Interaction of nitric oxide with prostaglandin endoperoxide H synthase-1

Implications for Fe-His bond cleavage in heme proteins

Johannes Schelvis, Steve A. Seibold, Jose F. Cerda, R. Michael Garavito, Gerald T. Babcock

Research output: Contribution to journalArticleResearchpeer-review

22 Citations (Scopus)

Abstract

We have investigated the cleavage of the bond between the heme iron and the proximal heme ligand, His388, in ferrous ovine prostaglandin endoperoxide H synthase-1 (oPGHS-1) on nitric oxide (NO) binding by using resonance Raman spectroscopy. The Fe-NO and N~O vibrations are observed at 526 and 1667 cm-1, respectively, which is indicative of a five-coordinated, heme-NO complex. We also observed NO photolysis under low-power, continuous wave conditions, which reflects nongeminate rebinding of NO to the heme cofactor on the millisecond time scale. Furthermore, we attempted to make a six-coordinated heme-NO complex by adding imidazole (Im) to ferrous oPGHS-1-NO. However, ferrous oPGHS-1-NO remained fivecoordinated even in the presence of 500 mM Im. The heme-NO complex remains bound in the heme pocket after Fe-His bond cleavage, and subsequent protein backbone movement is relatively small. Finally, we compared the structures of several heme proteins that form either five- or six-coordinated complexes with NO. Inspection of the heme-proximal His geometry did not reveal any common structural parameter that may be critical for Fe-His bond cleavage. However, the Fe-His stretching frequency [v(Fe-His)] shows a good correlation with Fe-His bond cleavage and is modulated by hydrogen bonding to the Nδ proton of the His. We propose that the strength of this hydrogen bond is the primary factor determining Fe-His bond cleavage: a strong hydrogen bond gives the His imidazolate character, which allows it to compensate for the NO trans ligand effect and to avoid Fe-His bond cleavage.

Original languageEnglish
Pages (from-to)10844-10850
Number of pages7
JournalJournal of Physical Chemistry B
Volume104
Issue number46
StatePublished - 23 Nov 2000

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Prostaglandin Endoperoxides
prostaglandins
Hemeproteins
Nitric oxide
nitric oxide
cleavage
Nitric Oxide
Heme
proteins
interactions
Hydrogen bonds
imidazoles
Ligands
hydrogen bonds
ligands
Photolysis
Stretching
continuous radiation
photolysis
Raman spectroscopy

Cite this

Schelvis, Johannes ; Seibold, Steve A. ; Cerda, Jose F. ; Michael Garavito, R. ; Babcock, Gerald T. / Interaction of nitric oxide with prostaglandin endoperoxide H synthase-1 : Implications for Fe-His bond cleavage in heme proteins. In: Journal of Physical Chemistry B. 2000 ; Vol. 104, No. 46. pp. 10844-10850.
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abstract = "We have investigated the cleavage of the bond between the heme iron and the proximal heme ligand, His388, in ferrous ovine prostaglandin endoperoxide H synthase-1 (oPGHS-1) on nitric oxide (NO) binding by using resonance Raman spectroscopy. The Fe-NO and N~O vibrations are observed at 526 and 1667 cm-1, respectively, which is indicative of a five-coordinated, heme-NO complex. We also observed NO photolysis under low-power, continuous wave conditions, which reflects nongeminate rebinding of NO to the heme cofactor on the millisecond time scale. Furthermore, we attempted to make a six-coordinated heme-NO complex by adding imidazole (Im) to ferrous oPGHS-1-NO. However, ferrous oPGHS-1-NO remained fivecoordinated even in the presence of 500 mM Im. The heme-NO complex remains bound in the heme pocket after Fe-His bond cleavage, and subsequent protein backbone movement is relatively small. Finally, we compared the structures of several heme proteins that form either five- or six-coordinated complexes with NO. Inspection of the heme-proximal His geometry did not reveal any common structural parameter that may be critical for Fe-His bond cleavage. However, the Fe-His stretching frequency [v(Fe-His)] shows a good correlation with Fe-His bond cleavage and is modulated by hydrogen bonding to the Nδ proton of the His. We propose that the strength of this hydrogen bond is the primary factor determining Fe-His bond cleavage: a strong hydrogen bond gives the His imidazolate character, which allows it to compensate for the NO trans ligand effect and to avoid Fe-His bond cleavage.",
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Interaction of nitric oxide with prostaglandin endoperoxide H synthase-1 : Implications for Fe-His bond cleavage in heme proteins. / Schelvis, Johannes; Seibold, Steve A.; Cerda, Jose F.; Michael Garavito, R.; Babcock, Gerald T.

