Accessibility of the distal heme face, rather than Fe-His bond strength, determines the heme-nitrosyl coordination number of cytochromes c′: Evidence from spectroscopic studies

Colin R. Andrew, Lenord J. Kemper, Tammy L. Busche, Arianne M. Tiwari, Michael C. Kecskes, James M. Stafford, Lea C. Croft, Shen Lu, Pierre Moenne-Loccoz, Willa Huston, James W B Moir, Robert R. Eady

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Abstract

The heme coordination chemistry and spectroscopic properties of Rhodobacter capsulatus cytochrome c′ (RCCP) have been compared to data from Alcaligenes xylosoxidans (AXCP), with the aim of understanding the basis for their different reactivities with nitric oxide (NO). Whereas ferrous AXCP reacts with NO to form a predominantly five-coordinate heme-nitrosyl complex via a six-coordinate intermediate, RCCP forms an equilibrium mixture of six-coordinate and five-coordinate heme-nitrosyl species in approximately equal proportions. Ferrous RCCP and AXCP both exhibit high Fe-His stretching frequencies (227 and 231 cm-1, respectively), suggesting that factors other than the Fe-His bond strength account for their differences in heme-nitrosyl coordination number. Resonance Raman spectra of ferrous-nitrosyl RCCP confirm the presence of both five-coordinate and six-coordinate heme-NO complexes. The six-coordinate heme-nitrosyl of RCCP exhibits a fairly typical Fe-NO stretching frequency (569 cm-1), in contrast to the relatively high value (579 cm -1) of the AXCP six-coordinate heme-nitrosyl intermediate. It is proposed that NO experiences greater steric hindrance in binding to the distal face of AXCP, as compared to RCCP, leading to a more distorted Fe-N-O geometry and an elevated Fe-NO stretching frequency. Evidence that RCCP has a more accessible distal coordination site than in AXCP stems from the fact that ferric RCCP readily forms a heme complex with exogenous imidazole, whereas AXCP does not. A model is proposed in which distal heme-face accessibility, rather than the proximal Fe-His bond strength, determines the heme-nitrosyl coordination number in cytochromes c′.

Original languageEnglish (US)
Pages (from-to)8664-8672
Number of pages9
JournalBiochemistry
Volume44
Issue number24
DOIs
StatePublished - Jun 21 2005

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Rhodobacter capsulatus
Cytochromes c
Heme
Nitric Oxide
Stretching
Alcaligenes
Raman scattering
Geometry

ASJC Scopus subject areas

  • Biochemistry

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Accessibility of the distal heme face, rather than Fe-His bond strength, determines the heme-nitrosyl coordination number of cytochromes c′ : Evidence from spectroscopic studies. / Andrew, Colin R.; Kemper, Lenord J.; Busche, Tammy L.; Tiwari, Arianne M.; Kecskes, Michael C.; Stafford, James M.; Croft, Lea C.; Lu, Shen; Moenne-Loccoz, Pierre; Huston, Willa; Moir, James W B; Eady, Robert R.

In: Biochemistry, Vol. 44, No. 24, 21.06.2005, p. 8664-8672.

Research output: Contribution to journalArticle

Andrew, CR, Kemper, LJ, Busche, TL, Tiwari, AM, Kecskes, MC, Stafford, JM, Croft, LC, Lu, S, Moenne-Loccoz, P, Huston, W, Moir, JWB & Eady, RR 2005, 'Accessibility of the distal heme face, rather than Fe-His bond strength, determines the heme-nitrosyl coordination number of cytochromes c′: Evidence from spectroscopic studies', Biochemistry, vol. 44, no. 24, pp. 8664-8672. https://doi.org/10.1021/bi050428g
Andrew, Colin R. ; Kemper, Lenord J. ; Busche, Tammy L. ; Tiwari, Arianne M. ; Kecskes, Michael C. ; Stafford, James M. ; Croft, Lea C. ; Lu, Shen ; Moenne-Loccoz, Pierre ; Huston, Willa ; Moir, James W B ; Eady, Robert R. / Accessibility of the distal heme face, rather than Fe-His bond strength, determines the heme-nitrosyl coordination number of cytochromes c′ : Evidence from spectroscopic studies. In: Biochemistry. 2005 ; Vol. 44, No. 24. pp. 8664-8672.
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abstract = "The heme coordination chemistry and spectroscopic properties of Rhodobacter capsulatus cytochrome c′ (RCCP) have been compared to data from Alcaligenes xylosoxidans (AXCP), with the aim of understanding the basis for their different reactivities with nitric oxide (NO). Whereas ferrous AXCP reacts with NO to form a predominantly five-coordinate heme-nitrosyl complex via a six-coordinate intermediate, RCCP forms an equilibrium mixture of six-coordinate and five-coordinate heme-nitrosyl species in approximately equal proportions. Ferrous RCCP and AXCP both exhibit high Fe-His stretching frequencies (227 and 231 cm-1, respectively), suggesting that factors other than the Fe-His bond strength account for their differences in heme-nitrosyl coordination number. Resonance Raman spectra of ferrous-nitrosyl RCCP confirm the presence of both five-coordinate and six-coordinate heme-NO complexes. The six-coordinate heme-nitrosyl of RCCP exhibits a fairly typical Fe-NO stretching frequency (569 cm-1), in contrast to the relatively high value (579 cm -1) of the AXCP six-coordinate heme-nitrosyl intermediate. It is proposed that NO experiences greater steric hindrance in binding to the distal face of AXCP, as compared to RCCP, leading to a more distorted Fe-N-O geometry and an elevated Fe-NO stretching frequency. Evidence that RCCP has a more accessible distal coordination site than in AXCP stems from the fact that ferric RCCP readily forms a heme complex with exogenous imidazole, whereas AXCP does not. A model is proposed in which distal heme-face accessibility, rather than the proximal Fe-His bond strength, determines the heme-nitrosyl coordination number in cytochromes c′.",
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T1 - Accessibility of the distal heme face, rather than Fe-His bond strength, determines the heme-nitrosyl coordination number of cytochromes c′

