Biomembranes platform talk for the annual Biophysical Society Meeting 2016
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Transcript of Biomembranes platform talk for the annual Biophysical Society Meeting 2016
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1Department of Chemistry and Biochemistry, University of Arizona, Tucson, AZ, USA 2Department of Physics, Indian Institute of Science, Bangalore, India
3Department of Physics, University of Arizona, Tucson, AZ, USA
Soohyun K. Lee1, Trivikram R. Molugu1, K.J. Mallikarjunaiah1,2, Michael F. Brown1,3
Elastic Deformation And Collective Dynamics in Lipid Membranes: A Solid-state 2H
NMR Relaxation Study
BPS platform talk 20163/1/2016, 4:00 PM
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J.J. Kinnun et al. (2015) BBA 1848, 246
How Does Hydration Affect Lipid Membranes And
Dynamics?
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How Does Hydration Affect Lipid Membranes And Dynamics?
Parsegian: X-ray diffraction - bilayer thickness increases with decrease in water level
Nagle: X-ray diffraction and diatometry Gawrisch: X-ray diffraction and infrared
measurements – bilayer thickness also changes with polyunsaturated lipids
Mallikarjunaiah: Solid-state 2H NMR - bilayer thickness is very sensitive to the hydration levels
Lets examine the membrane from the dynamics standpoint!
K.J. Mallikarjunaiah et al. (2011) Biophys. J. 100, 98
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• Introduction to solid-state 2H NMR experiments
• Model-free interpretation of lipid relaxation data
• Collective lipid dynamics
• Hydration-induced slow dynamics
• Conclusions
Outline of the Talk
J.J. Kinnun et al. (2015) BBA 1848, 246K.J. Mallikarjunaiah et al. (2011) Biophys. J. 100, 98
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• Introduction to solid-state 2H NMR experiments
• Model-free interpretation of lipid relaxation data
• Collective lipid dynamics
• Hydration-induced slow dynamics
• ConclusionsJ.J. Kinnun et al. (2015) BBA 1848, 246K.J. Mallikarjunaiah et al. (2011) Biophys. J. 100, 98
Outline of the Talk
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• Line shape measurements– Reveal motional amplitudes– Gives structural information
like in X-ray crystallography• Relaxation measurements– Depends on motional
amplitudes and rates– Informative on molecular
motions over a wide frequency range
Solid-state 2H NMR Experiments Are Done in Two Ways
A. Leftin et al. (2014) eMagRes 3, 199X. Xu et al. (2014) eMagRes 3, 275
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• Line shape measurements– Reveal motional amplitudes– Gives structural information
like in X-ray crystallography• Relaxation measurements– Depends on motional
amplitudes and rates– Informative on molecular
motions over a wide frequency range
Solid-state 2H NMR Experiments Are Done in Two Ways
A. Leftin et al. (2014) eMagRes 3, 199X. Xu et al. (2014) eMagRes 3, 275
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A. Leftin, M.F. Brown (2011) BBA 1808, 818
Solid-state 2H NMR Gives Site-resolved Information for Bilayers
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J.J. Kinnun et al. (2015) BBA 1848, 246
Solid-state 2H NMR Gives Site-resolved Information for Bilayers
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Closure Property of Reference Frames in Solid-state 2H NMR Experiment
A. Leftin et al. (2014) eMagRes 3, 199X. Xu et al. (2014) eMagRes 3, 275
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A. Leftin et al. (2013) JMB 425, 2973A. Leftin et al. (2011) BBA 1808, 818
Hierarchy of Membrane Dynamics
Molecular motions near the Larmor frequency contribute to Relaxation NMR relaxation methods are suitable to probe such dynamics.
