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National Biomedical Resource
for Advanced Electron Spin Resonance Spectroscopy

Our research is supported by grant 1R24GM146107 from the National Institute of General Medical Sciences (NIGMS), part of the National Institutes of Health.

  Key publications
Pulsed ESR Distance Measurements
Articles:

Dipolar Spectroscopy — Single–Resonance Methods
P. P. Borbat and J. H. Freed.
In EPR Spectroscopy: Fundamentals and Methods. D. Goldfarb, and S. Stoll, Eds. 139, 15530-15538 (2017)
Wiley & Sons: Chichester, UK.
<doi:10.1002/9780470034590.emrstm1519>
PMID: [None - Book]      PMCID: [None - Book]
 

Key features of an Hsp70 chaperone allosteric landscape revealed by ion–mobility native mass spectrometry and double electron–electron resonance
A. L. Lai, E. M. Clerico, M. E. Blackburn, N. A. Patel, C. V. Robinson, P. P. Borbat, J. H. Freed, and L. M. Gierasch.
J. Biol. Chem. 292, 8773-8785 (2017)
Supporting Information
<doi:10.1074/jbc.M116.770404>
PMID: 28428246      PMCID: PMC5448104
 

Stability and Conformation of a Chemoreceptor HAMP Domain Chimera Correlates with Signaling Properties
N. Sukomon, J. Widom, P. P. Borbat, J. H. Freed, and B. R. Crane.
Biophys. J. 112, 1383-1395 (2017)
Supporting Information
<doi:10.1016/j.bpj.2017.02.037>
PMID: 28402881      PMCID: PMC5390053
 

Signature of an aggregation-prone conformation of tau
N. A. Eschmann, E. R. Georgieva, P. Ganguly, P. P. Borbat, M. D. Rappaport, Y. Akdogan, J. H. Freed, J. -E. Shea, and S. Han.
Sci. Rep. 7, 44739 (2017)
Supporting Information
<doi:10.1038/srep44739>
PMID: 28303942      PMCID: PMC5356194
 

Bacterial Energy Sensor Aer Modulates the Activity of the Chemotaxis Kinase CheA Based on the Redox State of the Flavin Cofactor
D. Samanta, J. Widom, P. P. Borbat, J. H. Freed, and B. R. Crane.
J. Biol. Chem. 291, 25809-25814 (2016)
<doi:10.1074/jbc.C116.757492>
PMID: 27803157      PMCID: PMC5207056
 

Conformational Response of Influenza A M2 Transmembrane Domain to Amantadine Drug Binding at Low pH (pH 5.5)
E. R. Georgieva, P. P. Borbat, K. Grushin, S. Stoilova-McPhie, N. J. Kulkarni, Z. Liang, and J. H. Freed.
Front. Physiol. 7, 317 (2016)
Supporting Information
<doi:10.3389/fphys.2016.00317>
PMID: 27524969      PMCID: PMC4965473
 

Structural Basis for Activation, Assembly and Membrane Binding of ESCRT-III Snf7 Filaments
S. Tang, W. M. Henne, P. P. Borbat, N. J. Buchkovich, J. H. Freed, Y. Mao, J. C. Fromme, and S. D. Emr.
eLife 4 e12548 (2015)
Supporting Information
<doi:10.7554/eLife.12548>
PMID: 26670543      PMCID: PMC4720517
 

Pulsed Dipolar Spectroscopy Reveals that Tyrosyl Radicals Are Generated in Both Monomers of the Cyclooxygenase-2 Dimer
B. J. Orlando, P. P. Borbat, E. R. Georgieva, J. H. Freed, and M. G. Malkowski.
Biochemistry 54 7309-7312 (2015)
Supporting Information
<doi:10.1021/acs.biochem.5b00979>
PMID: 26636181      PMCID: PMC4707933
 

Signal Transduction in Light-Oxygen-Voltage Receptors Lacking the Adduct-Forming Cysteine Residue
E.F. Yee, R.P. Diensthuber, A.T. Vaidya, P.P. Borbat, C. Engelhard, J.H. Freed, R. Bittl, A. Möglich, and B.R. Crane.
Nature Comm. 6 10079 (2015)
<doi:10.1038/ncomms10079>
PMID: 26648256      PMCID: PMC4682037
 

