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Title: Spectroscopic studies reveal that the heme regulatory motifs of heme oxygenase-2 are dynamically disordered and exhibit redox-dependent interaction with heme

Abstract

Heme oxygenase (HO) catalyzes a key step in heme homeostasis: the O₂₋ and NADPH-cytochrome P450 reductase-dependent conversion of heme to biliverdin, Fe, and CO through a process in which the heme participates both as a prosthetic group and as a substrate. Mammals contain two isoforms of this enzyme, HO2 and HO1, which share the same α-helical fold forming the catalytic core and heme binding site, as well as a membrane spanning helix at their C-termini. However, unlike HO1, HO2 has an additional 30-residue N-terminus as well as two cysteine-proline sequences near the C-terminus that reside in heme regulatory motifs (HRMs). While the role of the additional N-terminal residues of HO2 is not yet understood, the HRMs have been proposed to reversibly form a thiol/disulfide redox switch that modulates the affinity of HO2 for ferric heme as a function of cellular redox poise. To further define the roles of the N- and C-terminal regions unique to HO2, we used multiple spectroscopic techniques to characterize these regions of the human HO2. Nuclear magnetic resonance spectroscopic experiments with HO2 demonstrate that, when the HRMs are in the oxidized state (HO2O), both the extra N-terminal and the C-terminal HRM-containing regions are disordered. However, proteinmore » NMR experiments illustrate that, under reducing conditions, the C-terminal region gains some structure as the Cys residues in the HRMs undergo reduction (HO2R) and, in experiments employing a diamagnetic protoporphyrin, suggest a redox-dependent interaction between the core and the HRM domains. Further, electron nuclear double resonance and X-ray absorption spectroscopic studies demonstrate that, upon reduction of the HRMs to the sulfhydryl form, a cysteine residue from the HRM region ligates to a ferric heme. Taken together with EPR measurements, which show the appearance of a new low-spin heme signal in reduced HO2, it appears that a cysteine residue(s) in the HRMs directly interacts with a second bound heme.« less

Authors:
 [1];  [2];  [1];  [3];  [3];  [1];  [1]
+ Show Author Affiliations
  1. Univ. of Michigan, Ann Arbor, MI (United States)
  2. SLAC National Accelerator Lab., Menlo Park, CA (United States)
  3. Northwestern Univ., Evanston, IL (United States)
Publication Date:
Research Org.:
SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1208862
Grant/Contract Number:  
AC03-76SF00515
Resource Type:
Accepted Manuscript
Journal Name:
Biochemistry
Additional Journal Information:
Journal Volume: 54; Journal Issue: 17; Journal ID: ISSN 0006-2960
Publisher:
American Chemical Society (ACS)
Country of Publication:
United States
Language:
English
Subject:
60 APPLIED LIFE SCIENCES

