3D Motions of Iron in Six-Coordinate {FeNO}7 Hemes by Nuclear Resonance Vibration Spectroscopy [3-D Motions of Iron in Six-coordinate {FeNO}7 Hemes by NRVS
Abstract
Abstract The vibrational spectrum of a six‐coordinate nitrosyl iron porphyrinate, monoclinic [Fe(T p FPP)(1‐MeIm)(NO)] (T p FPP=tetra‐ para ‐fluorophenylporphyrin; 1‐MeIm=1‐methylimidazole), has been studied by oriented single‐crystal nuclear resonance vibrational spectroscopy (NRVS). The crystal was oriented to give spectra perpendicular to the porphyrin plane and two in‐plane spectra perpendicular or parallel to the projection of the FeNO plane. These enable assignment of the FeNO bending and stretching modes. The measurements reveal that the two in‐plane spectra have substantial differences that result from the strongly bonded axial NO ligand. The direction of the in‐plane iron motion is found to be largely parallel and perpendicular to the projection of the bent FeNO on the porphyrin plane. The out‐of‐plane Fe‐N‐O stretching and bending modes are strongly mixed with each other, as well as with porphyrin ligand modes. The stretch is mixed with v 50 as was also observed for dioxygen complexes. The frequency of the assigned stretching mode of eight Fe‐X‐O (X=N, C, and O) complexes is correlated with the Fe−XO bond lengths. The nature of highest frequency band at ≈560 cm −1 has also been examined in two additional new derivatives. Previously assigned as the Fe−NO stretch (by resonance Raman), it is better describedmore »
- Authors:
-
- Univ. of Notre Dame, Notre Dame, IN (United States)
- Argonne National Lab. (ANL), Argonne, IL (United States)
- Northeastern Univ., Boston, MA (United States)
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States)
- Sponsoring Org.:
- National Institutes of Health (NIH); National Science Foundation (NSF); USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22), Scientific User Facilities Division; USDOE
- OSTI Identifier:
- 1373306
- Alternate Identifier(s):
- OSTI ID: 1400744
- Grant/Contract Number:
- AC02-06CH11357
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Chemistry - A European Journal
- Additional Journal Information:
- Journal Volume: 22; Journal Issue: 18; Journal ID: ISSN 0947-6539
- Publisher:
- ChemPubSoc Europe
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
Citation Formats
Peng, Qian, Pavlik, Jeffrey W., Silvernail, Nathan J., Alp, E. Ercan, Hu, Michael Y., Zhao, Jiyong, Sage, J. Timothy, and Scheidt, W. Robert. 3D Motions of Iron in Six-Coordinate {FeNO}7 Hemes by Nuclear Resonance Vibration Spectroscopy [3-D Motions of Iron in Six-coordinate {FeNO}7 Hemes by NRVS. United States: N. p., 2016.
Web. doi:10.1002/chem.201505155.
Peng, Qian, Pavlik, Jeffrey W., Silvernail, Nathan J., Alp, E. Ercan, Hu, Michael Y., Zhao, Jiyong, Sage, J. Timothy, & Scheidt, W. Robert. 3D Motions of Iron in Six-Coordinate {FeNO}7 Hemes by Nuclear Resonance Vibration Spectroscopy [3-D Motions of Iron in Six-coordinate {FeNO}7 Hemes by NRVS. United States. https://doi.org/10.1002/chem.201505155
Peng, Qian, Pavlik, Jeffrey W., Silvernail, Nathan J., Alp, E. Ercan, Hu, Michael Y., Zhao, Jiyong, Sage, J. Timothy, and Scheidt, W. Robert. Mon .
"3D Motions of Iron in Six-Coordinate {FeNO}7 Hemes by Nuclear Resonance Vibration Spectroscopy [3-D Motions of Iron in Six-coordinate {FeNO}7 Hemes by NRVS". United States. https://doi.org/10.1002/chem.201505155. https://www.osti.gov/servlets/purl/1373306.
