Biomolecular Modelling
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1 Biomolecular Modelling Carmen Domene Physical & Theoretical Chemistry Laboratory University of Oxford, UK
2 THANKS Dr Joachim Hein Dr Iain Bethune Dr Eilidh Grant & Qi Huangfu 2
3 EPSRC Grant, Simulations for Chemical Biology ( 210,000), 2009 EPSRC Grant, Quantum simulations for Chemical Biology ( 390,000), ~ 9 Million Aus (Open Access Initiative) CODEs (A) NAMD2.6 // 2.7 (IMD) and VMD NAMD2.6 modified to include Metadynamics technique (Visual Molecular Dynamics) 256 proc. Memory is not an issue. Data storage might be... (B) CPMD: 64 proc. 3
4 Some Publications Atypical mechanism of conduction in potassium channels. S. Furini, C. Domene, Proc. Natl. Acad. Sci. USA, 2009, 106 (38) Dynamics, energetics and selectivity of the low-k + KcsA channel structure. C. Domene, S. Furini, J. Mol. Biol. 2009, 389, Permeation of water through the KcsA K + channel. S. Furini, O. Beckstein, C. Domene, Proteins, 2009, 74 (2), Conformational changes and gating at the selectivity filter of potassium channels. C. Domene, M. L. Klein, D. Branduardi, F. L. Gervasio, M. Parrinello, J. Am. Chem. Soc. 2008, 130 (29) Polarization effects and selectivity in K + channels. C. Illingworth, S. Furini, C. Domene (submitted). 4
5 Membrane Proteins Biological Membrane = Lipid Bilayer + Membrane Proteins Selective Permeability due to Channel & Transport Proteins Receptors & Recognition on Membrane Bound Enzymes Molecular Cell Biology, Fourth Edition W. H. FREEMAN,
6 6 Active vs Passive transport of K + ions
7 7 Ion permeation in K + -channels
8 Permeation and Selectivity Sext S0 S1 S2 S3 S4 Cav Crystallographers assume in their refinements that if a site is not occupied by an ion, the site is likely to be occupied by a water molecule Zhou, Morais-Cabral, Kaufman, MacKinnon Nature,
9 Aqvist & Luzhkov, Nature 2000 Permeation and Selectivity Berneche & Roux, Nature 2001 The most favourable pathway for ion translocation ti is the simple cycling between states 1010(1) and 0101(1) Largest free energy barrier ~ 2 3 kcal mol -1 Barrier for passage from 1010(1) to Each colour level =1 kcal mol (1) = 6 kcal mol -1 Lowest energy pathway= Dotted line Among 3-ion states only 1101(1) has The position of the ions, Z 1, Z 2 and Z 3 a non-prohibitive free energy relative to the resting state, which, in effect, excludes any mechanism involving the three-ion states 9
10 Site 4 is mutated (i) Occupancy of S4 and S2 is reduced (ii) S1 and S3 unaltered (iii) The mutation reduces the total occupancy of the filter and complicated cated kinetic models were used to relate conduction and occupancy but these calculations have not given deeper insight into the conduction mechanism KWK mechanism KWK mechanism X X S2: Valid S1/S3: Valid 10
11 11 Classical Mechanism of permeation
12 12 Atypical Mechanism of Permeation??
