Homolytic cleavage of both heme-bound hydrogen peroxide and hydrogen sulfide leads to the formation of sulfheme

Arbelo-Lopez, Hector D.; Simakov, Nikolay A.; Smith, Jeremy C.; Lopez-Garriga, Juan; Wymore, Troy

doi:10.1021/acs.jpcb.6b02839

Homolytic cleavage of both heme-bound hydrogen peroxide and hydrogen sulfide leads to the formation of sulfheme

Journal Article · Wed Jun 29 00:00:00 EDT 2016 · Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry

DOI:https://doi.org/10.1021/acs.jpcb.6b02839· OSTI ID:1327756

Arbelo-Lopez, Hector D. ^[1]; Simakov, Nikolay A. ^[2]; Smith, Jeremy C. ^[3]; Lopez-Garriga, Juan ^[1]; Wymore, Troy ^[4]

Univ. of Puerto Rico, Mayaguez (Puerto Rico)
Univ. of Buffalo, Buffalo, NY (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States)
Univ. of Tennessee, Knoxville, TN (United States)

Many heme-containing proteins with a histidine in the distal E7 (HisE7) position can form sulfheme in the presence of hydrogen sulfide (H₂S) and a reactive oxygen species such as hydrogen peroxide. For reasons unknown, sulfheme derivatives are formed specifically on solvent-excluded heme pyrrole B. Sulfhemes severely decrease the oxygen-binding affinity in hemoglobin (Hb) and myoglobin (Mb). Here, use of hybrid quantum mechanical/molecular mechanical methods has permitted characterization of the entire process of sulfheme formation in the HisE7 mutant of hemoglobin I (HbI) from Lucina pectinata. This process includes a mechanism for H₂S to enter the solvent-excluded active site through a hydrophobic channel to ultimately form a hydrogen bond with H₂O₂ bound to Fe(III). Proton transfer from H₂O₂ to His64 to form compound (Cpd) 0, followed by hydrogen transfer from H₂S to the Fe(III) H₂O₂ complex, results in homolytic cleavage of the O–O and S–H bonds to form a reactive thiyl radical (HS*), ferryl heme Cpd II, and a water molecule. Subsequently, the addition of HS to Cpd II, followed by three proton transfer reactions, results in the formation of a three-membered ring ferric sulfheme that avoids migration of the radical to the protein matrix, in contrast to that in other peroxidative reactions. The transformation of this three-membered episulfide ring structure to the five-membered thiochlorin ring structure occurs through a significant potential energy barrier, although both structures are nearly isoenergetic. Both three- and five-membered ring structures reveal longer N_B–Fe(III) bonds compared with other pyrrole nitrogen–Fe(III) bonds, which would lead to decreased oxygen binding. Altogether, these results are in agreement with a wide range of experimental data and provide fertile ground for further investigations of sulfheme formation in other heme proteins and additional effects of H₂S on cell signaling and reactivity.

View Accepted Manuscript (DOE)

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1327756

Journal Information:: Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry, Journal Name: Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry Journal Issue: 30 Vol. 120; ISSN 1520-6106

Publisher:: American Chemical SocietyCopyright Statement

Country of Publication:: United States

Language:: English

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Homolytic cleavage of both heme-bound hydrogen peroxide and hydrogen sulfide leads to the formation of sulfheme

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