Overhauser Dynamic Nuclear Polarization for the Study of Hydration Dynamics, Explained

John Franck, Songi Han

Research output: Chapter in Book/Report/Conference proceedingChapter

1 Citation (Scopus)

Abstract

We outline the physical properties of hydration water that are captured by Overhauser Dynamic Nuclear Polarization (ODNP) relaxometry and explore the insights that ODNP yields about the water and the surface that this water is coupled to. As ODNP relies on the pairwise cross-relaxation between the electron spin of a spin probe and a proton nuclear spin of water, it captures the dynamics of single-particle diffusion of an ensemble of water molecules moving near the spin probe. ODNP principally utilizes the same physics as other nuclear magnetic resonance (NMR) relaxometry (i.e., relaxation measurement) techniques. However, in ODNP, electron paramagnetic resonance (EPR) excites the electron spins probes and their high net polarization acts as a signal amplifier. Furthermore, it renders ODNP parameters highly sensitive to water moving at rates commensurate with the EPR frequency of the spin probe (typically 10 GHz). Also, ODNP selectively enhances the NMR signal contributions of water moving within close proximity to the spin label. As a result, ODNP can capture ps–ns movements of hydration waters with high sensitivity and locality, even in samples with protein concentrations as dilute as 10 µM. To date, the utility of the ODNP technique has been demonstrated for two major applications: the characterization of the spatial variation in the properties of the hydration layer of proteins or other surfaces displaying topological diversity, and the identification of structural properties emerging from highly disordered proteins and protein domains. The former has been shown to correlate well with the properties of hydration water predicted by MD simulations and has been shown capable of evaluating the hydrophilicity or hydrophobicity of a surface. The latter has been demonstrated for studies of an interhelical loop of proteorhodopsin, the partial structure of α-synuclein embedded at the lipid membrane surface, incipient structures adopted by tau proteins en route to fibrils, and the structure and hydration profile of a transmembrane peptide. This chapter focuses on offering a mechanistic understanding of the ODNP measurement and the molecular dynamics encoded in the ODNP parameters. In particular, it clarifies how the electron–nuclear dipolar coupling encodes information about the molecular dynamics in the nuclear spin self-relaxation and, more importantly, the electron–nuclear spin cross-relaxation rates. The clarification of the molecular dynamics underlying ODNP should assist in establishing a connection to theory and computer simulation that will offer far richer interpretations of ODNP results in future studies.

Original languageEnglish (US)
Title of host publicationMethods in Enzymology
EditorsA. Joshua Wand
PublisherAcademic Press Inc.
Pages131-175
Number of pages45
ISBN (Print)9780128167625
DOIs
StatePublished - Jan 1 2019

Publication series

NameMethods in Enzymology
Volume615
ISSN (Print)0076-6879
ISSN (Electronic)1557-7988

Fingerprint

Hydration
Polarization
Water
Molecular Dynamics Simulation
Electron Spin Resonance Spectroscopy
Hydrophobic and Hydrophilic Interactions
Magnetic Resonance Spectroscopy
Synucleins
Molecular dynamics
Electrons
Relaxation Therapy
Water Movements
Spin Labels
tau Proteins
Proteins
Physics
Membrane Lipids
Paramagnetic resonance
Computer Simulation
Protons

Keywords

  • Biological water
  • Cross-relaxation
  • DNP
  • Dynamic heterogeneity
  • EPR
  • ESR
  • Hydration layer
  • Hydration water
  • ODNP
  • Relaxometry
  • Solvation dynamics
  • Solvation thermodynamics

ASJC Scopus subject areas

  • Biochemistry
  • Molecular Biology

Cite this

Franck, J., & Han, S. (2019). Overhauser Dynamic Nuclear Polarization for the Study of Hydration Dynamics, Explained. In A. J. Wand (Ed.), Methods in Enzymology (pp. 131-175). (Methods in Enzymology; Vol. 615). Academic Press Inc.. https://doi.org/10.1016/bs.mie.2018.09.024

Overhauser Dynamic Nuclear Polarization for the Study of Hydration Dynamics, Explained. / Franck, John; Han, Songi.

Methods in Enzymology. ed. / A. Joshua Wand. Academic Press Inc., 2019. p. 131-175 (Methods in Enzymology; Vol. 615).