Preformed Soluble Chemoreceptor Trimers That Mimic Cellular Assembly States and Activate CheA Autophosphorylation
A.R. Greenswag, X. Li, P.P. Borbat, D. Samanta, K.J. Watts, J.H. Freed, and B.R. Crane
Biochemistry 54, 3454-3468 (2015).
Supporting Information
<doi:10.1021/bi501570n>
PMID: 25967982      PMCID: PMC4772074
 

Mechanism of Influenza A M2 Transmembrane Domain Assembly in Lipid Membranes
E.R. Georgieva, P.P. Borbat, H.D. Norman, and J.H. Freed
Sci. Rep. 5, 11757 (2015).
Supporting Information
<doi:10.1038/srep11757>
PMID: 26190831      PMCID: PMC4507135
 

Assembly States of FliM and FliG Within the Flagellar Switch Complex
R. Sircar, P.P. Borbat, M.J. Lynch, J. Bhatnagar, M.S. Beyersdorf, C.J. Halkides, J.H. Freed and B.R. Crane.
J. Mol. Biol. 427, 867-886 (2015).
Supporting Information
<doi:10.1016/j.jmb.2014.12.009>
PMID: 25536293      PMCID: PMC4323944
 

Bacterial Chemoreceptor Dynamics Correlate With Activity State and Are Coupled Over Long Distances
D. Samanta, P.P. Borbat, B. Dzikovski, J.H. Freed, and B.R. Crane.
Proc. Natl. Acad. Sci. U. S. A. 112, 2455-2460 (2015).
Supporting Information
<doi:10.1073/pnas.1414155112>
PMID: 25675479      PMCID: PMC4345563
 

Pulse Dipolar ESR of Doubly Labeled Mini TAR DNA and Its Annealing to Mini TAR RNA
Y. Sun, P.P. Borbat, V.M. Grigoryants, W.K. Myers, J.H. Freed, and C.P. Scholes.
Biophys. J. 108, 893-902 (2015).
Supporting Information
<doi:10.1016/j.bpj.2014.12.028>
PMID: 25692594      PMCID: PMC4336369
 

Transport Domain Unlocking Sets the Uptake Rate of an Aspartate Transporter
N. Akyuz, E.R. Georgieva, Z. Zhou, S. Stolzenberg, M.A. Cuendet, G. Khelashvili, R.B. Altman, D.S. Terry, J.H. Freed, H. Weinstein, O. Boudker, and S.C. Blanchard.
Nature 518, 68-73 (2015).
<doi:10.1038/nature14158>
PMID: 25652997      PMCID: PMC4351760
 

Tau Binds to Lipid Membrane Surfaces via Short Amphipathic Helices Located in Its Microtubule-Binding Repeats
E.R. Georgieva, S. Xiao, P.P. Borbat, J.H. Freed, and D. Eliezer.
Biophys. J. 107, 1441-1452 (2014).
Supporting Information
<doi:10.1016/j.bpj.2014.07.046>
PMID: 25229151      PMCID: PMC4167292
 

Copper-Based Pulsed Dipolar ESR Spectroscopy as a Probe of Protein Conformation Linked to Disease States
G.E. Merz, P.P. Borbat, A.J. Pratt, E.D. Getzoff, J.H. Freed, and B.R. Crane.
Biophys. J. 107, 1669-1674 (2014).
Supporting Information
<doi:10.1016/j.bpj.2014.07.068>
PMID: 25296320      PMCID: PMC4190658
 

Aggregation Propensities of Superoxide Dismutase G93 Hotspot Mutants Mirror ALS Clinical Phenotypes
A.J. Pratt, D.S. Shin, G.E. Merz, R.P. Rambo, W.A. Lancaster, K.N. Dyer, P.P. Borbat, F.L. Poole II, M.W.W. Adams, J.H. Freed, B.R. Crane, J.A. Tainer, and E.D. Getzoff.
Proc. Natl. Acad. Sci. U. S. A. 111, E4568-E4576 (2014).
<doi:10.1073/pnas.1308531111>
PMID: 25316790      PMCID: PMC4217430
 

Pulse Dipolar Electron Spin Resonance: Distance Measurements
P.P. Borbat and J.H. Freed.
In Structural Information from Spin-Labels and Intrinsic Paramagnetic Centers in the Biosciences. Structure and Bonding. Vol. 152. J. Harmer and C. Timmel, Eds.
Springer: Heidelberg, Germany; New York, USA, 2013; pp. 1-82.
<doi:10.1007/430_2012_82>
PMID: [None - Book]      PMCID: [None - Book]
 