@article{osti_1373306,
title = {3D Motions of Iron in Six-Coordinate {FeNO}7 Hemes by Nuclear Resonance Vibration Spectroscopy [3-D Motions of Iron in Six-coordinate {FeNO}7 Hemes by NRVS},
author = {Peng, Qian and Pavlik, Jeffrey W. and Silvernail, Nathan J. and Alp, E. Ercan and Hu, Michael Y. and Zhao, Jiyong and Sage, J. Timothy and Scheidt, W. Robert},
abstractNote = {Abstract The vibrational spectrum of a six‐coordinate nitrosyl iron porphyrinate, monoclinic [Fe(T p FPP)(1‐MeIm)(NO)] (T p FPP=tetra‐ para ‐fluorophenylporphyrin; 1‐MeIm=1‐methylimidazole), has been studied by oriented single‐crystal nuclear resonance vibrational spectroscopy (NRVS). The crystal was oriented to give spectra perpendicular to the porphyrin plane and two in‐plane spectra perpendicular or parallel to the projection of the FeNO plane. These enable assignment of the FeNO bending and stretching modes. The measurements reveal that the two in‐plane spectra have substantial differences that result from the strongly bonded axial NO ligand. The direction of the in‐plane iron motion is found to be largely parallel and perpendicular to the projection of the bent FeNO on the porphyrin plane. The out‐of‐plane Fe‐N‐O stretching and bending modes are strongly mixed with each other, as well as with porphyrin ligand modes. The stretch is mixed with v 50 as was also observed for dioxygen complexes. The frequency of the assigned stretching mode of eight Fe‐X‐O (X=N, C, and O) complexes is correlated with the Fe−XO bond lengths. The nature of highest frequency band at ≈560 cm −1 has also been examined in two additional new derivatives. Previously assigned as the Fe−NO stretch (by resonance Raman), it is better described as the bend, as the motion of the central nitrogen atom of the FeNO group is very large. There is significant mixing of this mode. The results emphasize the importance of mode mixing; the extent of mixing must be related to the peripheral phenyl substituents.},
doi = {10.1002/chem.201505155},
journal = {Chemistry - A European Journal},
number = 18,
volume = 22,
place = {United States},
year = {Mon Mar 21 00:00:00 EDT 2016},
month = {Mon Mar 21 00:00:00 EDT 2016}
}
Web of Science
Works referenced in this record:
Relationships between nitric oxide, nitroxyl ion, nitrosonium cation and peroxynitrite
journal, May 1999
- Hughes, Martin N.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1411, Issue 2-3
Five- to Six-Coordination in (Nitrosyl)iron(II) Porphyrinates: Effects of Binding the Sixth Ligand
journal, September 2003
- Wyllie, Graeme R. A.; Schulz, Charles E.; Scheidt, W. Robert
- Inorganic Chemistry, Vol. 42, Issue 18
The Diagnostic Vibrational Signature of Pentacoordination in Heme Carbonyls
journal, July 2014
- Linder, Douglas P.; Silvernail, Nathan J.; Barabanschikov, Alexander
- Journal of the American Chemical Society, Vol. 136, Issue 28
Nitric Oxide Synthases: Properties and Catalytic Mechanism
journal, October 1995
- Griffith, O. W.; Stuehr, D. J.
- Annual Review of Physiology, Vol. 57, Issue 1
Structure?function studies on nitric oxide synthases
journal, January 2005
- Li, H.; Poulos, T.
- Journal of Inorganic Biochemistry, Vol. 99, Issue 1
Structure of Nitric Oxide Synthase Oxygenase Dimer with Pterin and Substrate
journal, March 1998
- Crane, B. R.
- Science, Vol. 279, Issue 5359
First-principles calculation of nuclear resonance vibrational spectra
journal, February 2007
- Petrenko, Taras; Sturhahn, Wolfgang; Neese, Frank
- Hyperfine Interactions, Vol. 175, Issue 1-3
Nuclear resonant inelastic absorption of synchrotron radiation in an anisotropic single crystal
journal, October 1998
- Kohn, V. G.; Chumakov, A. I.; Rüffer, R.
- Physical Review B, Vol. 58, Issue 13
Electronic Configuration of High-Spin Imidazole-Ligated Iron(II) Octaethylporphyrinates
journal, May 2006
- Hu, Chuanjiang; An, Jin; Noll, Bruce C.
