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Title: Proton mediated spin state transition of cobalt heme analogs

Abstract

The spin state transition from low spin to high spin upon substrate addition is one of the key steps in cytochrome P450 catalysis. External perturbations such as pH and hydrogen bonding can also trigger the spin state transition of hemes through deprotonated histidine (e.g. Cytochrome c). In this work, we report the isolated 2-methylimidazole Cobalt(II) [Co(TPP)(2-MeHIm)] and [Co(TTP)(2-MeHIm)], and the corresponding 2-methylimidazolate derivatives where the N–H proton of axial 2-MeHIm is removed. Interestingly, various spectroscopies including EPR and XAFS determine a high-spin state (S = 3/2) for the imidazolate derivatives, in contrast to the low-spin state (S = 1/2) of all known imidazole analogs. DFT assisted stereoelectronic investigations are applied to understand the metal-ligand interactions, which suggest that the dramatically displaced metal center allowing a promotion e g(d π) → b 1g(d x2–y2) is crucial for the occurrence of the spin state transition.

Authors:
 [1];  [2];  [2];  [3];  [3];  [1];  [4];  [4];  [5];  [5];  [6];  [1]
  1. Univ. of Chinese Academy of Sciences, Beijing (China)
  2. Nankai Univ., Tianjin (China)
  3. Chinese Academy of Sciences (CAS), Beijing (China)
  4. Beijing Normal Univ., Beijing (China)
  5. Argonne National Lab. (ANL), Argonne, IL (United States)
  6. Dalian Univ. of Technology, Dalian (China)
Publication Date:
Research Org.:
Argonne National Lab. (ANL), Argonne, IL (United States)
Sponsoring Org.:
National Natural Science Foundation of China (NNSFC); USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)
OSTI Identifier:
1526720
Grant/Contract Number:  
AC02-06CH11357
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 10; Journal Issue: 1; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY

Citation Formats

Zhao, Jianping, Peng, Qian, Wang, Zijian, Xu, Wei, Xiao, Hongyan, Wu, Qi, Sun, Hao -Ling, Ma, Fang, Zhao, Jiyong, Sun, Cheng -Jun, Zhao, Jianzhang, and Li, Jianfeng. Proton mediated spin state transition of cobalt heme analogs. United States: N. p., 2019. Web. doi:10.1038/s41467-019-10357-z.
Zhao, Jianping, Peng, Qian, Wang, Zijian, Xu, Wei, Xiao, Hongyan, Wu, Qi, Sun, Hao -Ling, Ma, Fang, Zhao, Jiyong, Sun, Cheng -Jun, Zhao, Jianzhang, & Li, Jianfeng. Proton mediated spin state transition of cobalt heme analogs. United States. doi:10.1038/s41467-019-10357-z.
Zhao, Jianping, Peng, Qian, Wang, Zijian, Xu, Wei, Xiao, Hongyan, Wu, Qi, Sun, Hao -Ling, Ma, Fang, Zhao, Jiyong, Sun, Cheng -Jun, Zhao, Jianzhang, and Li, Jianfeng. Fri . "Proton mediated spin state transition of cobalt heme analogs". United States. doi:10.1038/s41467-019-10357-z. https://www.osti.gov/servlets/purl/1526720.
@article{osti_1526720,
title = {Proton mediated spin state transition of cobalt heme analogs},
author = {Zhao, Jianping and Peng, Qian and Wang, Zijian and Xu, Wei and Xiao, Hongyan and Wu, Qi and Sun, Hao -Ling and Ma, Fang and Zhao, Jiyong and Sun, Cheng -Jun and Zhao, Jianzhang and Li, Jianfeng},
abstractNote = {The spin state transition from low spin to high spin upon substrate addition is one of the key steps in cytochrome P450 catalysis. External perturbations such as pH and hydrogen bonding can also trigger the spin state transition of hemes through deprotonated histidine (e.g. Cytochrome c). In this work, we report the isolated 2-methylimidazole Cobalt(II) [Co(TPP)(2-MeHIm)] and [Co(TTP)(2-MeHIm)], and the corresponding 2-methylimidazolate derivatives where the N–H proton of axial 2-MeHIm is removed. Interestingly, various spectroscopies including EPR and XAFS determine a high-spin state (S = 3/2) for the imidazolate derivatives, in contrast to the low-spin state (S = 1/2) of all known imidazole analogs. DFT assisted stereoelectronic investigations are applied to understand the metal-ligand interactions, which suggest that the dramatically displaced metal center allowing a promotion eg(dπ) → b1g(dx2–y2) is crucial for the occurrence of the spin state transition.},
doi = {10.1038/s41467-019-10357-z},
journal = {Nature Communications},
number = 1,
volume = 10,
place = {United States},
year = {2019},
month = {5}
}