13 Comparison of mechanisms of permeation Conduction Conduction KirBac KcsA Mechanism Direction [kcal/mol] [kcal/mol] KWK Outward 2.81 ± ±0.48 Inward 2.72± ±0.67 KK Outward 2.10± ± Inward 2.60± ±0.40 Both mechanisms display similar energy barriers In both, movement of one ion tends to assist others to travel in the same direction The KK mechanism is in agreement with experimental observations, and explains some others that did not fit within the KWK model 13
14 Comparison of mechanisms of permeation 1.45±0.33 kcal/mol in KcsA 0.82±0.77 kcal/mol in KirBac ΔG solvation for a K + ion in Cavity or S ext is in both mechanisms: 1.00±0.30 kcal/mol in KcsA 0.68±0.41 kcal/mol in KirBac 14 S. Furini & C. Domene, PNAS 2009, 106 (38)
15 KK mechanism Site 4 is mutated KWK mechanism KK mechanism X X X X X X S2: Valid S1/S3: Valid Not valid Not valid S1/S2 or S2/S3 S1-X-S3: S3: Valid Valid 15
16 Some Conclusions Alternative ti pathways to the KWK exit Vacancies can be implicated in the conduction mechanism The KK mechanism described here is likely to be just one example among the plethora of alternative configurations and conduction pathways thatt ions and water may adopt during permeation 16
17 Water flow through the empty bacterial potassium channel KcsA Peter Pohl, Proc. Natl. Acad. Sci. USA 2004, 101, Ion channels may yplay a secondary role as water channels E.G. neurons lack channels specialised in water transport, maybe K + -channels contribute to water homeostasis Water flow occurs only when all ions are rinsed out of the filter Water move through KcsA 1000 times faster than K + 17 Hypothesis: all binding sites are occupied by water
18 Transport of water through KcsA Osmotic permeability = cm 3 /s 80 windows (2ns/window) Furini S., Beckstein O., Domene C. Proteins, 74(2) ,
19 Selectivity filter in the absence of ions 19 GROMOS/SPC CHARMM/TIP3P Pressure MD ΔP=200MPa E. Tajkhorshid et al. Biophys J. 83, 2002
20 Some Conclusions Structural rearrangements of the SF take place in the absence of K + ions that allow for rapid water permeation, as experimentally observed The SF collapses to an hour-glass shape, and the central pore is blocked Water molecules can flow at high rates through KcsA by alternative paths to the central pore, that is behind the SF instead Can the addition of K + ions refold the SF to the four-fold symmetrical functional ion filter? 20
21 Gating
22 Gating
23 Activated Events Δ CLOSED OPEN How to Explore this Multidimensional Free Energy Surface? 23
24 Metadynamics Laio & Parrinello, PNAS 2002 Filling the wells adding small Gaussians: the forces are changed with a time-dependent term. The dynamics brings us to the closest local minimum of E(s) plus the sum of all the Gaussians E(s) Vr ( ) sr ( ) sr ( ) 2 F i ' t wexp 2 r r t' t 2δ s i i < = s Forces from the normal potential Forces from Gaussians localized on configurations already explored 24
25 Permeation and Metadynamics Is there a physical gate at the selectivity filter? RMSD 0.6 Å 25 Domene C, Klein ML, Branduardi D, Gervasio F, Parrinello M, JACS 130(29)
26 K + permeation and Metadynamics Crystal structure Val flip commonly observed in MD S2 disappears 26 Domene C, Klein ML, Branduardi D, Gervasio F, Parrinello M, JACS 130(29)
27 The Path Collective Variable S Collective Variable Path = a sequence of plausible intermediate configurations R(t) between two states (Interpolation). Choose first frame, last frame and atoms involved. S measures progress along the path Z Collective Variable Measures distance from the tread S=0 ; B S=0 B S=0 S=1 B B A A A A 27 D. Branduardi et al JChem Phys 2007
28 Metadynamics with S and Z Conformational Changes Backbone atoms of SF Position 1 K + ion ) (Å 2 ) Barrier = ~6 Kcal/mol l S0 S1 S2 S3 S4 1. G Y G V T 28
29 Some Conclusions There is a physical gate at the selectivity filter of K-channels. The selectivity filter is not rigid as initially thought, and its flexibility is crucial. The selectivity filter adopts at least two conformations: conductive and non-conductive. In-built mechanism for adjusting to high and low K+ concentrations. The conserved Gly residues are a requirement to fulfil specific dihedral angles during the course of these transformations. 29
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