Water Interactions with Membrane Proteins & Other Biomolecules from 1. H-X Heteronuclear Correlation NMR. Mei Hong Department of Chemistry, MIT
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1 Water Interactions with Membrane Proteins & Other Biomolecules from 1 H-X Heteronuclear Correlation NMR Mei Hong Department of Chemistry, MIT 4 th Winter School on Biomolecular Solid-State NMR, Stowe, VT, Jan , 2016
2 Diversity of water interactions with biomolecules SSNMR techniques: spin diffusion, HETCOR, & dipolar-dephased HETCOR Mechanism of water 1 H transfer: chemical exchange & spin diffusion Water for studying ion channels Open & closed states TM helix structure Site-specific hydrogen bonding Outline Hydration and H-bonding of Arg residues in antimicrobial peptides Dehydration & curvature induction of membranes by viral fusion proteins Water interactions with plant cell wall polysaccharides Water dynamics at low T: effects of cryoprotectants on membrane structure 2
3 Water is Important for Most Biological Systems Ion conduction & transport in ion channels Hydrogen bonding and charge distribution Hydration of polar & charged residues in proteins & carbohydrates Hydration & dehydration of membrane surfaces for function Low-temperature behavior of water: ice formation & glass formation 3
4 Water - Protein Heteronuclear Correlation NMR Williams & Hong, JMR,
5 Heterogeneous Water Dynamics of Hydrated Lipid Membranes Water dynamics of various lipid membranes: POPC/cholesterol POPE < POPG "Water" 1 H T 2 is the average T 2 of water & labile protons. Bulk water Inter-lamellar water on the membrane surface Water in transmembrane channels 5
6 Mechanism of Water Protein 1 H Polarization Transfer: Chemical Exchange & Spin Diffusion Doherty & Hong, JMR,
7 Diversity of water interactions with biomolecules SSNMR techniques: spin diffusion, HETCOR, & dipolar-dephased HETCOR Mechanism of water 1 H transfer: chemical exchange & spin diffusion Water for studying ion channels Open & closed states TM helix structure Site-specific hydrogen bonding Outline Hydration and H-bonding of Arg residues in antimicrobial peptides Dehydration & curvature induction of membranes by viral fusion proteins Water interactions with plant cell wall polysaccharides Water dynamics at low T: effects of cryoprotectants on membrane structure 7
8 Proton Conduction by the Influenza M2 Channel Khurana et al, PNAS, 106, 1069 (2009). Low ph? High ph Water protons Exchange & Spin diffusion M2 protons M2 13 C spins 8
9 Water-M2 Interaction in Lipid Membranes Luo & Hong, JACS,
10 1 H Polarization Transfer: Water-Protein Surface Area DQ detection to suppress lipid background 13 C signals Luo & Hong, JACS, I P (t m ) I P ( ) D eff π S WP V P t m 10
11 3D Lattice Simulations of Spin Diffusion M x,y,z (t m + Δt m ) = M x,y,z (t m ) + D ij Δt m M i (t m ) M x,y,z (t m ) i a 2 V prot = 12.7 nm 3 (ρ=1.43 g/cm 3 ). V Amt = 0.2 nm 3. Helix tilt: D WP = nm 3 /ms. Indirect W >L >P pathway ignored. [ ] 11
12 Model of the Water-Filled Pore: Drug Dehydrates the Channel ph Amt Luo & Hong, JACS,
13 Water-Exposed Surface Area of M2 Changes with Channel Opening and Drug Binding Luo & Hong, JACS,
14 Periodicity in TM Helix Bundle Structure from Water 1 H Polarization Transfer 14
15 Lipid- vs Pore-Facing Residues & ph-dependent Channel Diameters from Water Transfer Profiles Williams & Hong, JMR,
16 Helical Periodicity in Water Protein 1 H Polarization Transfer Profile Williams & Hong, JMR,
17 Proton Conduction Mechanism in M2 17
18 1 H Transfer Between Water & His37 From HETCOR R N...O = 2.63 Å Hong et al, JACS,