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Works referenced in this record:

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    Works referencing / citing this record:

    Hydrogen-Bonding Interactions Trigger a Spin-Flip in Iron(III) Porphyrin Complexes
    journal, February 2015

    • Sahoo, Dipankar; Quesne, Matthew G.; de Visser, Sam P.
    • Angewandte Chemie International Edition, Vol. 54, Issue 16
    • DOI: 10.1002/anie.201411399

    EasySpin, a comprehensive software package for spectral simulation and analysis in EPR
    journal, January 2006


    Spin-state/stereochemical relationships in iron porphyrins: implications for the hemoproteins
    journal, December 1981

    • Scheidt, W. Robert; Reed, Christopher A.
    • Chemical Reviews, Vol. 81, Issue 6
    • DOI: 10.1021/cr00046a002

    Structure and Chemistry of Cytochrome P450
    journal, June 2005

    • Denisov, Ilia G.; Makris, Thomas M.; Sligar, Stephen G.
    • Chemical Reviews, Vol. 105, Issue 6
    • DOI: 10.1021/cr0307143

    Synthetic oxygen carriers related to biological systems
    journal, April 1979

    • Jones, Robert D.; Summerville, David A.; Basolo, Fred.
    • Chemical Reviews, Vol. 79, Issue 2
    • DOI: 10.1021/cr60318a002

    Low-spin manganese(III) porphyrin imidazolate and cyanide complexes. Modulation of magnetic anisotropy by axial ligation
    journal, December 1984

    • Hansen, Andrew P.; Goff, Harold M.
    • Inorganic Chemistry, Vol. 23, Issue 26
    • DOI: 10.1021/ic00194a023

    Pincer porphyrin: x-ray crystal structure of a binuclear zinc/copper complex
    journal, November 1987

    • Rodgers, Steven J.; Koch, Carol A.; Tate, John R.
    • Inorganic Chemistry, Vol. 26, Issue 22
    • DOI: 10.1021/ic00269a003

    Structure of the Deoxymyoglobin Model [Fe(TPP)(2-MeHIm)] Reveals Unusual Porphyrin Core Distortions
    journal, April 2002

    • Ellison, Mary K.; Schulz, Charles E.; Scheidt, W. Robert
    • Inorganic Chemistry, Vol. 41, Issue 8
    • DOI: 10.1021/ic020012g

    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
    • DOI: 10.1021/ic052194v

    Oxygenation of Cobalt Porphyrinates: Coordination or Oxidation?
    journal, March 2010

    • Li, Jianfeng; Noll, Bruce C.; Oliver, Allen G.
    • Inorganic Chemistry, Vol. 49, Issue 5
    • DOI: 10.1021/ic902309f

    EPR and Magnetic Susceptibility Studies of Cobalt(II)- and Nickel(II)-Substituted Azurins from Pseudomonas aeruginosa . Electronic Structure of the Active Sites
    journal, January 1996

    • Jiménez, Hermas R.; Salgado, Jesús; Moratal, José M.
    • Inorganic Chemistry, Vol. 35, Issue 10
    • DOI: 10.1021/ic9513548

    19 F NMR and Structural Evidence for Spin-State Modulation of Six-Coordinate Cobalt(II) in a Weak Field Porphyrin Ligand 1
    journal, September 1998

    • Smirnov, Valeriy V.; Woller, Eric K.; DiMagno, Stephen G.
    • Inorganic Chemistry, Vol. 37, Issue 19
    • DOI: 10.1021/ic980156o

    A deoxymyoglobin model with a sterically unhindered axial imidazole
    journal, February 1988

    • Momenteau, Michel.; Scheidt, W. Robert.; Eigenbrot, C. W.
    • Journal of the American Chemical Society, Vol. 110, Issue 4
    • DOI: 10.1021/ja00212a032

    X-ray absorption edge determination of the oxidation state and coordination number of copper. Application to the type 3 site in Rhus vernicifera laccase and its reaction with oxygen
    journal, October 1987

    • Kau, Lung Shan; Spira-Solomon, Darlene J.; Penner-Hahn, James E.
    • Journal of the American Chemical Society, Vol. 109, Issue 21
    • DOI: 10.1021/ja00255a032

    EPR evidence for hydrogen bond donation to the terminal oxygen of cobalt-oxygen model compounds and cobalt oxymyoglobin
    journal, December 1985