T2 - Evidence from spectroscopic studies

AU - Andrew, Colin R.

AU - Kemper, Lenord J.

AU - Busche, Tammy L.

AU - Tiwari, Arianne M.

AU - Kecskes, Michael C.

AU - Stafford, James M.

AU - Croft, Lea C.

AU - Lu, Shen

AU - Moenne-Loccoz, Pierre

AU - Huston, Willa

AU - Moir, James W B

AU - Eady, Robert R.

PY - 2005/6/21

Y1 - 2005/6/21

N2 - The heme coordination chemistry and spectroscopic properties of Rhodobacter capsulatus cytochrome c′ (RCCP) have been compared to data from Alcaligenes xylosoxidans (AXCP), with the aim of understanding the basis for their different reactivities with nitric oxide (NO). Whereas ferrous AXCP reacts with NO to form a predominantly five-coordinate heme-nitrosyl complex via a six-coordinate intermediate, RCCP forms an equilibrium mixture of six-coordinate and five-coordinate heme-nitrosyl species in approximately equal proportions. Ferrous RCCP and AXCP both exhibit high Fe-His stretching frequencies (227 and 231 cm-1, respectively), suggesting that factors other than the Fe-His bond strength account for their differences in heme-nitrosyl coordination number. Resonance Raman spectra of ferrous-nitrosyl RCCP confirm the presence of both five-coordinate and six-coordinate heme-NO complexes. The six-coordinate heme-nitrosyl of RCCP exhibits a fairly typical Fe-NO stretching frequency (569 cm-1), in contrast to the relatively high value (579 cm -1) of the AXCP six-coordinate heme-nitrosyl intermediate. It is proposed that NO experiences greater steric hindrance in binding to the distal face of AXCP, as compared to RCCP, leading to a more distorted Fe-N-O geometry and an elevated Fe-NO stretching frequency. Evidence that RCCP has a more accessible distal coordination site than in AXCP stems from the fact that ferric RCCP readily forms a heme complex with exogenous imidazole, whereas AXCP does not. A model is proposed in which distal heme-face accessibility, rather than the proximal Fe-His bond strength, determines the heme-nitrosyl coordination number in cytochromes c′.

AB - The heme coordination chemistry and spectroscopic properties of Rhodobacter capsulatus cytochrome c′ (RCCP) have been compared to data from Alcaligenes xylosoxidans (AXCP), with the aim of understanding the basis for their different reactivities with nitric oxide (NO). Whereas ferrous AXCP reacts with NO to form a predominantly five-coordinate heme-nitrosyl complex via a six-coordinate intermediate, RCCP forms an equilibrium mixture of six-coordinate and five-coordinate heme-nitrosyl species in approximately equal proportions. Ferrous RCCP and AXCP both exhibit high Fe-His stretching frequencies (227 and 231 cm-1, respectively), suggesting that factors other than the Fe-His bond strength account for their differences in heme-nitrosyl coordination number. Resonance Raman spectra of ferrous-nitrosyl RCCP confirm the presence of both five-coordinate and six-coordinate heme-NO complexes. The six-coordinate heme-nitrosyl of RCCP exhibits a fairly typical Fe-NO stretching frequency (569 cm-1), in contrast to the relatively high value (579 cm -1) of the AXCP six-coordinate heme-nitrosyl intermediate. It is proposed that NO experiences greater steric hindrance in binding to the distal face of AXCP, as compared to RCCP, leading to a more distorted Fe-N-O geometry and an elevated Fe-NO stretching frequency. Evidence that RCCP has a more accessible distal coordination site than in AXCP stems from the fact that ferric RCCP readily forms a heme complex with exogenous imidazole, whereas AXCP does not. A model is proposed in which distal heme-face accessibility, rather than the proximal Fe-His bond strength, determines the heme-nitrosyl coordination number in cytochromes c′.

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