Architecture of the Soluble Receptor Aer2 Indicates an In-Line Mechanism for PAS and HAMP Domain Signaling
M.V. Airola, D. Huh, N. Sukomon, J. Widom, R. Sircar, P.P. Borbat, J.H. Freed, K.J. Watts, and B.R. Crane.
J. Mol. Biol. 425, 886-901 (2013).
Supporting Information
<doi:10.1016/j.jmb.2012.12.011>
PMID: 23274111      PMCID: PMC3577987
 

HAMP Domain Conformers that Propagate Opposite Signals in Bacterial Chemoreceptors
M.V. Airola, N. Sukomon, D. Samanta, P.P. Borbat, J.H. Freed, K.J. Watts, and B.R. Crane.
PLoS Biol. 11, e1001479, (2013).
Supporting Information
<doi:10.1371/journal.pbio.1001479>
PMID: 23424282      PMCID: PMC3570549
 

Improved Sensitivity for Long-Distance Measurements in Biomolecules: Five-Pulse Double Electron-Electron Resonance
P.P. Borbat, E.R. Georgieva, and J.H. Freed.
J. Phys. Chem. Lett. 4, 170-175 (2013).
Supporting Information
<doi:10.1021/jz301788n>
PMID: 23301118      PMCID: PMC3538160
 

Conformational Ensemble of the Sodium-Coupled Aspartate Transporter
E.R. Georgieva, P.P. Borbat, C. Ginter, J.H. Freed, and O. Boudker.
Nat. Struct. Mol. Biol. 20, 215-221 (2013).
Supporting Information
<doi:10.1038/nsmb.2494>
PMID: 23334289      PMCID: PMC3565060
 

Locating a Lipid at the Portal to the Lipoxygenase Active Site
B.J. Gaffney, M. Bradshaw, S. Frausto, F. Wu, J.H. Freed, and P.P. Borbat.
Biophysical J. 103, 2134-2144, (2012).
Supporting Information
<doi:10.1016/j.bpj.2012.10.002>
PMID: 23200047      PMCID: PMC3512035
 

Pulsed ESR Dipolar Spectroscopy for Distance Measurements in Immobilized Spin Labeled Proteins in Liquid Solution
Z. Yang, Y. Liu, P.P. Borbat, J.L. Zweier, J.H. Freed, and W.L. Hubbell.
J. Am. Chem. Soc. 134, 9950-9952 (2012).
Supporting Information
<doi:10.1021/ja303791p>
PMID: 22676043      PMCID: PMC3409244
 

Self-Association of the Histidine Kinase CheA as Studied by Pulsed Dipolar ESR Spectroscopy
J. Bhatnagar, R. Sircar, P.P. Borbat, J.H. Freed, and B.R. Crane.
Biophys. J. 102, 2192-2201 (2012).
Supporting Information
<doi:10.1016/j.bpj.2012.03.038>
PMID: 22824284      PMCID: PMC3341552
 

Effect of Freezing Conditions on Distances and Their Distributions Derived From Double Electron Electron Resonance (DEER): A Study of Doubly-Spin-Labeled T4 Lysozyme
E.R. Georgieva, A.S. Roy, V.M. Grigoryants, P.P. Borbat, K.A. Earle, C.P. Scholes, and J.H. Freed.
J. Magn. Reson. 216, 69-77 (2012).
Supporting Information
<doi:10.1016/j.jmr.2012.01.004>
PMID: 22341208      PMCID: PMC3323113
 

Distance Measurements: Continuous-Wave (CW)- and Pulsed Dipolar EPR
S.K. Misra and J.H. Freed.
In Multifrequency Electron Paramagnetic Resonance, S.K. Misra, Ed.
Wiley-VCH: New York, 2011; Chapter 12, pp. 545-588.
PMID: [None - Book]      PMCID: [None - Book]
 

Channel and Nonchannel Forms of Spin-Labeled Gramicidin in Membranes and Their Equilibria
B.G. Dzikovski, P.P. Borbat, and J.H. Freed.
J. Phys. Chem. B 115, 176-185 (2011).
Supporting Information
<doi:10.1021/jp108105k>
PMID: 21142163      PMCID: PMC3076037
 

The Lipid-Binding Domain of Wild Type and Mutant α-Synuclein: Compactness and Interconversion Between the Broken and Extended Helix Forms
E.R. Georgieva, T.F. Ramlall, P.P. Borbat, J.H. Freed, and D. Eliezer.
J. Biol. Chem. 285, 28261-28274 (2010).
Supporting Information
<doi:10.1074/jbc.M110.157214>
PMID: 20592036      PMCID: PMC2934691
 

