NMR solution structure of Cu(I) rusticyanin from thiobacillus ferrooxidans

Structural basis for the extreme acid stability and redox potential

Maria Victoria Botuyan, Anna Toy-Palmer, John Chung, Robert C. Blake, Paul Beroza, David Case, H. Jane Dyson

Research output: Contribution to journalArticle

81 Citations (Scopus)

Abstract

The solution structure of the Cu(I) form of the rusticyanin from Thiobacillus ferrooxidans has been calculated from a total of 1979 distance and dihedral angle constraints derived from 1H,13C and 15N NMR spectra. The structures reveal two β-sheets, one of six strands and one of seven strands that are tightly packed in a β-barrel or β-sandwich arrangement, and a short helix that extends on the outside of one of the sheets to form a second hydrophobic core. The copper coordination sphere is composed of the standard type I ligands (His2CysMet) in a distorted tetrahedral arrangement. The copper-binding site is located within a hydrophobic region at one end of the molecule, surrounded by a number of aromatic rings and hydrophobic residues. This configuration probably contributes to the acid stability of the copper site, since close association of the aromatic rings with the histidine ligands would sterically hinder their dissociation from the copper. An electrostatic analysis based on a comparison of the structures of rusticyanin and French bean plastocyanin shows that factors determining the high redox potential of rusticyanin include contributions from charged side-chains and from the disposition of backbone peptide dipoles, particularly in the 81 to 86 region of the sequence and the ligand, cysteine residue. These interactions should also contribute to the acid stability by inhibiting protonation of His143.

Original languageEnglish (US)
Pages (from-to)752-767
Number of pages16
JournalJournal of molecular biology
Volume263
Issue number5
DOIs
StatePublished - Nov 15 1996

Fingerprint

Thiobacillus
Oxidation-Reduction
Copper
Acids
Ligands
Plastocyanin
Static Electricity
Histidine
Cysteine
Binding Sites
Peptides
rusticyanin

All Science Journal Classification (ASJC) codes

  • Molecular Biology

Keywords

  • Rusticyanin
  • Solution structure
  • Type 1 copper protein

Cite this

Botuyan, Maria Victoria ; Toy-Palmer, Anna ; Chung, John ; Blake, Robert C. ; Beroza, Paul ; Case, David ; Dyson, H. Jane. / NMR solution structure of Cu(I) rusticyanin from thiobacillus ferrooxidans : Structural basis for the extreme acid stability and redox potential. In: Journal of molecular biology. 1996 ; Vol. 263, No. 5. pp. 752-767.
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NMR solution structure of Cu(I) rusticyanin from thiobacillus ferrooxidans : Structural basis for the extreme acid stability and redox potential. / Botuyan, Maria Victoria; Toy-Palmer, Anna; Chung, John; Blake, Robert C.; Beroza, Paul; Case, David; Dyson, H. Jane.

In: Journal of molecular biology, Vol. 263, No. 5, 15.11.1996, p. 752-767.

Research output: Contribution to journalArticle

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T1 - NMR solution structure of Cu(I) rusticyanin from thiobacillus ferrooxidans

T2 - Structural basis for the extreme acid stability and redox potential

AU - Botuyan, Maria Victoria

AU - Toy-Palmer, Anna

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AB - The solution structure of the Cu(I) form of the rusticyanin from Thiobacillus ferrooxidans has been calculated from a total of 1979 distance and dihedral angle constraints derived from 1H,13C and 15N NMR spectra. The structures reveal two β-sheets, one of six strands and one of seven strands that are tightly packed in a β-barrel or β-sandwich arrangement, and a short helix that extends on the outside of one of the sheets to form a second hydrophobic core. The copper coordination sphere is composed of the standard type I ligands (His2CysMet) in a distorted tetrahedral arrangement. The copper-binding site is located within a hydrophobic region at one end of the molecule, surrounded by a number of aromatic rings and hydrophobic residues. This configuration probably contributes to the acid stability of the copper site, since close association of the aromatic rings with the histidine ligands would sterically hinder their dissociation from the copper. An electrostatic analysis based on a comparison of the structures of rusticyanin and French bean plastocyanin shows that factors determining the high redox potential of rusticyanin include contributions from charged side-chains and from the disposition of backbone peptide dipoles, particularly in the 81 to 86 region of the sequence and the ligand, cysteine residue. These interactions should also contribute to the acid stability by inhibiting protonation of His143.

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