ΔH MB = m ΔH HB + (ΔH MP ΔH HP ) 1.0 mm CuSO 4 à 0.03 mm apo-azurin 100 mm bis-tris, 100 mm NaCl 21
22 Cu 2+ displacement of protons ph
23 Cu 2+ displacement of protons ph 7.0 A Cys112 His117 Cu 2+ Cys112 His117 Cu His His83 His His Cu Coordination 1.80 ± 0.04 H + displaced from metal site 0.06 ± 0.14 H + protonate His ± 0.15 H + protonate the buffer Experimental number of protons going to the buffer: 1.5 ±
24 Cu 2+ binding to Azurin ph 7.0 Buffer n log K ΔG (kcal/mol) ΔH (kcal/mol) TΔS (kcal/mol) ΔS (cal/mol K) Cu 2+ bis-tris 1.0 ± ± ± ± ± ± 2 TAPSO 1.0 ± ± ± ± ± ± 7 DIPSO ± ± ± ± ± 3 TES ± ± ± ± ± 4 Average 15.4 ± ± ± 1 23 ± 1 78 ± 3 Enthalpically unfavorable Coordination site is not tuned for Cu 2+ Entropically very favorable Cu 2+ desolvation; displaced protons; little rearrangement at site 24
25 Cu + coordination chemistry Prevent oxidation: anaerobic environment Suppress disproportionation: Cu + -stabilizing ligand 2 Cu + (aq) Cu2+ (aq) + Cu0 (s) K = 1.3 (± 0.8) x 10 6 Me 6 Trien (Me 6 T) ph 7.0 Cu I Me 6 TrienH log K = 13.6 ± 0.4 ΔH ML = -7.4 ± 0.5 kcal/mol 1,1,4,7,10,10-hexamethyltriethylenetetraamine 25
26 Cu + binding to Azurin ph 7.0 µcal/sec Time (min) Cu + -Me 6 T Cu + + Me 6 T ΔH ML Me 6 T + H + Me 6 T-H ΔH HL Azurin-H Azurin + H + ΔH HP Cu + + Azurin Cu + -Azurin ΔH MP m Buffer + m H + m Buffer-H ΔH HB ΔH ITC = ΔH MP ΔH HP ΔH ML + ΔH HL + m ΔH HB kcal mol -1 of injectant ΔH MP ΔH HP = ΔH ITC + ΔH ML ΔH HL m ΔH HB Perform experiment in > 3 buffers: y = mx + b [Cu + ]/[Azurin] 0.3 mm Cu + /16.5 mm Me 6 T à 0.03 mm apo-azurin/16.5 mm Me 6 T 100 mm HEPES, 100 mm NaCl ΔH ITC = m ΔH HB + (ΔH MP ΔH HP + ΔH HL ΔH ML ) 29
27 Cu + displacement of protons ph
28 Cu + displacement of protons ph 7.0 B H Cys112 His117 Cu + His117 H + Cu Cys112 + His His83 His His Cu Coordination 1.8 ± 0.04 H + displaced from metal site 0.45 ± 0.14 H + protonate His ± 0.03 H + protonate His ± 0.04 H + protonate Me 6 T 0.93 ± 0.15 H + protonate the buffer Experimental number of protons going to the buffer: 0.3 ±
29 Cu + binding to Azurin ph 7.0 Buffer n log K ΔG (kcal/mol) ΔH (kcal/mol) TΔS (kcal/ mol) ΔS (cal/mol K) HEPES 0.8 ± ± ± ± ± ± 4 PIPES 0.8 ± ± ± ± ± ± 5 Cu + ACES 0.6 ± ± ± ± ± ± 3 TES 0.5 ± ± ± ± ± ± 3 TAPSO 0.5 ± ± ± ± ± ± 5 Average 17.6 ± ± ± 1 7 ± 1 23 ± 2 Enthalpically very favorable Coordination site is tuned for Cu + Entropically favorable Cu + desolvation; displaced protons, but His35 & His83 protonated 29
30 Metallothionein MDPNCSCAADGACTCATSCKCKECKCTSCKKSCCSCCPSGCAKCAQGCICKGASDKCSCCA Relative metal ion affinity: Ni 2+ ~Co 2+ <Zn 2+ <Cd 2+ ~Pb 2+ <Ag + ~Cu + <Hg 2+ Krezel and Maret have reported that 4 Zn 2+ bind with K = 6 x 10 11, 2 Zn 2+ bind with K ~ and 1 Zn 2+ binds with K = 5 x 10 7.
