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Dynamics Of Geminate Rebinding Of NO With Cytochrome C In Aqueous Solution Using Femtosecond Vibrational Spectroscopy.

Jooyoung Kim, J. Park, T. Lee, Manho Lim
Published 2012 · Chemistry, Medicine

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Using femtosecond vibrational spectroscopy, we investigated the rebinding dynamics of NO to cytochrome c (Cytc) and a model heme, microperoxidase-8 (Mp), after photodeligation of CytcNO in D(2)O solution and MpNO in an 81% glycerol/water (v/v) mixture at room temperature. Whereas the stretching mode of the NO band in MpNO was described by a Gaussian centered at 1653 cm(-1) with a full width at half-maximum (fwhm) of 41 cm(-1), that in CytcNO revealed an asymmetric structured band that peaked at 1619 cm(-1) with an fwhm of about 27 cm(-1). The structured NO band in CytcNO was well described by the sum of three Gaussians, and its shape did not evolve with time but its amplitude decayed exponentially with a time constant of 7 ± 1 ps. The transient NO band in MpNO also decayed exponentially with a time constant of 8 ± 1 ps. Rebinding of NO to Cytc was slightly faster than that of NO to Mp and was almost complete by 30 ps, which was much faster than the rebinding of NO to myoglobin (Mb). When the deligated NO was constrained near the Fe atom either by a viscous solvent or by the protein matrix, it rebound to heme Fe much faster than CO, suggesting that NO has a higher propensity for binding to heme Fe and the high reactivity governed the rebinding kinetics. Moreover, the faster ligand rebinding in Cytc than in Mb suggests that Cytc does not have a primary docking site (PDS)-like structure found in Mb that suppresses rebinding by restraining ligand motion and the PDS can also hold the deligated NO in a manner that impedes NO rebinding; however, due to higher NO reactivity with heme Fe, the impediment is not as efficient as for CO.
This paper references
10.1073/pnas.0912938107
Picosecond primary structural transition of the heme is retarded after nitric oxide binding to heme proteins
S. Kruglik (2010)
10.1016/S0020-1693(00)91476-2
The pH dependence of the stereochemistry around the heme group in NO–cytochrome c (horse heart)
Tetsushiko Yoshimura (1988)
10.1021/BI962744O
Identification of conformational substates involved in nitric oxide binding to ferric and ferrous myoglobin through difference Fourier transform infrared spectroscopy (FTIR).
L. Miller (1997)
10.1021/BI0497291
Proximal and distal influences on ligand binding kinetics in microperoxidase and heme model compounds.
W. Cao (2004)
10.1021/jp802246h
Native and unfolded cytochrome c--comparison of dynamics using 2D-IR vibrational echo spectroscopy.
S. Kim (2008)
10.1073/PNAS.77.10.5606
Geminate recombination of O2 and hemoglobin.
D. A. Chernoff (1980)
10.1021/JP0489020
Dynamics of Geminate Recombination of NO with Myoglobin in Aqueous Solution Probed by Femtosecond Mid-IR Spectroscopy
S. Kim (2004)
10.5012/BKCS.2009.30.1.177
Dynamics of CO Rebinding to Protoheme in Viscous Solutions
T. Lee (2009)
10.1021/BI0102252
Main chain and side chain dynamics of a heme protein: 15N and 2H NMR relaxation studies of R. capsulatus ferrocytochrome c2.
P. Flynn (2001)
10.1021/BI010715U
Protein conformational relaxation and ligand migration in myoglobin: a nanosecond to millisecond molecular movie from time-resolved Laue X-ray diffraction.
V. Šrajer (2001)
10.1073/PNAS.90.12.5805
Nonexponential relaxation after ligand dissociation from myoglobin: a molecular dynamics simulation.
K. Kuczera (1993)
10.1073/PNAS.90.10.4718
Perturbations of the distal heme pocket in human myoglobin mutants probed by infrared spectroscopy of bound CO: correlation with ligand binding kinetics.
S. Balasubramanian (1993)
10.1073/PNAS.90.12.5801
Nonexponential protein relaxation: dynamics of conformational change in myoglobin.