Motions Collective Motions
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(b)
(c)
NMR Relaxation Experiments(a)
Quadrupolar echo-T2
T1 inversion recovery
CPMG-T2
A. Leftin et al. (2011) BBA 1808, 818X. Xu et al. (2014) eMagRes 3, 275
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• Introduction to solid-state 2H NMR experiments
• Model-free interpretation of lipid relaxation data
• Collective lipid dynamics
• Hydration-induced slow dynamics
• Conclusions
Outline of the Talk
J.J. Kinnun et al. (2015) BBA 1848, 246K.J. Mallikarjunaiah et al. (2011) Biophys. J. 100, 98
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Model-free Interpretation of Lipid Relaxation Data
Gateway to discoveries on membrane motions
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Relaxation Measurements Are Related to Quasi-elastic
Properties
• D is the viscoelastic property, the lower the stiffer (Viscosity is and K is the elastic constant)
• The linear dependence is due to the slow collective dynamics• Assumptions are that the sample is large vesicles and motions are of
bilayer dimension
X. Xu et al. (2014) eMagRes 3, 275
G.V. Martinez et al. Phys. Rev. E (2002) 66 050902
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M.F. Brown (1984) JCP 80, 2832A.A. Nevzorov & M.F. Brown (1997) JCP 107, 10288
Order Fluctuations & Elastic Membrane Deformation
3D membrane deformation model:
2D flexible surface model:
Free membrane limit (l < t < d)
Strongly coupled limit (t << d < l)
Free membrane limit (t << l < d)
3D quasi-elastic deformations (Brown)
smectic undulations (Blinc) peristaltic fluctuations
free planar membrane (Marqusee;Kothe; Blinc)
Vesicle shape fluctuations (Vilfan; Kothe)
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• Introduction to solid-state 2H NMR experiments
• Model-free interpretation of lipid relaxation data
• Collective lipid dynamics
• Hydration-induced slow dynamics
• Conclusions
Outline of the Talk
J.J. Kinnun et al. (2015) BBA 1848, 246K.J. Mallikarjunaiah et al. (2011) Biophys. J. 100, 98
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A. Leftin et al. (2011) BBA 1808, 818
Effect of Head Group on Membrane
Elasticity
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• Linear square-law plot shows presence of collective dynamics
• For a given lipid, slope of the square-law plot is temperature independent
• The thermal energy is spent on structural perturbation
• Elastic properties do not change in liquid-crystal phase upon heating
Effect of Temperature on Membrane Structure And
Elasticity
A. Leftin et al. Biophys. J. (2014) 107, 2274 A. Leftin et al. J. Mol. Biol. (2013) 425, 2973
R1Z / s−1
45
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• Correspondence of NMR observables with material properties
• Progressive increase in bilayer stiffness with increasing sterol content
• Emergence of bilayer elasticity over atomistic distances!
• Evolution of biophysical function?
Bending Energies Deduced from
2H NMR Spin–lattice Relaxation
M.F. Brown et al. (2001) Phys. Rev. E 64, 010901G.V. Martinez et al. (2002) Phys. Rev. E 66, 050902
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Outline of the Talk
J.J. Kinnun et al. (2015) BBA 1848, 246K.J. Mallikarjunaiah et al. (2011) Biophys. J. 100, 98
• Introduction to solid-state 2H NMR experiments
• Model-free interpretation of lipid relaxation data
• Collective lipid dynamics
• Hydration-induced slow dynamics
• Conclusions
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Outline of the Talk
J.J. Kinnun et al. (2015) BBA 1848, 246K.J. Mallikarjunaiah et al. (2011) Biophys. J. 100, 98
• Introduction to solid-state 2H NMR experiments
• Model-free interpretation of lipid relaxation data
• Collective lipid dynamics
• Hydration-induced slow dynamics
• Conclusions
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Spin-lattice Relaxation Rates Indicate Collective Order-director
FluctuationsDMPC-d54
A. Leftin et al. (2013) J. Mol. Biol 425, 2973A. Leftin et al. (2014) Biophys. J. 107, 2274
Spin-Lattice Relaxation Rates Indicate Collective Dynamics in
Membrane Lipids
POPC-d31
• Segmental order parameters and spin-lattice relaxation rates follow a theoretical square-law functional dependence
• Temperature independent square-law plots indicate collective membrane dynamics similar to nematic liquid-crystals
R1Z / s−1
R1Z / s−1
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• Undulatory motion gets more prominent at higher hydration• Square-law breaking
near the head group is due to penetration of water into the lipid
Hydration Mediated Ultra-slow Dynamics in Lipid Membranes
H2O
K.J. Mallikarjunaiah et al. (2011) Biophys. J. 100, 98A. Leftin, T.R. Molugu (2014) Biophys. J. 107, 2274
50302010
R2 / s−1
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Outline of the Talk
J.J. Kinnun et al. (2015) BBA 1848, 246K.J. Mallikarjunaiah et al. (2011) Biophys. J. 100, 98
• Introduction to solid-state 2H NMR experiments
• Model-free interpretation of lipid relaxation data
• Collective lipid dynamics
• Hydration-induced slow dynamics
• Conclusions
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• Liquid-crystalline phospholipids showed temperature independent elastic property.
• Chain length of disaturated phospholipid membranes weakly affected elasticity.
• Phosphoethanolamine membranes were stiffer than phosphocholine membranes, should be a consequence of the molecular packing.
• Membrane hydration showed a significant effect on elastic properties.
• High values for transverse relaxation rates indicated ultra-slow collective dynamics.
• Square-law breaking at high hydration should be the consequence of excess water penetrating into bilayer core.
• Membrane dehydration, addition of cholesterol, osmolytes, consistently showed stiffening effect on membranes
• Square-law connected the microscopic segmental dynamics to the macroscopic membrane properties.
Biophysical Conclusions
X. Xu et al. (2014) eMagRes 3, 275J.J. Kinnun et al. (2015) BBA 1848, 246
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Andrey Struts
Acknowledgements
Xiaolin Xu
Rami Musharrafieh
Udeep Chawla
Soohyun Lee
Suchi Perera
Michael Brown Michael PitmanVikram Molugu
THANK YOU ALL!Amanda Johnson