19 Diversity of water interactions with biomolecules SSNMR techniques: spin diffusion, HETCOR, & dipolar-dephased HETCOR Mechanism of water 1 H transfer: chemical exchange & spin diffusion Water for studying ion channels Open & closed states TM helix structure Site-specific hydrogen bonding Outline Hydration and H-bonding of Arg residues in antimicrobial peptides Dehydration & curvature induction of membranes by viral fusion proteins Water interactions with plant cell wall polysaccharides Water dynamics at low T: effects of cryoprotectants on membrane structure 19
20 Cationic Antimicrobial Peptides: Arginine- Phosphate Salt Bridges Protegrin-1 oligomeric structure: β-barrel in bacterial membranes Qu et al, Infect. Immun. 64, 1240 (1996). Extensive 13 C- 31 P REDOR distance data revealed the existence of Argphosphate salt bridges in PG-1 and other cationic AMPs: Stabilized by: electrostatic attraction hydrogen bonding Do water molecules play a role in stabilizing Arg-phosphate salt bridges? 20
21 HETCOR Spectra of an Antimicrobial Peptide PG-1 in POPE/ POPG membrane, 283 K Regular 1 H- 13 C & 1 H- 15 N HETCOR spectra do not allow unambiguous distinction of Hα and water protons (4.5-5 ppm). Li et al, J. Phys. Chem,
22 13 C- and 15 N Dipolar Dephasing in HETCOR: Distinguish Organic Protons from Water Protons Yao et al, JMR,
23 13 C, 15 N MELODI- HETCOR Allows Assignment of Water H N and guanidinium 1 H s assigned by 15 N MELODI. Hα (~4.8 ppm) assigned by 13 C MELODI. 2 ms HH-CP sufficient to detect water cross peak to guanidinium. Li et al, J. Phys. Chem, Membrane-bound Arg is solvated by water. 23
24 MD Simulations of Arg-Water Interactions in HIV Tat Tat: GRKKR RQRRR PPQ. A cationic cell-penetrating peptide. Herce & Garcia, PNAS,
25 Diversity of water interactions with biomolecules SSNMR techniques: spin diffusion, HETCOR, & dipolar-dephased HETCOR Mechanism of water 1 H transfer: chemical exchange & spin diffusion Water for studying ion channels Open & closed states TM helix structure Site-specific hydrogen bonding Outline Hydration and H-bonding of Arg residues in antimicrobial peptides Dehydration & curvature induction of membranes by viral fusion proteins Water interactions with plant cell wall polysaccharides Water dynamics at low T: effects of cryoprotectants on membrane structure 25
26 Virus-Cell Membrane Fusion Viral fusion requires High membrane curvature. Partial dehydration of the membrane surface. 26
27 What is the Conformation of the Transmembrane Domain of the Parainfluenza Virus? 27
28 TMD Conformation Also Depends on the Lipids Yao et al. PNAS,
29 Strand-Helix-Strand in PE Membranes Spontaneous curvature Helicity = I Cαβ/CαC, helix /(I Cαβ/CαC,helix + I Cαβ/CαC,strand ) 29
30 The Viral TMD Dehydrates PE Membranes 1 H- 31 P HETCOR The β-strand TMD reduces the % of membrane-bound water and increases bulk water %: the peptide dehydrates PE-rich membranes. Yao et al. PNAS,
31 TMD Induces Strong Curvature to PE Membranes + TMD DOPE 31 P chemical shift (ppm) 31 P chemical shift (ppm) TMD quantitatively converts the DOPE spectrum to an isotropic peak. 31
32 SAXS: TMD Induces an Ia3d Phase to DOPE Gerard Wong, UCLA Ia3d (gyroid) An Ia3d cubic phase coexists with an H II phase. Q-ratios for the Ia3d phase gives the lattice parameter, which suggests a hemifusion stalk with a waist of 10 nm, similar to the pure- DOPE stalk waist of ~ 9 nm. (Siegel, 1999). Yao et al. PNAS,
33 TMD Uses the β-sheet Conformation to Induce NGC & Stabilize Hemifusion Intermediates β-strands are anisotropic and can have different surface orientations, which can cause different curvatures to the two membrane leaflets. The NGC is characteristic of hemifusion intermediates. The β-strand is likely oligomerized into β-sheets. Yao et al. PNAS,