In: Journal of Physical Chemistry B, Vol. 104, No. 46, 23.11.2000, p. 10844-10850.

Research output: Contribution to journalArticleResearchpeer-review

TY - JOUR

T1 - Interaction of nitric oxide with prostaglandin endoperoxide H synthase-1

T2 - Implications for Fe-His bond cleavage in heme proteins

AU - Schelvis, Johannes

AU - Seibold, Steve A.

AU - Cerda, Jose F.

AU - Michael Garavito, R.

AU - Babcock, Gerald T.

PY - 2000/11/23

Y1 - 2000/11/23

N2 - We have investigated the cleavage of the bond between the heme iron and the proximal heme ligand, His388, in ferrous ovine prostaglandin endoperoxide H synthase-1 (oPGHS-1) on nitric oxide (NO) binding by using resonance Raman spectroscopy. The Fe-NO and N~O vibrations are observed at 526 and 1667 cm-1, respectively, which is indicative of a five-coordinated, heme-NO complex. We also observed NO photolysis under low-power, continuous wave conditions, which reflects nongeminate rebinding of NO to the heme cofactor on the millisecond time scale. Furthermore, we attempted to make a six-coordinated heme-NO complex by adding imidazole (Im) to ferrous oPGHS-1-NO. However, ferrous oPGHS-1-NO remained fivecoordinated even in the presence of 500 mM Im. The heme-NO complex remains bound in the heme pocket after Fe-His bond cleavage, and subsequent protein backbone movement is relatively small. Finally, we compared the structures of several heme proteins that form either five- or six-coordinated complexes with NO. Inspection of the heme-proximal His geometry did not reveal any common structural parameter that may be critical for Fe-His bond cleavage. However, the Fe-His stretching frequency [v(Fe-His)] shows a good correlation with Fe-His bond cleavage and is modulated by hydrogen bonding to the Nδ proton of the His. We propose that the strength of this hydrogen bond is the primary factor determining Fe-His bond cleavage: a strong hydrogen bond gives the His imidazolate character, which allows it to compensate for the NO trans ligand effect and to avoid Fe-His bond cleavage.

AB - We have investigated the cleavage of the bond between the heme iron and the proximal heme ligand, His388, in ferrous ovine prostaglandin endoperoxide H synthase-1 (oPGHS-1) on nitric oxide (NO) binding by using resonance Raman spectroscopy. The Fe-NO and N~O vibrations are observed at 526 and 1667 cm-1, respectively, which is indicative of a five-coordinated, heme-NO complex. We also observed NO photolysis under low-power, continuous wave conditions, which reflects nongeminate rebinding of NO to the heme cofactor on the millisecond time scale. Furthermore, we attempted to make a six-coordinated heme-NO complex by adding imidazole (Im) to ferrous oPGHS-1-NO. However, ferrous oPGHS-1-NO remained fivecoordinated even in the presence of 500 mM Im. The heme-NO complex remains bound in the heme pocket after Fe-His bond cleavage, and subsequent protein backbone movement is relatively small. Finally, we compared the structures of several heme proteins that form either five- or six-coordinated complexes with NO. Inspection of the heme-proximal His geometry did not reveal any common structural parameter that may be critical for Fe-His bond cleavage. However, the Fe-His stretching frequency [v(Fe-His)] shows a good correlation with Fe-His bond cleavage and is modulated by hydrogen bonding to the Nδ proton of the His. We propose that the strength of this hydrogen bond is the primary factor determining Fe-His bond cleavage: a strong hydrogen bond gives the His imidazolate character, which allows it to compensate for the NO trans ligand effect and to avoid Fe-His bond cleavage.

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M3 - Article

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SP - 10844

EP - 10850

JO - Journal of Physical Chemistry B

JF - Journal of Physical Chemistry B

SN - 1520-6106

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