On the possible roles of N-terminal His-rich domains of Cu,Zn SODs of some Gram-negative bacteria

Dávid Árus, A. Jancsó, Dániel Szunyogh, Ferenc Matyuska, N. Nagy, Eufrozina Hoffmann, T. Körtvélyesi, T. Gajda

Research output: Contribution to journalArticle

19 Citations (Scopus)

Abstract

The Cu,Zn superoxide dismutases (Cu,Zn SOD) isolated from some Gram-negative bacteria possess a His-rich N-terminal metal binding extension. The N-terminal domain of Haemophilus ducreyi Cu,Zn SOD has been previously proposed to play a copper(II)-, and may be a zinc(II)-chaperoning role under metal ion starvation, and to behave as a temporary (low activity) superoxide dismutating center if copper(II) is available. The N-terminal extension of Cu,Zn SOD from Actinobacillus pleuropneumoniae starts with an analogous sequence (HxDHxH), but contains considerably fewer metal binding sites. In order to study the possibility of the generalization of the above mentioned functions over all Gram-negative bacteria possessing His-rich N-terminal extension, here we report thermodynamic and solution structural analysis of the copper(II) and zinc(II) complexes of a peptide corresponding to the first eight amino acids (HADHDHKK-NH 2, L) of the enzyme isolated from A. pleuropneumoniae. In equimolar solutions of Cu(II)/Zn(II) and the peptide the MH 2L complexes are dominant in the neutral pH-range. L has extraordinary copper(II) sequestering capacity (K D,Cu = 7.4 × 10 - 13 M at pH 7.4), which is provided only by non-amide (side chain) donors. The central ion in CuH 2L is coordinated by four nitrogens {NH 2,3N im} in the equatorial plane. In ZnH 2L the peptide binds to zinc(II) through a {NH 2,2N im,COO -} donor set, and its zinc binding affinity is relatively modest (K D,Zn = 4.8 × 10 - 7 M at pH 7.4). Consequently, the presented data do support a general chaperoning role of the N-terminal His-rich region of Gram-negative bacteria in copper(II) uptake, but do not confirm similar function for zinc(II). Interestingly, the complex CuH 2L has very high SOD-like activity, which may further support the multifunctional role of the copper(II)-bound N-terminal His-rich domain of Cu,Zn SODs of Gram-negative bacteria. The proposed structure for the MH 2L complexes has been verified by semiempirical quantum chemical calculations (PM6), too.

Original languageEnglish
Pages (from-to)10-18
Number of pages9
JournalJournal of Inorganic Biochemistry
Volume106
Issue number1
DOIs
Publication statusPublished - Jan 2012

Fingerprint

Gram-Negative Bacteria
Copper
Bacteria
Zinc
Actinobacillus pleuropneumoniae
Metals
Haemophilus ducreyi
Ions
Peptides
Starvation
Thermodynamics
Structural analysis
Superoxides
Metal ions
Nitrogen
Binding Sites
Amino Acids
Enzymes
Superoxide Dismutase-1
Superoxide Dismutase

Keywords

  • Copper(II)
  • Cu,Zn SOD
  • Histidine
  • Peptide complexes
  • Zinc(II)

ASJC Scopus subject areas

  • Biochemistry
  • Inorganic Chemistry

Cite this

On the possible roles of N-terminal His-rich domains of Cu,Zn SODs of some Gram-negative bacteria. / Árus, Dávid; Jancsó, A.; Szunyogh, Dániel; Matyuska, Ferenc; Nagy, N.; Hoffmann, Eufrozina; Körtvélyesi, T.; Gajda, T.

In: Journal of Inorganic Biochemistry, Vol. 106, No. 1, 01.2012, p. 10-18.

Research output: Contribution to journalArticle

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AU - Matyuska, Ferenc

AU - Nagy, N.

AU - Hoffmann, Eufrozina

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AB - The Cu,Zn superoxide dismutases (Cu,Zn SOD) isolated from some Gram-negative bacteria possess a His-rich N-terminal metal binding extension. The N-terminal domain of Haemophilus ducreyi Cu,Zn SOD has been previously proposed to play a copper(II)-, and may be a zinc(II)-chaperoning role under metal ion starvation, and to behave as a temporary (low activity) superoxide dismutating center if copper(II) is available. The N-terminal extension of Cu,Zn SOD from Actinobacillus pleuropneumoniae starts with an analogous sequence (HxDHxH), but contains considerably fewer metal binding sites. In order to study the possibility of the generalization of the above mentioned functions over all Gram-negative bacteria possessing His-rich N-terminal extension, here we report thermodynamic and solution structural analysis of the copper(II) and zinc(II) complexes of a peptide corresponding to the first eight amino acids (HADHDHKK-NH 2, L) of the enzyme isolated from A. pleuropneumoniae. In equimolar solutions of Cu(II)/Zn(II) and the peptide the MH 2L complexes are dominant in the neutral pH-range. L has extraordinary copper(II) sequestering capacity (K D,Cu = 7.4 × 10 - 13 M at pH 7.4), which is provided only by non-amide (side chain) donors. The central ion in CuH 2L is coordinated by four nitrogens {NH 2,3N im} in the equatorial plane. In ZnH 2L the peptide binds to zinc(II) through a {NH 2,2N im,COO -} donor set, and its zinc binding affinity is relatively modest (K D,Zn = 4.8 × 10 - 7 M at pH 7.4). Consequently, the presented data do support a general chaperoning role of the N-terminal His-rich region of Gram-negative bacteria in copper(II) uptake, but do not confirm similar function for zinc(II). Interestingly, the complex CuH 2L has very high SOD-like activity, which may further support the multifunctional role of the copper(II)-bound N-terminal His-rich domain of Cu,Zn SODs of Gram-negative bacteria. The proposed structure for the MH 2L complexes has been verified by semiempirical quantum chemical calculations (PM6), too.

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