- Inorganic Chemistry, Vol. 45, Issue 10
Nitric oxide signaling: no longer simply on or off
journal, April 2006
- Cary, Stephen P. L.; Winger, Jonathan A.; Derbyshire, Emily R.
- Trends in Biochemical Sciences, Vol. 31, Issue 4
A structural basis for H-NOX signaling in Shewanella oneidensis by trapping a histidine kinase inhibitory conformation
journal, November 2009
- Erbil, W. K.; Price, M. S.; Wemmer, D. E.
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 47
New Perspectives on Iron-Ligand Vibrations of Oxyheme Complexes
journal, August 2011
- Li, Jianfeng; Peng, Qian; Barabanschikov, Alexander
- Chemistry - A European Journal, Vol. 17, Issue 40
Heme-based sensors in biological systems
journal, April 1999
- Rodgers, Kenton R.
- Current Opinion in Chemical Biology, Vol. 3, Issue 2
Tetragonal to TriclinicA Phase Change for [Fe(TPP)(NO)]
journal, February 2009
- Silvernail, Nathan J.; Olmstead, Marilyn M.; Noll, Bruce C.
- Inorganic Chemistry, Vol. 48, Issue 3
Nitrite as regulator of hypoxic signaling in mammalian physiology
journal, September 2009
- van Faassen, Ernst E.; Bahrami, Soheyl; Feelisch, Martin
- Medicinal Research Reviews, Vol. 29, Issue 5
Phonon Density of States Measured by Inelastic Nuclear Resonant Scattering
journal, May 1995
- Sturhahn, W.; Toellner, T. S.; Alp, E. E.
- Physical Review Letters, Vol. 74, Issue 19
Probing Heme Vibrational Anisotropy: An Imidazole Orientation Effect?
journal, September 2013
- Peng, Qian; Li, Ming; Hu, Chuanjiang
- Inorganic Chemistry, Vol. 52, Issue 19
Nitric oxide interaction with insect nitrophorins and thoughts on the electron configuration of the FeNO complex
journal, January 2005
- Walker, F.
- Journal of Inorganic Biochemistry, Vol. 99, Issue 1
Nitric Oxide: A Physiologic Messenger Molecule
journal, June 1994
- Bredt, D. S.; Snyder, S. H.
- Annual Review of Biochemistry, Vol. 63, Issue 1
Nitrosyl adducts of FixL as probes of heme environment
journal, October 2000
- Rodgers, Kenton R.; Lukat-Rodgers, Gudrun S.; Tang, Lei
- JBIC Journal of Biological Inorganic Chemistry, Vol. 5, Issue 5
Nitrosylmetalloporphyrins. II. Synthesis and molecular stereochemistry of nitrosyl-.alpha.,.beta.,.gamma.,.delta.-tetraphenylporphinatoiron(II)
journal, January 1975
- Scheidt, W. Robert; Frisse, Mark E.
- Journal of the American Chemical Society, Vol. 97, Issue 1
Role of the anion nitrite in ischemia-reperfusion cytoprotection and therapeutics
journal, July 2007
- Dezfulian, C.; Raat, N.; Shiva, S.
- Cardiovascular Research, Vol. 75, Issue 2
Fully optimized contracted Gaussian basis sets for atoms Li to Kr
journal, August 1992
- Schäfer, Ansgar; Horn, Hans; Ahlrichs, Reinhart
- The Journal of Chemical Physics, Vol. 97, Issue 4
Nuclear resonance vibrational spectroscopy ? NRVS
journal, January 2005
- Scheidt, W.; Durbin, S.; Sage, J.
- Journal of Inorganic Biochemistry, Vol. 99, Issue 1
NO Orientation and Tilting in (Nitrosyl)iron(II) Deuteroporphyrin IX
journal, July 2003
- Wyllie, Graeme R. A.; Scheidt, W. Robert
- Inorganic Chemistry, Vol. 42, Issue 14
NO activation of guanylyl cyclase
journal, October 2004
- Russwurm, Michael; Koesling, Doris
- The EMBO Journal, Vol. 23, Issue 22
Ligand?protein interactions in nitric oxide synthase
journal, January 2005
- Rousseau, D.; Li, D.; Couture, M.
