Evidence for hydrogen bonding of bound dioxygen to the distal histidine of oxycobalt myoglobin and haemoglobin

T. Kitagawa, M. R. Ondrias, Denis L. Rousseau, M. Ikeda-saito, T. Yonetani

Research output: Contribution to journalArticle

94 Citations (Scopus)

Abstract

The origin of the differences in oxygen binding energy in various haemoglobins and myoglobins has long been debated. PERtz1 proposed that the haem-coordinated histidine (proximal histidine) strains the haem iron in low affinity globins but relaxes it in high affinity globins. The existence of such tension in T-structure deoxyhaemoglobin (deoxyHb) was recently confirmed by electron paramagnetic resonance (EPR)2,3, resonance Raman 4,5 and NMR6 spectroscopy. Although its contribution to the free energy of cooperativity is insignificant in the deoxy state, the tension at the haem is considered to be ∼1 kcal mol-1 for the ligated form in which the haem iron moves into the porphyrin plane7. The remaining free energy is probably stored in other parts of the molecule. Therefore, a study of the stabilization mechanisms of the oxygenated form became increasingly important. A hydrogen bond between the bound oxygen and the distal histidine has been proposed by Pauling8; this would be expected to stabilize the oxy form of the protein and could contribute to the regulation of the oxygen affinity through the oxygen dissociation rate. A series of EPR and functional studies on various cobalt-substituted monomeric haemoglobins and myoglobins suggested the presence of such hydrogen bonding8-12 and it has recently been established in crystals of oxy iron myoglobin (oxyFeMb) 13 and in oxyhaemoglobin14. Here we present resonance Raman spectra of the oxy forms of cobalt-porphyrin-substituted myoglobin and haemoglobin (CoMb and CoHb) recorded in buffered H2O and D 2O solutions at 406.7 nm excitation. Only the Raman lines corresponding to the O - O stretching mode of the bound oxygen15, appearing near 1,130 cm-1, are shifted (2-5 cm-1) on replacement of H2O by D2O; no other vibrations, including the Co - O2 stretching mode, exhibit any frequency shifts. This indicates that the bound oxygen in oxyCoMb and in both subunits of oxyCoHb interacts with the adjacent exchangeable proton, and confirms the formation of a hydrogen bond between the bound oxygen and the distal histidine9.

Original languageEnglish (US)
Pages (from-to)869-871
Number of pages3
JournalNature
Volume298
Issue number5877
DOIs
StatePublished - 1982
Externally publishedYes

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Oxyhemoglobins
Hydrogen Bonding
Histidine
Myoglobin
Oxygen
Heme
Hydrogen
Hemoglobins
Globins
Iron
Porphyrins
Electron Spin Resonance Spectroscopy
Cobalt
Comb and Wattles
Vibration
oxymyoglobin
Protons
Spectrum Analysis
Proteins

ASJC Scopus subject areas

  • General

Cite this

Evidence for hydrogen bonding of bound dioxygen to the distal histidine of oxycobalt myoglobin and haemoglobin. / Kitagawa, T.; Ondrias, M. R.; Rousseau, Denis L.; Ikeda-saito, M.; Yonetani, T.

In: Nature, Vol. 298, No. 5877, 1982, p. 869-871.

Research output: Contribution to journalArticle

Kitagawa, T. ; Ondrias, M. R. ; Rousseau, Denis L. ; Ikeda-saito, M. ; Yonetani, T. / Evidence for hydrogen bonding of bound dioxygen to the distal histidine of oxycobalt myoglobin and haemoglobin. In: Nature. 1982 ; Vol. 298, No. 5877. pp. 869-871.
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abstract = "The origin of the differences in oxygen binding energy in various haemoglobins and myoglobins has long been debated. PERtz1 proposed that the haem-coordinated histidine (proximal histidine) strains the haem iron in low affinity globins but relaxes it in high affinity globins. The existence of such tension in T-structure deoxyhaemoglobin (deoxyHb) was recently confirmed by electron paramagnetic resonance (EPR)2,3, resonance Raman 4,5 and NMR6 spectroscopy. Although its contribution to the free energy of cooperativity is insignificant in the deoxy state, the tension at the haem is considered to be ∼1 kcal mol-1 for the ligated form in which the haem iron moves into the porphyrin plane7. The remaining free energy is probably stored in other parts of the molecule. Therefore, a study of the stabilization mechanisms of the oxygenated form became increasingly important. A hydrogen bond between the bound oxygen and the distal histidine has been proposed by Pauling8; this would be expected to stabilize the oxy form of the protein and could contribute to the regulation of the oxygen affinity through the oxygen dissociation rate. A series of EPR and functional studies on various cobalt-substituted monomeric haemoglobins and myoglobins suggested the presence of such hydrogen bonding8-12 and it has recently been established in crystals of oxy iron myoglobin (oxyFeMb) 13 and in oxyhaemoglobin14. Here we present resonance Raman spectra of the oxy forms of cobalt-porphyrin-substituted myoglobin and haemoglobin (CoMb and CoHb) recorded in buffered H2O and D 2O solutions at 406.7 nm excitation. Only the Raman lines corresponding to the O - O stretching mode of the bound oxygen15, appearing near 1,130 cm-1, are shifted (2-5 cm-1) on replacement of H2O by D2O; no other vibrations, including the Co - O2 stretching mode, exhibit any frequency shifts. This indicates that the bound oxygen in oxyCoMb and in both subunits of oxyCoHb interacts with the adjacent exchangeable proton, and confirms the formation of a hydrogen bond between the bound oxygen and the distal histidine9.",
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T1 - Evidence for hydrogen bonding of bound dioxygen to the distal histidine of oxycobalt myoglobin and haemoglobin