    • Walker, F. Ann; Bowen, James
    • Journal of the American Chemical Society, Vol. 107, Issue 25
    • DOI: 10.1021/ja00311a067

    Imidazolate complexes of ferric porphyrins
    journal, August 1977

    • Nappa, Mario; Valentine, Joan S.; Snyder, Patricia A.
    • Journal of the American Chemical Society, Vol. 99, Issue 17
    • DOI: 10.1021/ja00459a045

    Stereochemistry of cobalt porphyrins. III. Structure of 2,3,7,8,12,13,17,18-octaethylporphinato(1-methylimidazole)cobalt(II). Model for deoxycoboglobin
    journal, July 1974

    • Little, Robert G.; Ibers, James A.
    • Journal of the American Chemical Society, Vol. 96, Issue 14
    • DOI: 10.1021/ja00821a018

    Stereochemistry of low-spin cobalt porphyrins. VI. Molecular stereochemistry of (1,2-dimethylimidazole)-.alpha.,.beta.,.gamma.,.delta.-tetraphenylporphinatocobalt(II)
    journal, July 1974

    • Dwyer, Patrick N.; Madura, Paul; Scheidt, W. Robert
    • Journal of the American Chemical Society, Vol. 96, Issue 15
    • DOI: 10.1021/ja00822a018

    Electronic Configuration Assignment and the Importance of Low-Lying Excited States in High-Spin Imidazole-Ligated Iron(II) Porphyrinates
    journal, April 2005

    • Hu, Chuanjiang; Roth, Arne; Ellison, Mary K.
    • Journal of the American Chemical Society, Vol. 127, Issue 15
    • DOI: 10.1021/ja044077p

    EPR and Optical Spectroscopic Studies of Met80X Mutants of Yeast Ferricytochrome c . Models for Intermediates in the Alkaline Transition
    journal, January 2005

    • Silkstone, Gary G.; Cooper, Christopher E.; Svistunenko, Dimitri
    • Journal of the American Chemical Society, Vol. 127, Issue 1
    • DOI: 10.1021/ja045719b

    Proton-Mediated Electron Configuration Change in High-Spin Iron(II) Porphyrinates
    journal, November 2005

    • Hu, Chuanjiang; Noll, Bruce C.; Schulz, Charles E.
    • Journal of the American Chemical Society, Vol. 127, Issue 43
    • DOI: 10.1021/ja055129t

    Structural Insights into Ligand Dynamics: Correlated Oxygen and Picket Motion in Oxycobalt Picket Fence Porphyrins
    journal, June 2012

    • Li, Jianfeng; Noll, Bruce C.; Oliver, Allen G.
    • Journal of the American Chemical Society, Vol. 134, Issue 25
    • DOI: 10.1021/ja303475a

    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
    • DOI: 10.1021/ja408431z

    Characterization of Porphyrin-Co(III)-‘Nitrene Radical’ Species Relevant in Catalytic Nitrene Transfer Reactions
    journal, April 2015

    • Goswami, Monalisa; Lyaskovskyy, Volodymyr; Domingos, Sérgio R.
    • Journal of the American Chemical Society, Vol. 137, Issue 16
    • DOI: 10.1021/jacs.5b01197

    Synthesis of Co II –NO Complexes and Their Reactivity as a Source of Nitroxyl
    journal, September 2016

    • Walter, Melody R.; Dzul, Stephen P.; Rodrigues, Andria V.
    • Journal of the American Chemical Society, Vol. 138, Issue 38
    • DOI: 10.1021/jacs.6b05896

    Unraveling 5f-6d hybridization in uranium compounds via spin-resolved L-edge spectroscopy
    journal, October 2017


    Thermal stability and crystallochemical analysis for CoII-based coordination polymers with TPP and TPPS porphyrins
    journal, January 2013

    • Fidalgo-Marijuan, Arkaitz; Barandika, Gotzone; Bazán, Begoña
    • CrystEngComm, Vol. 15, Issue 20
    • DOI: 10.1039/c3ce40161h

    Identification of the ligand-exchange process in the alkaline transition of horse heart cytochrome c
    journal, August 1987

    • Gadsby, P. M.; Peterson, J.; Foote, N.
    • Biochemical Journal, Vol. 246, Issue 1
    • DOI: 10.1042/bj2460043

    Density‐functional thermochemistry. III. The role of exact exchange
    journal, April 1993

    • Becke, Axel D.
    • The Journal of Chemical Physics, Vol. 98, Issue 7, p. 5648-5652
    • DOI: 10.1063/1.464913

    Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density
    journal, January 1988