Citation Formats

Bagai, Ireena, Sarangi, Ritimukta, Fleischhacker, Angela S., Sharma, Ajay, Hoffman, Brian M., Zuiderweg, Erik R. P., and Ragsdale, Stephen W. Spectroscopic studies reveal that the heme regulatory motifs of heme oxygenase-2 are dynamically disordered and exhibit redox-dependent interaction with heme. United States: N. p., 2015. Web. doi:10.1021/bi501489r.
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Bagai, Ireena, Sarangi, Ritimukta, Fleischhacker, Angela S., Sharma, Ajay, Hoffman, Brian M., Zuiderweg, Erik R. P., & Ragsdale, Stephen W. Spectroscopic studies reveal that the heme regulatory motifs of heme oxygenase-2 are dynamically disordered and exhibit redox-dependent interaction with heme. United States. https://doi.org/10.1021/bi501489r
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Bagai, Ireena, Sarangi, Ritimukta, Fleischhacker, Angela S., Sharma, Ajay, Hoffman, Brian M., Zuiderweg, Erik R. P., and Ragsdale, Stephen W. Tue . "Spectroscopic studies reveal that the heme regulatory motifs of heme oxygenase-2 are dynamically disordered and exhibit redox-dependent interaction with heme". United States. https://doi.org/10.1021/bi501489r. https://www.osti.gov/servlets/purl/1208862.
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@article{osti_1208862,
title = {Spectroscopic studies reveal that the heme regulatory motifs of heme oxygenase-2 are dynamically disordered and exhibit redox-dependent interaction with heme},
author = {Bagai, Ireena and Sarangi, Ritimukta and Fleischhacker, Angela S. and Sharma, Ajay and Hoffman, Brian M. and Zuiderweg, Erik R. P. and Ragsdale, Stephen W.},
abstractNote = {Heme oxygenase (HO) catalyzes a key step in heme homeostasis: the O₂₋ and NADPH-cytochrome P450 reductase-dependent conversion of heme to biliverdin, Fe, and CO through a process in which the heme participates both as a prosthetic group and as a substrate. Mammals contain two isoforms of this enzyme, HO2 and HO1, which share the same α-helical fold forming the catalytic core and heme binding site, as well as a membrane spanning helix at their C-termini. However, unlike HO1, HO2 has an additional 30-residue N-terminus as well as two cysteine-proline sequences near the C-terminus that reside in heme regulatory motifs (HRMs). While the role of the additional N-terminal residues of HO2 is not yet understood, the HRMs have been proposed to reversibly form a thiol/disulfide redox switch that modulates the affinity of HO2 for ferric heme as a function of cellular redox poise. To further define the roles of the N- and C-terminal regions unique to HO2, we used multiple spectroscopic techniques to characterize these regions of the human HO2. Nuclear magnetic resonance spectroscopic experiments with HO2 demonstrate that, when the HRMs are in the oxidized state (HO2O), both the extra N-terminal and the C-terminal HRM-containing regions are disordered. However, protein NMR experiments illustrate that, under reducing conditions, the C-terminal region gains some structure as the Cys residues in the HRMs undergo reduction (HO2R) and, in experiments employing a diamagnetic protoporphyrin, suggest a redox-dependent interaction between the core and the HRM domains. Further, electron nuclear double resonance and X-ray absorption spectroscopic studies demonstrate that, upon reduction of the HRMs to the sulfhydryl form, a cysteine residue from the HRM region ligates to a ferric heme. Taken together with EPR measurements, which show the appearance of a new low-spin heme signal in reduced HO2, it appears that a cysteine residue(s) in the HRMs directly interacts with a second bound heme.},
doi = {10.1021/bi501489r},
journal = {Biochemistry},
number = 17,
volume = 54,
place = {United States},
year = {Tue May 05 00:00:00 EDT 2015},
month = {Tue May 05 00:00:00 EDT 2015}
}
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  • Lad, Latesh; Schuller, David J.; Shimizu, Hideaki
  • Journal of Biological Chemistry, Vol. 278, Issue 10
  • DOI: 10.1074/jbc.m211450200

Structural Characterization of the Hemophore HasAp from Pseudomonas aeruginosa : NMR Spectroscopy Reveals Protein−Protein Interactions between Holo-HasAp and Hemoglobin ,
journal, December 2008

  • Alontaga, Aileen Y.; Rodriguez, Juan Carlos; Schönbrunn, Ernst
  • Biochemistry, Vol. 48, Issue 1
  • DOI: 10.1021/bi801860g

Heme Oxygenase-2 Interaction with Metalloporphyrins: Function of Heme Regulatory Motifs
journal, August 2001

  • Huang, Tian J.; McCoubrey, William K.; Maines, Mahin D.
  • Antioxidants & Redox Signaling, Vol. 3, Issue 4
  • DOI: 10.1089/15230860152543023

Multiple Transcripts Encoding Heme Oxygenase-2 in Rat Testis: Developmental and Cell-Specific Regulation of Transcripts and Protein1
journal, December 1995

Characterization of two constitutive forms of rat liver microsomal heme oxygenase. Only one molecular species of the enzyme is inducible.
journal, January 1986

Evidence suggesting that the two forms of heme oxygenase are products of different genes.
journal, March 1988

Heme-heme oxygenase complex. Structure of the catalytic site and its implication for oxygen activation.
journal, January 1994

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    Dynamic and structural differences between heme oxygenase-1 and -2 are due to differences in their C-terminal regions
    journal, April 2019

    • Kochert, Brent A.; Fleischhacker, Angela S.; Wales, Thomas E.
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    The molecular basis of transient heme-protein interactions: analysis, concept and implementation
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    • Bioscience Reports, Vol. 39, Issue 1
    • DOI: 10.1042/bsr20181940

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    journal, January 2019

    • Shimizu, Toru; Lengalova, Alzbeta; Martínek, Václav
    • Chemical Society Reviews, Vol. 48, Issue 24
    • DOI: 10.1039/c9cs00268e
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