Structure of the Ternary Complex Formed by a Chemotaxis Receptor Signaling Domain, the CheA Histidine Kinase, and the Coupling Protein CheW As Determined by Pulsed Dipolar ESR Spectroscopy
J. Bhatnagar, P.P. Borbat, A.M. Pollard, A.M. Bilwes, J.H. Freed, and B.R. Crane.
Biochemistry, 49, 3824-3841 (2010).
Supporting Information
<doi:10.1021/bi100055m>
PMID: 20355710      PMCID: PMC2873776
 

Molecular-Scale Force Measurement in a Coiled-Coil Peptide Dimer by Electron Spin Resonance
S.V. Gullà, G. Sharma, P.Borbat, J.H. Freed, H. Ghimire, M.R. Benedikt, N.L. Holt, G.A. Lorigan, K. Rege, C. Mavroidis, and D.E. Budil.
J. Am. Chem. Soc. 131, 5374-5375 (2009).
Supporting Information
<doi:10.1021/ja900230w>
PMID: 19331323      PMCID: PMC2888838
 

Calculation of Double-Quantum-Coherence Two-dimensional Spectra: Distance Measurements and Orientational Correlations
S.K. Misra, P.P. Borbat, J.H. Freed.
Appl. Magn. Reson. 36, 237-258 (2009).
<doi:10.1007/s00723-009-0023-5>
PMID: 20161423      PMCID: PMC2786184
 

A Scissors Mechanism for Stimulation of SNARE-Mediated Lipid Mixing by Cholesterol
J. Tong, P.P. Borbat, J.H. Freed, and Y.-K. Shin.
PNAS 106, 5141-5146 (2009).
<doi:10.1073/pnas.0813138106>
PMID: 19251653      PMCID: PMC2663986
 

Membrane-Bound α-Synuclein Forms an Extended Helix: Long-Distance Pulsed ESR Measurements Using Vesicles, Bicelles, and Rodlike Micelles
E.R. Georgieva, T.F. Ramlall, P.P. Borbat, J.H. Freed, and D. Eliezer.
J. Am. Chem. Soc. 130, 12856-12857 (2008).
Supporting Information
<doi:10.1021/ja804517m>
PMID: 18774805      PMCID: PMC2626176
 

Determination of the Oligomeric States of Human and Rat Monoamine Oxidases in the Outer Mitochondrial Membrane and Octyl β-D-Glucopyranoside Micelles Using Pulsed Dipolar Electron Spin Resonance Spectroscopy
A.K. Upadhyay, P.P. Borbat, J. Wang, J.H. Freed, and D.E. Edmondson.
Biochemistry 47, 1554-1566 (2008).
<doi:10.1021/bi7021377>
PMID: 18198902      PMCID: [accepted before 04/08]
 

Pros and Cons of Pulse Dipolar ESR: DQC and DEER
P.P. Borbat and J.H. Freed.
EPR Newletter 17, 21-33 (2007).
 

Conformational Motion of the ABC Transporter MsbA Induced by ATP Hydrolysis
P.P. Borbat, K. Surendhran, M. Bortolus, P. Zou, J.H. Freed, H.S. Mchaourab.
PLoS Biology 5, 2211-2219 (2007).
Supporting Information
<doi:10.1371/journal.pbio.0050271>
PMID: 17927448      PMCID: PMC2001213
 

Rigid Body Refinement of Protein Complexes with Long-Range Distance Restraints from Pulsed Dipolar ESR
J. Bhatnagar, J.H. Freed, and B.R. Crane.
In Two-Component Signaling Systems, Part B, M. Simon, B.R. Crane and A.B. Crane, Eds.
Methods in Enzymology 423, Ch. 4, pp. 117-133 (2007).
<doi:10.1016/S0076-6879(07)23004-6>
PMID: 17609128     
 

Measuring Distances by Pulsed Dipolar ESR Spectroscopy: Spin-Labeled Histidine Kinases
P.P. Borbat and J.H. Freed.
In Two-Component Signaling Systems, Part B, M. Simon, B.R. Crane and A.B. Crane, Eds.
Methods in Enzymology 423, Ch. 3, pp. 52-116 (2007).
<doi:10.1016/S0076-6879(07)23003-4>
PMID: 17609127     
 

Characterizing the Structure and Dynamics of Folded Oligomers: Pulsed ESR Studies of Peptoid Helices
A.T. Fafarman, P.P. Borbat, J.H. Freed and K. Kirshenbaum.
Chem. Comm., 377-379 (2007).
<doi:10.1039/b612198e>
PMID: 17220976     
 