M. Lim (1993)
10.1021/JA017359N
Measurements of the photodissociation quantum yields of MbNO and MbO(2) and the vibrational relaxation of the six-coordinate heme species.
X. Ye (2002)
10.1016/0301-4622(87)80034-0
Rebinding and relaxation in the myoglobin pocket.
A. Ansari (1987)
10.1016/S0022-2836(83)80094-1
Geminate recombination of carbon monoxide to myoglobin.
E. R. Henry (1983)
10.1364/OL.25.001798
Noise suppression in femtosecond mid-infrared light sources.
P. Hamm (2000)
10.1021/jp106588d
Protein folding dynamics of cytochrome c seen by transient grating and transient absorption spectroscopies.
Jungkweon Choi (2011)
10.1111/PHP.1990.51.6.741
Transient and time-resolved optical studies of photolyzed carbonmonoxy hemoglobin and myoglobin.
Findsen Ew (1990)
10.1016/J.BBABIO.2007.10.004
Ultrafast dynamics of ligands within heme proteins.
M. Vos (2008)
10.1021/jp3026495
Direct observation of ligand rebinding pathways in hemoglobin using femtosecond mid-IR spectroscopy.
S. Kim (2012)
10.1021/JA00074A023
Photochemistry of nitric oxide adducts of water-soluble iron(III) porphyrin and ferrihemoproteins studied by nanosecond laser photolysis
M. Hoshino (1993)
10.1021/BI011440L
FTIR and resonance Raman studies of nitric oxide binding to H93G cavity mutants of myoglobin.
M. R. Thomas (2001)
10.1021/BI983022V
Heme protein dynamics revealed by geminate nitric oxide recombination in mutants of iron and cobalt myoglobin.
Y. Kholodenko (1999)
10.1016/S0969-2126(96)00121-9
Fast events in protein folding.
W. Eaton (1996)
10.1021/BI701935V
Structural dynamics of myoglobin: FTIR-TDS study of NO migration and binding.
K. Nienhaus (2008)
10.1021/JA054249Y
Temperature-dependent studies of NO recombination to heme and heme proteins.
D. Ionașcu (2005)
10.1016/0022-2836(90)90197-T
High-resolution refinement of yeast iso-1-cytochrome c and comparisons with other eukaryotic cytochromes c.
G. Louie (1990)
10.1021/JP9813286
STRUCTURE OF THE AMIDE I BAND OF PEPTIDES MEASURED BY FEMTOSECOND NONLINEAR-INFRARED SPECTROSCOPY
P. Hamm (1998)
10.1021/jp300849y
Absorption band III kinetics probe the picosecond heme iron motion triggered by nitric oxide binding to hemoglobin and myoglobin.
Byung-Kuk Yoo (2012)
10.1021/jp300176q
Protein conformation-controlled rebinding barrier of NO and its binding trajectories in myoglobin and hemoglobin at room temperature.
S. Kim (2012)
10.1073/PNAS.75.5.2108
Kinetics of hemoglobin and transition state theory.
A. Szabó (1978)
10.5012/BKCS.2003.24.10.1470
Structural dynamics of myoglobin probed by femtosecond infrared spectroscopy of the amide band
S. Kim (2003)
10.1021/JP991163G
Dependence of NO Recombination Dynamics in Horse Myoglobin on Solution Glycerol Content
A. P. Shreve (1999)
10.1021/BI00230A025
Ligand binding and protein relaxation in heme proteins: a room temperature analysis of nitric oxide geminate recombination
J. Petrich (1991)
10.1021/BI00174A029
Geminate recombination of diatomic ligands CO, O2, and NO with myoglobin.
K. N. Walda (1994)
10.1016/s0021-9258(18)41630-4
Distal pocket residues affect picosecond ligand recombination in myoglobin. An experimental and molecular dynamics study of position 29 mutants.
Q. Gibson (1992)
10.1021/BI00695A021
Dynamics of ligand binding to myoglobin.
R. Austin (1975)
10.1021/JA057172M
Dynamics of nitric oxide rebinding and escape in horseradish peroxidase.