- Journal of Inorganic Biochemistry, Vol. 99, Issue 1
Structural Origin of Two Paramagnetic Species in Six-Coordinated Nitrosoiron(II) Porphyrins Revealed by Density Functional Theory Analysis of the g Tensors
journal, November 2000
- Patchkovskii, S.; Ziegler, T.
- Inorganic Chemistry, Vol. 39, Issue 23
Reversible NO Motion in Crystalline [Fe(Porph)(1-MeIm)(NO)] Derivatives
journal, February 2008
- Silvernail, Nathan J.; Pavlik, Jeffrey W.; Noll, Bruce C.
- Inorganic Chemistry, Vol. 47, Issue 3
Resonance Raman characterization of nitric oxide adducts of cytochrome P450cam: the effect of substrate structure on the iron-ligand vibrations
journal, April 1991
- Hu, Songzhou; Kincaid, James R.
- Journal of the American Chemical Society, Vol. 113, Issue 8
Correlated Ligand Dynamics in Oxyiron Picket Fence Porphyrins: Structural and Mössbauer Investigations
journal, October 2013
- Li, Jianfeng; Noll, Bruce C.; Oliver, Allen G.
- Journal of the American Chemical Society, Vol. 135, Issue 41
Nonheme Iron-Nitrosyl Complex Formation in Rat Hepatocytes: Detection by Electron Paramagnetic Resonance Spectroscopy
journal, April 1993
- Stadler, J.; Bergonia, H. A.; Disilvio, M.
- Archives of Biochemistry and Biophysics, Vol. 302, Issue 1
Principles of structure, bonding, and reactivity for metal nitrosyl complexes
journal, September 1974
- Enemark, J. H.; Feltham, R. D.
- Coordination Chemistry Reviews, Vol. 13, Issue 4
Convenient small-scale method for the insertion of iron into porphyrins
journal, February 1990
- Landergren, Marie; Baltzer, Lars
- Inorganic Chemistry, Vol. 29, Issue 3
The New Chemical Biology of Nitrite Reactions with Hemoglobin: R-State Catalysis, Oxidative Denitrosylation, and Nitrite Reductase/Anhydrase
journal, January 2009
- Gladwin, Mark T.; Grubina, Rozalina; Doyle, Michael P.
- Accounts of Chemical Research, Vol. 42, Issue 1
Biochemistry of nitric oxide and its redox-activated forms
journal, December 1992
- Stamler, J.; Singel, D.; Loscalzo, J.
- Science, Vol. 258, Issue 5090
Oriented Single-Crystal Nuclear Resonance Vibrational Spectroscopy of [Fe(TPP)(MI)(NO)]: Quantitative Assessment of the trans Effect of NO
journal, August 2010
- Lehnert, Nicolai; Sage, J. Timothy; Silvernail, Nathan
- Inorganic Chemistry, Vol. 49, Issue 15
Probing Vibrational Anisotropy with Nuclear Resonance Vibrational Spectroscopy
journal, June 2010
- Pavlik, Jeffrey W.; Barabanschikov, Alexander; Oliver, Allen G.
- Angewandte Chemie, Vol. 122, Issue 26
Six- to Five-Coordinate Heme−Nitrosyl Conversion in Cytochrome c‘ and Its Relevance to Guanylate Cyclase †
journal, February 2002
- Andrew, Colin R.; George, Simon J.; Lawson, David M.
- Biochemistry, Vol. 41, Issue 7
Femtomolar Sensitivity of a NO Sensor from Clostridium botulinum
journal, November 2004
- Nioche, P.
- Science, Vol. 306, Issue 5701
NO and CO differentially activate soluble guanylyl cyclase via a heme pivot-bend mechanism
journal, January 2007
- Ma, Xiaolei; Sayed, Nazish; Beuve, Annie
- The EMBO Journal, Vol. 26, Issue 2
How Biology Handles Nitrite
journal, April 2014
- Maia, Luisa B.; Moura, José J. G.