31 Metallothionein-3 MDPNCSCAADGACTCATSCKCKECKCTSCKKSCCSCCPSGCAKCAQGCICKGASDKCSCCA MDPETCPCPSGGSCTCADSCKCEGCKCTSCKKSCCSCCPAECEKCAKDCVCKGGEAAEAEAEKCSCCQ Collaboration with Rachel Austen (Bates à Barnard) MT-3 is the metallothionein isoform found in neuronal tissue Unique Pro residues in N-terminal β domain and insert in C-terminal α domain High affinity for Pb 2+ suggests potential role in lead neurotoxicity Quantify Pb 2+ binding to MT-3 and competition with Zn 2+
32 Metallothionein-3 Pb2+ à Zn7MT3 ph 6.0, 100 mm MES, 25 ± 0.2 C, 307 rpm Best Fit values: nitc = 5.8 ± 0.03 KITC = 3.1 (± 0.2) x 105 ΔHITC = ± 0.05 kcal/mol Average values: nitc = 6.9 ± 1.5 KITC = 3 x 105 ΔHITC = -9 kcal/mol
33 Metallothionein-3 EDTA à Pb 7 MT3 ph 6.0, 100 mm MES, 25 ± 0.2 C, 307 rpm One set of sites: n ITC = 0.50 ± 0.01 K ITC = 8.3 (± 0.1) x 10 5 ΔH ITC = -7.8 ± 0.1 kcal/mol Two sets of sites: K 1ITC = 3 (± 1) x 10 8 ΔH 1TC = -0.7 ± 0.1 kcal/mol K 2TC = 1.7 (± 0.2) x 10 6 ΔH 2ITC = -5.0 ± 0.03 kcal/mol Competition: K EDTA = 1.3 x (fixed) ΔH EDTA = -11 kcal/mol (fixed) K MT = 8 (± 2) x ΔH MT = -6.6 kcal/mol (fixed)
34 Metallothionein-3 EDTA à Zn 7 MT3 ph 6.0, 100 mm MES, 25 ± 0.2 C, 307 rpm One set of sites: n ITC = 0.17 ± 0.01 K ITC = 2.3 (± 0.6) x 10 6 ΔH ITC = -6.5 ± 0.2 kcal/mol Two sets of sites: K 1ITC = 1.3 (± 0.3) x 10 8 ΔH 1TC = ± 0.03 kcal/mol K 2TC = 3.9 (± 0.5) x 10 5 ΔH 2ITC = -4.3 ± 0.1 kcal/mol Competition: K EDTA = 4.1 x (fixed) ΔH EDTA = -7.6 kcal/mol (fixed) K MT = 7.8 (± 0.7) x ΔH MT = -3.2 kcal/mol (fixed)
35 Metallothionein-3 Experimental enthalpies of metal ions binding to MT-3 at ph 6.0, and analysis to obtain the buffer-dependent binding enthalpies; units of kcal/mol. Analysis to determine buffer-independent formation enthalpies for M 7 MT-3 and the formation enthalpies with deprotonated Cys thiols; units of kcal/mol
36 Metallothionein-3 Thermodynamic values for the three populations of metal ions binding to MT-3 at ph 6.0 and 298 K. a) units of kcal/mol, b) units of cal/mol K M. C. Carpenter, A. Shami Shah, S. DeSilva, A. Gleaton, A. Su, B. Goundie, M. L. Croteau, M. J. Stevenson, D. E. Wilcox, R. N. Austin, Thermodynamics of Pb(II) and Zn(II) Binding to MT-3, a Neurologically Important Metallothionein, Metallomics, 2016, in press
37 Ln 3+ -binding peptides Lanthanide-binding peptides (Lamp) have been selected with phage display Bind to Ln 3+ -hydroxo species and form insoluble aggregates Potential applications in separation of Ln 3+ ions from seawater and wastewater Aggregates and their formation have been characterized by several methods: ICP-OES, FT-IR, SEM, TEM, EDX, EXAFS, NMR and ITC (i) Nucleophilic attack (ii) Generation of Ln-hydroxide Lamp (iii) Stabilization of Ln-hydroxide (iv) Hydrophobic accumulation (v) Precipitation
