Abstract
Heme-binding protein 23 kDa (HBP23), a rat isoform of human proliferation-associated gene product (PAG), is a member of the peroxiredoxin family of peroxidases, having two conserved cysteine residues. Recent biochemical studies have shown that HBP23/PAG is an oxidative stress-induced and proliferation-coupled multifunctional protein that exhibits specific bindings to c-Abl protein tyrosine kinase and heme, as well as a peroxidase activity. A 2.6-A resolution crystal structure of rat HBP23 in oxidized form revealed an unusual dimer structure in which the active residue Cys-52 forms a disulfide bond with conserved Cys-173 from another subunit by C-terminal tail swapping. The active site is largely hydrophobic with partially exposed Cys-173, suggesting a reduction mechanism of oxidized HBP23 by thioredoxin. Thus, the unusual cysteine disulfide bond is involved in peroxidation catalysis by using thioredoxin as the source of reducing equivalents. The structure also provides a clue to possible interaction surfaces for c-Abl and heme. Several significant structural differences have been found from a 1-Cys peroxiredoxin, ORF6, which lacks the C-terminal conserved cysteine corresponding to Cys-173 of HBP23.
MeSH Terms
Amino Acid Sequence
Animals
Arabidopsis Proteins
Binding Sites
Crystallography, X-Ray
Heme/metabolism
Humans
Models, Molecular
Molecular Sequence Data
Peroxidases/chemistry,metabolism
Peroxiredoxins
Protein Conformation
Rats
Recombinant Proteins/chemistry
Sequence Homology, Amino Acid
Chemicals
Arabidopsis Proteins
Recombinant Proteins
Heme
Peroxidases
BAS1 protein, Arabidopsis
Peroxiredoxins
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Hirotsu S
Department of Molecular Biology, Nara Institute of Science and Technology, 8916-5 Takayama, Ikoma, Nara 630-0101, Japan.
Abe Y
Okada K
Nagahara N
Hori H
Nishino T
Hakoshima T
References (27)
27 references, click to expand
-
Crystallographic characterization of a stress-induced multifunctional protein, rat HBP-23.
J Struct Biol. 1999 Jun 1;126(1):80-3
PMID: 10329492
-
Methods used in the structure determination of bovine mitochondrial F1 ATPase.
Acta Crystallogr D Biol Crystallogr. 1996 Jan 1;52(Pt 1):30-42
PMID: 15299723
-
Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons.
Proteins. 1991;11(4):281-96
PMID: 1758883
-
Improved methods for building protein models in electron density maps and the location of errors in these models.
Acta Crystallogr A. 1991 Mar 1;47 ( Pt 2):110-9
PMID: 2025413
-
Slow-cooling protocols for crystallographic refinement by simulated annealing.
Acta Crystallogr A. 1990 Jul 1;46 ( Pt 7):585-93
PMID: 2206482
-
The non-flavin redox center of the streptococcal NADH peroxidase. II. Evidence for a stabilized cysteine-sulfenic acid.
J Biol Chem. 1989 Jul 25;264(21):12330-8
PMID: 2501303
-
Processing of X-ray diffraction data collected in oscillation mode.
Methods Enzymol. 1997;276:307-26
PMID: 27754618
-
[27] Maximum-likelihood heavy-atom parameter refinement for multiple isomorphous replacement and multiwavelength anomalous diffraction methods.
Methods Enzymol. 1997;276:472-494
PMID: 27799110
-
The refined structure of the selenoenzyme glutathione peroxidase at 0.2-nm resolution.
Eur J Biochem. 1983 Jun 1;133(1):51-69
PMID: 6852035
-
Purification, characterization, and cloning of a heme-binding protein (23 kDa) in rat liver cytosol.
Biochemistry. 1995 Oct 17;34(41):13398-406
PMID: 7577926
-
Induction of the antioxidant stress proteins heme oxygenase-1 and MSP23 by stress agents and oxidised LDL in cultured vascular smooth muscle cells.
FEBS Lett. 1995 Jul 17;368(2):239-42
PMID: 7628613
-
Antioxidant function of recombinant human natural killer enhancing factor.
Biochem Biophys Res Commun. 1995 Mar 28;208(3):964-9
PMID: 7702627
-
Structural determinants of peptide-binding orientation and of sequence specificity in SH3 domains.
Nature. 1994 Nov 24;372(6504):375-9
PMID: 7802869
-
Inhibition of metal-catalyzed oxidation systems by a yeast protector protein in the presence of thioredoxin.
Biochem Biophys Res Commun. 1994 May 30;201(1):8-15
PMID: 7911017
-
Thioredoxin-dependent peroxide reductase from yeast.
J Biol Chem. 1994 Nov 4;269(44):27670-8
PMID: 7961686
-
Dimerization of thiol-specific antioxidant and the essential role of cysteine 47.
Proc Natl Acad Sci U S A. 1994 Jul 19;91(15):7022-6
PMID: 8041739
-
A human cDNA corresponding to a gene overexpressed during cell proliferation encodes a product sharing homology with amoebic and bacterial proteins.
J Biol Chem. 1993 May 25;268(15):11050-6
PMID: 8496166
-
Removal of hydrogen peroxide by thiol-specific antioxidant enzyme (TSA) is involved with its antioxidant properties. TSA possesses thiol peroxidase activity.
J Biol Chem. 1996 Jun 28;271(26):15315-21
PMID: 8663080
-
Crystal structures of reduced, oxidized, and mutated human thioredoxins: evidence for a regulatory homodimer.
Structure. 1996 Jun 15;4(6):735-51
PMID: 8805557
-
AP-1 transcriptional activity is regulated by a direct association between thioredoxin and Ref-1.
Proc Natl Acad Sci U S A. 1997 Apr 15;94(8):3633-8
PMID: 9108029
-
The PAG gene product, a stress-induced protein with antioxidant properties, is an Abl SH3-binding protein and a physiological inhibitor of c-Abl tyrosine kinase activity.
Genes Dev. 1997 Oct 1;11(19):2456-67
PMID: 9334312
-
Roles for the two cysteine residues of AhpC in catalysis of peroxide reduction by alkyl hydroperoxide reductase from Salmonella typhimurium.
Biochemistry. 1997 Oct 28;36(43):13349-56
PMID: 9341227
-
Characterization of a mammalian peroxiredoxin that contains one conserved cysteine.
J Biol Chem. 1998 Mar 13;273(11):6303-11
PMID: 9497358
-
The pag gene product, a physiological inhibitor of c-abl tyrosine kinase, is overexpressed in cells entering S phase and by contact with agents inducing oxidative stress.
FEBS Lett. 1998 Feb 13;423(1):39-44
PMID: 9506838
-
Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1.
EMBO J. 1998 May 1;17(9):2596-606
PMID: 9564042
-
Crystal structure of a novel human peroxidase enzyme at 2.0 A resolution.
Nat Struct Biol. 1998 May;5(5):400-6
PMID: 9587003
-
Crystal structure of the abl-SH3 domain complexed with a designed high-affinity peptide ligand: implications for SH3-ligand interactions.
J Mol Biol. 1998 Aug 21;281(3):513-21
PMID: 9698566