AU - Kitagawa, T.

AU - Ondrias, M. R.

AU - Rousseau, Denis L.

AU - Ikeda-saito, M.

AU - Yonetani, T.

PY - 1982

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N2 - The origin of the differences in oxygen binding energy in various haemoglobins and myoglobins has long been debated. PERtz1 proposed that the haem-coordinated histidine (proximal histidine) strains the haem iron in low affinity globins but relaxes it in high affinity globins. The existence of such tension in T-structure deoxyhaemoglobin (deoxyHb) was recently confirmed by electron paramagnetic resonance (EPR)2,3, resonance Raman 4,5 and NMR6 spectroscopy. Although its contribution to the free energy of cooperativity is insignificant in the deoxy state, the tension at the haem is considered to be ∼1 kcal mol-1 for the ligated form in which the haem iron moves into the porphyrin plane7. The remaining free energy is probably stored in other parts of the molecule. Therefore, a study of the stabilization mechanisms of the oxygenated form became increasingly important. A hydrogen bond between the bound oxygen and the distal histidine has been proposed by Pauling8; this would be expected to stabilize the oxy form of the protein and could contribute to the regulation of the oxygen affinity through the oxygen dissociation rate. A series of EPR and functional studies on various cobalt-substituted monomeric haemoglobins and myoglobins suggested the presence of such hydrogen bonding8-12 and it has recently been established in crystals of oxy iron myoglobin (oxyFeMb) 13 and in oxyhaemoglobin14. Here we present resonance Raman spectra of the oxy forms of cobalt-porphyrin-substituted myoglobin and haemoglobin (CoMb and CoHb) recorded in buffered H2O and D 2O solutions at 406.7 nm excitation. Only the Raman lines corresponding to the O - O stretching mode of the bound oxygen15, appearing near 1,130 cm-1, are shifted (2-5 cm-1) on replacement of H2O by D2O; no other vibrations, including the Co - O2 stretching mode, exhibit any frequency shifts. This indicates that the bound oxygen in oxyCoMb and in both subunits of oxyCoHb interacts with the adjacent exchangeable proton, and confirms the formation of a hydrogen bond between the bound oxygen and the distal histidine9.

AB - The origin of the differences in oxygen binding energy in various haemoglobins and myoglobins has long been debated. PERtz1 proposed that the haem-coordinated histidine (proximal histidine) strains the haem iron in low affinity globins but relaxes it in high affinity globins. The existence of such tension in T-structure deoxyhaemoglobin (deoxyHb) was recently confirmed by electron paramagnetic resonance (EPR)2,3, resonance Raman 4,5 and NMR6 spectroscopy. Although its contribution to the free energy of cooperativity is insignificant in the deoxy state, the tension at the haem is considered to be ∼1 kcal mol-1 for the ligated form in which the haem iron moves into the porphyrin plane7. The remaining free energy is probably stored in other parts of the molecule. Therefore, a study of the stabilization mechanisms of the oxygenated form became increasingly important. A hydrogen bond between the bound oxygen and the distal histidine has been proposed by Pauling8; this would be expected to stabilize the oxy form of the protein and could contribute to the regulation of the oxygen affinity through the oxygen dissociation rate. A series of EPR and functional studies on various cobalt-substituted monomeric haemoglobins and myoglobins suggested the presence of such hydrogen bonding8-12 and it has recently been established in crystals of oxy iron myoglobin (oxyFeMb) 13 and in oxyhaemoglobin14. Here we present resonance Raman spectra of the oxy forms of cobalt-porphyrin-substituted myoglobin and haemoglobin (CoMb and CoHb) recorded in buffered H2O and D 2O solutions at 406.7 nm excitation. Only the Raman lines corresponding to the O - O stretching mode of the bound oxygen15, appearing near 1,130 cm-1, are shifted (2-5 cm-1) on replacement of H2O by D2O; no other vibrations, including the Co - O2 stretching mode, exhibit any frequency shifts. This indicates that the bound oxygen in oxyCoMb and in both subunits of oxyCoHb interacts with the adjacent exchangeable proton, and confirms the formation of a hydrogen bond between the bound oxygen and the distal histidine9.

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