- Chemical Reviews, Vol. 114, Issue 10
Interplay of Structure and Vibrational Dynamics in Six-Coordinate Heme Nitrosyls
journal, February 2007
- Silvernail, Nathan J.; Barabanschikov, Alexander; Pavlik, Jeffrey W.
- Journal of the American Chemical Society, Vol. 129, Issue 8
Monochromatization of synchrotron radiation for nuclear resonant scattering experiments
journal, January 2000
- Toellner, T. S.
- Hyperfine Interactions, Vol. 125, Issue 1/4, p. 3-28
Solid-State Structures of Metalloporphyrin NO x Compounds
journal, April 2002
- Wyllie, Graeme R. A.; Scheidt, W. Robert
- Chemical Reviews, Vol. 102, Issue 4
A new local density functional for main-group thermochemistry, transition metal bonding, thermochemical kinetics, and noncovalent interactions
journal, November 2006
- Zhao, Yan; Truhlar, Donald G.
- The Journal of Chemical Physics, Vol. 125, Issue 19, Article No. 194101
Nitric oxide: first in a new class of neurotransmitters
journal, July 1992
- Snyder, S.
- Science, Vol. 257, Issue 5069
Consistent porphyrin force field. 2. Nickel octaethylporphyrin skeletal and substituent mode assignments from nitrogen-15, meso-d4, and methylene-d16 Raman and infrared isotope shifts
journal, January 1990
- Li, Xiao Yuan.; Czernuszewicz, Roman S.; Kincaid, James R.
- The Journal of Physical Chemistry, Vol. 94, Issue 1
Influence of magnetic interaction on lattice dynamics of FeBO 3
journal, October 2001
- Parlinski, K.; Łażewski, J.; Jochym, P. T.
- Europhysics Letters (EPL), Vol. 56, Issue 2
Heme Carbonyls: Environmental Effects on ν C - O and Fe−C/C−O Bond Length Correlations
journal, October 2005
- Silvernail, Nathan J.; Roth, Arne; Schulz, Charles E.
- Journal of the American Chemical Society, Vol. 127, Issue 41
Anisotropic Iron Motion in Nitrosyl Iron Porphyrinates: Natural and Synthetic Hemes
journal, February 2014
- Pavlik, Jeffrey W.; Peng, Qian; Silvernail, Nathan J.
- Inorganic Chemistry, Vol. 53, Issue 5
Nuclear resonance vibrational spectroscopy of a protein active-site mimic
journal, August 2001
- Sage, J. T.; Paxson, C.; Wyllie, G. R. A.
- Journal of Physics: Condensed Matter, Vol. 13, Issue 34
Embracing sulfide and CO to understand nitric oxide biology
journal, November 2013
- Feelisch, Martin; Olson, Kenneth R.
- Nitric Oxide, Vol. 35
Mapping NO Movements in Crystalline [Fe(Porph)(NO)(1-MeIm)]
journal, February 2009
- Silvernail, Nathan J.; Barabanschikov, Alexander; Sage, J. Timothy
- Journal of the American Chemical Society, Vol. 131, Issue 6
Bacterial Lipopeptides Induce Nitric Oxide Synthase and Promote Apoptosis through Nitric Oxide-independent Pathways in Rat Macrophages
journal, March 1995
- Terenzi, Fulvia; Díaz-Guerra, María J. M.; Casado, Marta
- Journal of Biological Chemistry, Vol. 270, Issue 11
Observation of coherent reaction dynamics in heme proteins
journal, October 1994
- Zhu, L.; Sage, J.; Champion, P.
- Science, Vol. 266, Issue 5185
Electronic Structure of Six-Coordinate Iron(III)−Porphyrin NO Adducts: The Elusive Iron(III)−NO(radical) State and Its Influence on the Properties of These Complexes
journal, November 2008
- Praneeth, V. K. K.; Paulat, Florian; Berto, Timothy C.