X. Ye (2006)
10.1038/NSB0397-209
Ultrafast rotation and trapping of carbon monoxide dissociated from myoglobin
Manho Lim (1997)
10.1016/0162-0134(94)85114-X
Nitric oxide binding to ferrous native horse heart cytochrome c and to its carboxymethylated derivative: a spectroscopic and thermodynamic study.
P. Ascenzi (1994)
10.1021/jp804656t
Dynamics of ultrafast rebinding of CO to carboxymethyl cytochrome c.
Jooyoung Kim (2009)
10.1021/JA00996A034
Model systems for interacting heme moieties. II. The ferriheme octapeptide of cytochrome c.
D. Urry (1967)
10.1006/ABIO.1997.2136
Water (H2O and D2O) molar absorptivity in the 1000-4000 cm-1 range and quantitative infrared spectroscopy of aqueous solutions.
Venyaminov SYu (1997)
10.1021/JA953311W
Studies on the Reaction Mechanism for Reductive Nitrosylation of Ferrihemoproteins in Buffer Solutions
M. Hoshino (1996)
10.1021/JP952483C
Picosecond Structural Dynamics of Myoglobin following Photolysis of Carbon Monoxide
Timothy P. Causgrove and (1996)
10.1038/371808A0
Crystal structure of photolysed carbonmonoxy-myoglobin
I. Schlichting (1994)
10.1021/JA00210A011
Picosecond and nanosecond geminate recombination of myoglobin with carbon monoxide, oxygen, nitric oxide and isocyanides
K. Jongeward (1988)
10.1016/0009-2614(86)80149-X
CO cage recombination in hemoglobin: Picosecond photolysis and nanosecond observation
S. Pin (1986)
10.1073/pnas.0702622104
Temperature-dependent heme kinetics with nonexponential binding and barrier relaxation in the absence of protein conformational substates
X. Ye (2007)
10.1021/JA0502270
Protein conformation-induced modulation of ligand binding kinetics: a femtosecond mid-IR study of nitric oxide binding trajectories in myoglobin.
S. Kim (2005)
10.1126/SCIENCE.1078797
Watching a Protein as it Functions with 150-ps Time-Resolved X-ray Crystallography
F. Schotte (2003)
10.1016/S0009-2614(98)00533-8
Chirped wavepacket dynamics of HgBr from the photolysis of HgBr2 in solution
M. Lim (1998)
10.1021/BI00411A022
Photophysics and reactivity of heme proteins: a femtosecond absorption study of hemoglobin, myoglobin, and protoheme.
J. Petrich (1988)
10.1021/BI00126A001
Why nitric oxide
T. Traylor (1992)
10.1021/CR00027A007
Mechanisms of Ligand Recognition in Myoglobin
B. Springer (1994)
10.1046/J.1432-1033.2003.03358.X
Microperoxidase 8 catalysed nitrogen oxides formation from oxidation of N-hydroxyguanidines by hydrogen peroxide.
R. Ricoux (2003)
10.1021/BI00096A007
Protein response to photodissociation of CO from carbonmonoxymyoglobin probed by time-resolved infrared spectroscopy of the amide I band.
T. Causgrove (1993)
10.1038/NSB1094-701
Photolysis-induced structural changes in single crystals of carbonmonoxy myoglobin at 40 K
T. Teng (1994)
10.1039/B508183C
Geminate carbon monoxide rebinding to a c-type haem.
G. Silkstone (2005)
10.1021/jp1050436
Viscosity-dependent dynamics of CO rebinding to microperoxidase-8 in glycerol/water solution.
J. Park (2010)
10.1038/2061150a0
Production of a ‘Cytochrome c’ with Myoglobin-like Properties by Alkylating the Cyanide Complex with Bromoacetate
Abel Schejter (1965)
10.1016/0162-0134(86)80064-2
Hemes and hemoproteins. 1: Preparation and analysis of the heme-containing octapeptide (microperoxidase-8) and identification of the monomeric form in aqueous solution.
J. Aron (1986)
10.1073/PNAS.90.24.11860
Fast events in protein folding initiated by nanosecond laser photolysis.