Research output: Chapter in Book/Report/Conference proceedingChapter

Franck, J & Han, S 2019, Overhauser Dynamic Nuclear Polarization for the Study of Hydration Dynamics, Explained. in AJ Wand (ed.), Methods in Enzymology. Methods in Enzymology, vol. 615, Academic Press Inc., pp. 131-175. https://doi.org/10.1016/bs.mie.2018.09.024
Franck J, Han S. Overhauser Dynamic Nuclear Polarization for the Study of Hydration Dynamics, Explained. In Wand AJ, editor, Methods in Enzymology. Academic Press Inc. 2019. p. 131-175. (Methods in Enzymology). https://doi.org/10.1016/bs.mie.2018.09.024
Franck, John ; Han, Songi. / Overhauser Dynamic Nuclear Polarization for the Study of Hydration Dynamics, Explained. Methods in Enzymology. editor / A. Joshua Wand. Academic Press Inc., 2019. pp. 131-175 (Methods in Enzymology).
@inbook{aa5ec342edc043e28488a8561a0f3473,
title = "Overhauser Dynamic Nuclear Polarization for the Study of Hydration Dynamics, Explained",
abstract = "We outline the physical properties of hydration water that are captured by Overhauser Dynamic Nuclear Polarization (ODNP) relaxometry and explore the insights that ODNP yields about the water and the surface that this water is coupled to. As ODNP relies on the pairwise cross-relaxation between the electron spin of a spin probe and a proton nuclear spin of water, it captures the dynamics of single-particle diffusion of an ensemble of water molecules moving near the spin probe. ODNP principally utilizes the same physics as other nuclear magnetic resonance (NMR) relaxometry (i.e., relaxation measurement) techniques. However, in ODNP, electron paramagnetic resonance (EPR) excites the electron spins probes and their high net polarization acts as a signal amplifier. Furthermore, it renders ODNP parameters highly sensitive to water moving at rates commensurate with the EPR frequency of the spin probe (typically 10 GHz). Also, ODNP selectively enhances the NMR signal contributions of water moving within close proximity to the spin label. As a result, ODNP can capture ps–ns movements of hydration waters with high sensitivity and locality, even in samples with protein concentrations as dilute as 10 µM. To date, the utility of the ODNP technique has been demonstrated for two major applications: the characterization of the spatial variation in the properties of the hydration layer of proteins or other surfaces displaying topological diversity, and the identification of structural properties emerging from highly disordered proteins and protein domains. The former has been shown to correlate well with the properties of hydration water predicted by MD simulations and has been shown capable of evaluating the hydrophilicity or hydrophobicity of a surface. The latter has been demonstrated for studies of an interhelical loop of proteorhodopsin, the partial structure of α-synuclein embedded at the lipid membrane surface, incipient structures adopted by tau proteins en route to fibrils, and the structure and hydration profile of a transmembrane peptide. This chapter focuses on offering a mechanistic understanding of the ODNP measurement and the molecular dynamics encoded in the ODNP parameters. In particular, it clarifies how the electron–nuclear dipolar coupling encodes information about the molecular dynamics in the nuclear spin self-relaxation and, more importantly, the electron–nuclear spin cross-relaxation rates. The clarification of the molecular dynamics underlying ODNP should assist in establishing a connection to theory and computer simulation that will offer far richer interpretations of ODNP results in future studies.",
keywords = "Biological water, Cross-relaxation, DNP, Dynamic heterogeneity, EPR, ESR, Hydration layer, Hydration water, ODNP, Relaxometry, Solvation dynamics, Solvation thermodynamics",
author = "John Franck and Songi Han",
year = "2019",
month = "1",
day = "1",
doi = "10.1016/bs.mie.2018.09.024",
language = "English (US)",
isbn = "9780128167625",
series = "Methods in Enzymology",
publisher = "Academic Press Inc.",
pages = "131--175",
editor = "Wand, {A. Joshua}",
booktitle = "Methods in Enzymology",
address = "United States",

}

TY - CHAP

T1 - Overhauser Dynamic Nuclear Polarization for the Study of Hydration Dynamics, Explained