- Journal of the American Chemical Society, Vol. 130, Issue 46
Predicting Nuclear Resonance Vibrational Spectra of [Fe(OEP)(NO)]
journal, December 2011
- Peng, Qian; Pavlik, Jeffrey W.; Scheidt, W. Robert
- Journal of Chemical Theory and Computation, Vol. 8, Issue 1
FTIR and Resonance Raman Studies of Nitric Oxide Binding to H93G Cavity Mutants of Myoglobin †
journal, December 2001
- Thomas, Melissa R.; Brown, Derek; Franzen, Stefan
- Biochemistry, Vol. 40, Issue 49
Probing Vibrational Anisotropy with Nuclear Resonance Vibrational Spectroscopy
journal, June 2010
- Pavlik, Jeffrey W.; Barabanschikov, Alexander; Oliver, Allen G.
- Angewandte Chemie International Edition, Vol. 49, Issue 26
Quantitative Vibrational Dynamics of Iron in Carbonyl Porphyrins
journal, June 2007
- Leu, Bogdan M.; Silvernail, Nathan J.; Zgierski, Marek Z.
- Biophysical Journal, Vol. 92, Issue 11
The Chemical Biology of Nitric Oxide
book, January 2000
- Miranda, Katrina M.; Espey, Michael G.; Jourd'heuil, David
- Nitric Oxide: Biology and Pathobiology
The physiological role of nitric oxide
journal, January 1993
- Butler, Anthony R.; Williams, D. Lyn H.
- Chemical Society Reviews, Vol. 22, Issue 4
Microwave-Assisted Piloty−Robinson Synthesis of 3,4-Disubstituted Pyrroles
journal, April 2007
- Milgram, Benjamin C.; Eskildsen, Katrine; Richter, Steven M.
- The Journal of Organic Chemistry, Vol. 72, Issue 10
Nuclear resonant spectroscopy
journal, January 2004
- Sturhahn, Wolfgang
- Journal of Physics: Condensed Matter, Vol. 16, Issue 5
Resonance Raman Investigation of Fe−N−O Structure of Nitrosylheme in Myoglobin and Its Mutants
journal, August 1999
- Tomita, Takeshi; Hirota, Shun; Ogura, Takashi
- The Journal of Physical Chemistry B, Vol. 103, Issue 33
Vibrational Probes and Determinants of the S = 0 ⇌ S = 2 Spin Crossover in Five-Coordinate [Fe(TPP)(CN)] −
journal, October 2012
- Li, Jianfeng; Peng, Qian; Barabanschikov, Alexander
- Inorganic Chemistry, Vol. 51, Issue 21
Comprehensive Fe–Ligand Vibration Identification in {FeNO} 6 Hemes
journal, December 2014
- Li, Jianfeng; Peng, Qian; Oliver, Allen G.
- Journal of the American Chemical Society, Vol. 136, Issue 52
Nitric oxide and iron proteins
journal, May 1999
- Cooper, Chris E.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1411, Issue 2-3
Direct Probe of Iron Vibrations Elucidates NO Activation of Heme Proteins
journal, August 2005
- Zeng, Weiqiao; Silvernail, Nathan J.; Wharton, David C.
- Journal of the American Chemical Society, Vol. 127, Issue 32
Generation of EPR-detectable nitrosyl-iron complexes in tumor target cells cocultured with activated macrophages
journal, June 1991
- Drapier, J. C.; Pellat, C.; Henry, Y.
- Journal of Biological Chemistry, Vol. 266, Issue 16
Heme coordination and structure of the catalytic site in nitric oxide synthase.
journal, October 1993
- Wang, J.; Stuehr, D. J.; Ikeda-Saito, M.
- Journal of Biological Chemistry, Vol. 268, Issue 30
Nitric oxide synthase structure and mechanism
journal, June 1993
- Marletta, M. A.
- Journal of Biological Chemistry, Vol. 268, Issue 17
Microwave-Assisted Piloty−Robinson Synthesis of 3,4-Disubstituted Pyrroles
journal, April 2007
- Milgram, Benjamin C.; Eskildsen, Katrine; Richter, Steven M.
- The Journal of Organic Chemistry, Vol. 72, Issue 10, 3941–3944
Works referencing / citing this record:
What Can Be Learned from Nuclear Resonance Vibrational Spectroscopy: Vibrational Dynamics and Hemes
journal, September 2017
- Scheidt, W. Robert; Li, Jianfeng; Sage, J. Timothy
- Chemical Reviews, Vol. 117, Issue 19