C. Jones (1993)
10.1016/S0006-3495(99)76954-7
Connection between the taxonomic substates and protonation of histidines 64 and 97 in carbonmonoxy myoglobin.
J. Müller (1999)
10.1021/IC00059A010
Resonance Raman spectroscopic studies of the nitric oxide adducts of cobaltous-reconstituted myoglobin and hemoglobin
S. Hu (1993)
10.1021/CR000078Y
Nitric oxide and myoglobins.
J. K. Møller (2002)
10.1006/JMBI.1994.1302
Ultrafast measurements of geminate recombination of NO with site-specific mutants of human myoglobin.
J. Petrich (1994)
10.1002/cphc.200800280
Folding dynamics of ferrocytochrome C in a denaturant-free environment probed by transient grating spectroscopy.
Jungkweon Choi (2008)
10.1074/jbc.M605760200
Ligand Dynamics in an Electron Transfer Protein
G. Silkstone (2007)



This paper is referenced by
10.1002/anie.201604552
Structural Interpretation of Metastable States in Myoglobin-NO.
M. Soloviov (2016)
10.1063/1.4996448
Implications of short time scale dynamics on long time processes
Krystel El Hage (2017)
10.1080/08927022.2017.1416115
Free energy simulations for protein ligand binding and stability
Krystel El Hage (2018)
10.1111/febs.12526
Modulation of ligand–heme reactivity by binding pocket residues demonstrated in cytochrome c' over the femtosecond–second temporal range
Henry J. Russell (2013)
10.1002/wcms.1386
Reactive molecular dynamics: From small molecules to proteins
M. Meuwly (2019)
10.1021/jp509644m
Picosecond dynamics of photoexcited DNO-bound myoglobin probed by femtosecond vibrational spectroscopy.
T. Lee (2015)
10.1088/2632-2153/ab5922
High-Dimensional Potential Energy Surfaces for Molecular Simulations
Oliver T. Unke (2019)
10.1038/s41598-018-22944-z
Solvent Composition Drives the Rebinding Kinetics of Nitric Oxide to Microperoxidase
Padmabati Mondal (2018)
10.1021/jp407733g
Direct observation of the low-spin Fe(III)-NO(radical) intermediate state during rebinding of NO to photodeligated ferric cytochrome c.
J. Park (2013)
10.5012/BKCS.2014.35.3.758
Vibrational Relaxation of Cyanate or Thiocyanate Bound to Ferric Heme Proteins Studied by Femtosecond Infrared Spectroscopy
Seongchul Park (2014)
10.5075/EPFL-THESIS-6739
Ultrafast photoinduced processes in metal - containing molecular complexes and in proteins
Roberto Monni (2015)
10.1073/pnas.1424446112
NO binding kinetics in myoglobin investigated by picosecond Fe K-edge absorption spectroscopy
M. Silatani (2015)
10.1016/j.bbabio.2014.07.018
Time-resolved infrared spectroscopic studies of ligand dynamics in the active site from cytochrome c oxidase.
M. Vos (2015)
10.5451/UNIBAS-006727339
Atomistic simulations of the reactive processes in the heme-containing proteins
M. Soloviov (2015)
10.1002/ANGE.201604552
Strukturelle Interpretation metastabiler Zustände in Myoglobin-NO
M. Soloviov (2016)
10.1039/c7cp02634j
Structural changes and picosecond to second dynamics of cytochrome c in interaction with nitric oxide in ferrous and ferric redox states.
S. Kruglik (2017)
10.1038/s41467-020-17923-w
Femtosecond X-ray emission study of the spin cross-over dynamics in haem proteins
D. Kinschel (2020)
Infrared and UV-visible time-resolved techniques for the study of tetrapyrrole-based proteins
H. Russell (2013)
10.1039/c3pp50014d
Geminate rebinding dynamics of nitric oxide to ferric hemoglobin in D2O solution.
J. Park (2013)
10.1063/5.0009628
Non-conventional force fields for applications in spectroscopy and chemical reaction dynamics.
D. Koner (2020)
10.5075/EPFL-THESIS-9932
Ultrafast X-ray Spectroscopy of Heme Proteins
D. Kinschel (2020)
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