AU - Franck, John

AU - Han, Songi

PY - 2019/1/1

Y1 - 2019/1/1

N2 - We outline the physical properties of hydration water that are captured by Overhauser Dynamic Nuclear Polarization (ODNP) relaxometry and explore the insights that ODNP yields about the water and the surface that this water is coupled to. As ODNP relies on the pairwise cross-relaxation between the electron spin of a spin probe and a proton nuclear spin of water, it captures the dynamics of single-particle diffusion of an ensemble of water molecules moving near the spin probe. ODNP principally utilizes the same physics as other nuclear magnetic resonance (NMR) relaxometry (i.e., relaxation measurement) techniques. However, in ODNP, electron paramagnetic resonance (EPR) excites the electron spins probes and their high net polarization acts as a signal amplifier. Furthermore, it renders ODNP parameters highly sensitive to water moving at rates commensurate with the EPR frequency of the spin probe (typically 10 GHz). Also, ODNP selectively enhances the NMR signal contributions of water moving within close proximity to the spin label. As a result, ODNP can capture ps–ns movements of hydration waters with high sensitivity and locality, even in samples with protein concentrations as dilute as 10 µM. To date, the utility of the ODNP technique has been demonstrated for two major applications: the characterization of the spatial variation in the properties of the hydration layer of proteins or other surfaces displaying topological diversity, and the identification of structural properties emerging from highly disordered proteins and protein domains. The former has been shown to correlate well with the properties of hydration water predicted by MD simulations and has been shown capable of evaluating the hydrophilicity or hydrophobicity of a surface. The latter has been demonstrated for studies of an interhelical loop of proteorhodopsin, the partial structure of α-synuclein embedded at the lipid membrane surface, incipient structures adopted by tau proteins en route to fibrils, and the structure and hydration profile of a transmembrane peptide. This chapter focuses on offering a mechanistic understanding of the ODNP measurement and the molecular dynamics encoded in the ODNP parameters. In particular, it clarifies how the electron–nuclear dipolar coupling encodes information about the molecular dynamics in the nuclear spin self-relaxation and, more importantly, the electron–nuclear spin cross-relaxation rates. The clarification of the molecular dynamics underlying ODNP should assist in establishing a connection to theory and computer simulation that will offer far richer interpretations of ODNP results in future studies.

AB - We outline the physical properties of hydration water that are captured by Overhauser Dynamic Nuclear Polarization (ODNP) relaxometry and explore the insights that ODNP yields about the water and the surface that this water is coupled to. As ODNP relies on the pairwise cross-relaxation between the electron spin of a spin probe and a proton nuclear spin of water, it captures the dynamics of single-particle diffusion of an ensemble of water molecules moving near the spin probe. ODNP principally utilizes the same physics as other nuclear magnetic resonance (NMR) relaxometry (i.e., relaxation measurement) techniques. However, in ODNP, electron paramagnetic resonance (EPR) excites the electron spins probes and their high net polarization acts as a signal amplifier. Furthermore, it renders ODNP parameters highly sensitive to water moving at rates commensurate with the EPR frequency of the spin probe (typically 10 GHz). Also, ODNP selectively enhances the NMR signal contributions of water moving within close proximity to the spin label. As a result, ODNP can capture ps–ns movements of hydration waters with high sensitivity and locality, even in samples with protein concentrations as dilute as 10 µM. To date, the utility of the ODNP technique has been demonstrated for two major applications: the characterization of the spatial variation in the properties of the hydration layer of proteins or other surfaces displaying topological diversity, and the identification of structural properties emerging from highly disordered proteins and protein domains. The former has been shown to correlate well with the properties of hydration water predicted by MD simulations and has been shown capable of evaluating the hydrophilicity or hydrophobicity of a surface. The latter has been demonstrated for studies of an interhelical loop of proteorhodopsin, the partial structure of α-synuclein embedded at the lipid membrane surface, incipient structures adopted by tau proteins en route to fibrils, and the structure and hydration profile of a transmembrane peptide. This chapter focuses on offering a mechanistic understanding of the ODNP measurement and the molecular dynamics encoded in the ODNP parameters. In particular, it clarifies how the electron–nuclear dipolar coupling encodes information about the molecular dynamics in the nuclear spin self-relaxation and, more importantly, the electron–nuclear spin cross-relaxation rates. The clarification of the molecular dynamics underlying ODNP should assist in establishing a connection to theory and computer simulation that will offer far richer interpretations of ODNP results in future studies.

KW - Biological water

KW - Cross-relaxation

KW - DNP

KW - Dynamic heterogeneity

KW - EPR

KW - ESR

KW - Hydration layer

KW - Hydration water

KW - ODNP

KW - Relaxometry

KW - Solvation dynamics

KW - Solvation thermodynamics

UR - http://www.scopus.com/inward/record.url?scp=85058050049&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85058050049&partnerID=8YFLogxK

U2 - 10.1016/bs.mie.2018.09.024

DO - 10.1016/bs.mie.2018.09.024

M3 - Chapter

SN - 9780128167625

T3 - Methods in Enzymology

SP - 131

EP - 175

BT - Methods in Enzymology

A2 - Wand, A. Joshua

PB - Academic Press Inc.

ER -