38 µcal/sec kcal/mole of injectant Ln 3+ -binding peptides Dy 3+ à Lamp-1 Dy 3+ à Lamp-2 Nd 3+ à Lamp-3 b d 2 Supplementary Figure S17 a c kcal/mole of injectant µcal/sec µcal/sec kcal/mole of injectant µcal/sec kcal/mole of injectant b µcal/sec kcal/mole of injectant d kcal/mole of injectant µcal/sec Dy 3+ à LBT3 (control) kcal/mole of injectant µcal/sec Molar Ratio Molar Ratio Molar Ratio Supplementary Figure S17. Thermodynamic analysis of the mineralization reaction. ITC experiments for the reaction of Dy 3+ with (a) Lamp-1, (b) Lamp-2, and (c) LBT3, and (d) Nd 3+ with Lamp-3. The upper panels show the calorimetric titration profile. The lower panels show a least squares fit of the data to the heat absorbed/mol of titrant versus the ratio of the total concentration of Dy 3+ or Nd 3+ to the total concentration of peptide. The solid line is the best fit of
39 Ln 3+ -binding peptides Thermodynamic values from ITC measurements of Ln 3+ binding to peptides. Peptide Target H (kcal/mol) -T S (kcal/mol) G (kcal/mol) K (x10 3 M -1 ) N Lamp-1 Dy ± ± ± ± a Lamp-2 Dy ± ± ± ± a LBT3 Dy ± ± ± ± ± 0.01 RE-1 Dy 3+ n.d n.d n.d n.d n.d Lamp-3 Nd ± ± ± ± a was calculated using the equation = -RT ln a) assumed to be 1
40 ITC of Metal-Protein Interactions 1. General - know the metal chemistry (e.g., disproportionation of Cu + ; solubility) 2. Azurin - delivery of metal in well-defined complex with buffer or chelate avoids unwanted (unknown) reactions, and allows high affinity binding sites to be studied - number of protons displaced upon metal binding at a given ph can be quantified with ITC data in different buffers 3. Metallothionein-3 - it may be necessary or useful to measure the extraction (chelation) of the metal from the protein by a chelating agent and analyze with microscopic reversibility, after accounting for chelate-metal thermodynamics (ΔH, K). 4. Lanthanide-binding peptides - correlation between ITC data and molecular processes can be challenging in complex systems (N. E. Grossoehme, A. M. Spuches, D. E. Wilcox J. Biol. Inorg. Chem , )
41 Acknowledgements Yi Zhang G'01 Shreeram Akilesh '00 Dr. Anne Rich Austin Schenk '00 Nick Grossoehme G 07 (Winthrop U) Dr. Anne Spuches (E Carolina U) Colette Quinn G 09 (TA Instruments) Jolene Schuster G 09 NIH ES07373 Dartmouth Superfund Research Program Jessica Son 11 Becky Rapf 12 Molly Carpenter G 14 George Lisi G 14 Max Png 14 Molly Croteau G 15 *Michael Stevenson G 16 *Michael Cukan G 18 NSF CHE and CHE Thermodynamics of Metal-Protein Interactions
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