34 Diversity of water interactions with biomolecules SSNMR techniques: spin diffusion, HETCOR, & dipolar-dephased HETCOR Mechanism of water 1 H transfer: chemical exchange & spin diffusion Water for studying ion channels Open & closed states TM helix structure Site-specific hydrogen bonding Outline Hydration and H-bonding of Arg residues in antimicrobial peptides Dehydration & curvature induction of membranes by viral fusion proteins Water interactions with plant cell wall polysaccharides Water dynamics at low T: effects of cryoprotectants on membrane structure 34
35 Plant Cell Walls: A Carbohydrate-Protein Complex Cellulose microfibril Plant cell walls Provide rigidity to plant cells. Regulate plant growth. Store energy as carbohydrates. Surface cellulose Interior crystalline cellulose What is the 3D structural arrangement of polysaccharides in the cell wall? 35
36 Carbohydrate Structure in Plant Cell Walls Polygalacturonic acid (-) 36
37 Results from 2D & 3D MAS Spectra: Single- Network Model of the Plant Cell Wall Cellulose, hemicellulose, and pectins coexist in a single 3D network instead of two separate networks ( 13 C cross peak data) Hemicellulose does not coat the cellulose microfibril surface, but is embedded into the microfibril at limited spots. Pectins: one fraction binds cellulose and is immobilized, while another fraction is interstitial and highly dynamic. Dick-Perez et al, Biochemistry,
38 Water Dynamics is Sensitive to the Polysaccharide Content of the Cell Wall White Cosgrove & Hong, JACS,
39 Water-Polysaccharide 1 H Transfer: Buildup Curves Water-cellulose transfer lags behind water-matrix transfer. White Cosgrove & Hong, JACS,
40 Charge & Pore Size Affect Water Dynamics Ca 2+ crosslinked wall, more bound water, fast 1 H SD Ca 2+ -depleted CW, dynamic water, slow 1 H SD Sparse cell wall after extraction, fast 1 H SD rate. 40
41 2D HETCOR Reveals Dynamic Differences Between Bound & Bulk Water in Cell Walls White Cosgrove & Hong, JACS,
42 Diversity of water interactions with biomolecules SSNMR techniques: spin diffusion, HETCOR, & dipolar-dephased HETCOR Mechanism of water 1 H transfer: chemical exchange & spin diffusion Water for studying ion channels Open & closed states TM helix structure Site-specific hydrogen bonding Outline Hydration and H-bonding of Arg residues in antimicrobial peptides Dehydration & curvature induction of membranes by viral fusion proteins Water interactions with plant cell wall polysaccharides Water dynamics at low T: effects of cryoprotectants on membrane structure 42
43 Cryoprotection of Lipid Membranes for Low-T NMR Phase diagrams glycerol DMF Murata and Tanaka, Nat. Materials, 2012 Baudot & Boutron, Cryobiology,
44 Glycerol: Limited Cryoprotective Ability Lee & Hong, J. Biomol. NMR,
45 DMSO: Excellent Cryoprotection Down to 200 K Lee & Hong, J. Biomol. NMR,
46 Trehalose < Glycerol << PEG < DMF < DMSO Lee & Hong, J. Biomol. NMR,
47 T-Dependent 13 C Linewidths: DMSO Orders the Glycerol Backbone & Chain Termini Lee & Hong, J. Biomol. NMR,
48 DMSO Depth & Immobilization of Lipids β α The less mobile the lipid is at high T (e.g. by DMSO binding), the more ordered it is at low T. 48
49 Summary 1 H- 13 C, 1 H- 15 N, and 1 H- 31 P HETCOR with optional dipolar dephasing is a versatile approach for studying water interactions in many biomolecules: Ion channel structure and dynamics; TM helix protein topology; H-bonding to Arg to lower the ΔG of insertion of cationic membrane peptides; Membrane dehydration by viral fusion proteins; Water dynamics in complex biomaterials such as plant cell walls. 49
50 MIT & ISU Lipid hydration: Tim Doherty M2: Wenbin Luo, Jonathan Williams, Keith Fritzsching AMP: Shenhui Li, Ming Tang Viral fusion: Hongwei Yao, Yu Yang, Michelle Lee Plant cell walls: Tuo Wang, Paul White Low-T NMR: Myungwoon Lee Acknowledgement Collaborators Prof. Bill DeGrado, Jun Wang & Yibing Wu (UCSF) Prof. Alan Waring (UCLA) Prof. Gerard Wong (UCLA) Prof. Daniel Cosgrove (Penn State) Prof. Olga Zabotina (ISU) Funding 50
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