Inter-Helix Distances in Lysophospholipid Micelle-Bound α-Synuclein from Pulsed ESR Measurements
P. Borbat, T.F. Ramlall, J.H. Freed, and D. Eliezer.
J. Am. Chem. Soc. 128, 10004-05 (2006).
Supporting Information
<doi:10.1021/ja063122l>
PMID: 16881616     
 

Two-Pulse Electron Spin Echo Study of Deuterium-Helium Solids
E.P. Bernard, V.V. Khmelenko, E. Vehmanen, P.P. Borbat, J.H. Freed, and D.M. Lee.
Proc. 24th Intl. Conf. on Low Temp. Physics, 372-373 (2006).
 

Pulse Electron Spin Resonance Method for Investigation of Atoms in Impurity-Helium Solids
E.P. Bernard, V.V. Khmelenko, E. Vehmanen, P.P. Borbat, J.H. Freed, and D.M. Lee.
Proc. 24th Intl. Conf. on Low Temp. Physics, 1659-1660 (2006).
 

Reconstruction of the Chemotaxis Receptor-Kinase Assembly
S.-Y. Park, P.P. Borbat, G. Gonzalez-Bonet, J. Bhatnagar, A.M. Pollard, J.H. Freed, A.M. Bilwes & B.R. Crane.
Nat. Struct. Molec. Biol. 13, 400-407 (2006).
Supporting Information
<doi:10.1038/nsmb1085>
PMID: 16622408     
 

EPR Distance Measurements Support a Model for Long-Range Radical Initiation in E. coli Ribonucleotide Reductase
M. Bennati, J.H. Robblee, V. Mugnaini, J. Stubbe, J.H. Freed, and P. Borbat.
J. Am. Chem. Soc. 127, 15014-15015 (2005).
<doi:10.1021/ja054991y>
PMID: 16248626     
 

Effects of Finite Pulse Width on Two-Dimensional Fourier Transform Electron Spin Resonance
Z. Liang, R.H. Crepeau, J.H. Freed.
J. Magn. Reson. 177, 247-260 (2005).
<doi:10.1016/j.jmr.2005.07.024>
PMID: 16150620     
 

The Determination of Pair Distance Distributions by Pulsed ESR Using Tikhonov Regularization
Y.-W. Chiang, P.P. Borbat, J.H. Freed.
J. Magn. Reson. 172, 279-295 (2005).
<doi:10.1016/j.jmr.2004.10.012>
PMID: 15649755     
 

Spin-Labeled Gramicidin A: Channel Formation and Dissociation
B.G. Dzikovski, P.P. Borbat, and J.H. Freed.
Biophys. J. 87, 3504-3517 (2004).
<doi:10.1529/biophysj.104.044305>
PMID: 15326023      PMCID: PMC1304816
 

Measurement of Large Distances in Biomolecules Using Double-Quantum Filtered Refocused Electron Spin-Echoes
P.P. Borbat, J.H. Davis, S.E. Butcher, and J.H. Freed.
J. Am. Chem. Soc. 126, 7746-7747 (2004).
<doi:10.1021/ja049372o>
PMID: 15212500     
 

Protein Structure Determination Using Long-Distance Constraints from Double-Quantum Coherence ESR: Study of T4 Lysozyme
P.P. Borbat, H.S. Mchaourab, and J.H. Freed.
J. Am. Chem. Soc. 124, 5304-5314 (2002).
<doi:10.1021/ja020040y>
PMID: 11996571     
 

Electron Spin Resonance in Studies of Membranes and Proteins
P.P. Borbat, A.J. Costa-Filho, K.A. Earle, J.K. Moscicki, J.H. Freed.
Science 291, 266-269, (2001).
<doi:10.1126/science.291.5502.266>
PMID: 11253218     
 

Double Quantum ESR and Distance Measurements
P.P. Borbat and J.H. Freed.
In Distance Measurements in Biological Systems by EPR, L.J. Berliner, S.S. Eaton, and G.R, Eaton, Eds.
Biological Magnetic Resonance 19, Chapter 9, pp. 383-459 (2000). (Kluwer, NY).
 

Multiple-Quantum ESR and Distance Measurements
P.P. Borbat and J.H. Freed.
Chem. Phys. Lett. 313, 145-154 (1999).
<doi:10.1016/S0009-2614(99)00972-0>