Abstract
In heme enzymes belonging to the peroxidase-cyclooxygenase superfamily the proximal histidine is in close interaction with a fully conserved asparagine. The crystal structure of a mixture of glycoforms of myeloperoxidase (MPO) purified from granules of human leukocytes prompted us to revise the orientation of this asparagine and the protonation status of the proximal histidine. The data we present contrast with previous MPO structures, but are strongly supported by molecular dynamics simulations. Moreover, comprehensive analysis of published lactoperoxidase structures suggest that the described proximal heme architecture is a general structural feature of animal heme peroxidases. Its importance is underlined by the fact that the MPO variant N421D, recombinantly expressed in mammalian cell lines, exhibited modified spectral properties and diminished catalytic activity compared with wild-type recombinant MPO. It completely lost its ability to oxidize chloride to hypochlorous acid, which is a characteristic feature of MPO and essential for its role in host defense. The presented crystal structure of MPO revealed further important differences compared with the published structures including the extent of glycosylation, interaction between light and heavy polypeptides, as well as heme to protein covalent bonds. These data are discussed with respect to biosynthesis and post-translational maturation of MPO as well as to its peculiar biochemical and biophysical properties.
MeSH Terms
Asparagine/chemistry,genetics,metabolism
Cell Line
Chlorides/metabolism
Crystallography, X-Ray
Glycosylation
Heme/chemistry,genetics,metabolism
Histidine/chemistry,genetics,metabolism
Humans
Hypochlorous Acid/metabolism
Lactoperoxidase/chemistry,genetics,metabolism
Leukocytes/enzymology
Mutation, Missense
Oxidation-Reduction
Peroxidase/chemistry,genetics,metabolism
Protein Processing, Post-Translational/physiology
Protein Structure, Tertiary/physiology
Chemicals
Chlorides
Heme
Histidine
Asparagine
Hypochlorous Acid
Lactoperoxidase
Peroxidase
Authors & Affiliations
11 authors, click to expand affiliations / ORCID
Carpena Xavier
Institute of Research in Biomedicine (IRB-Barcelona), Parc Científic, Baldiri i Reixac 10, 08028 Barcelona, Spain.
Vidossich Pietro
Schroettner Klarissa
Calisto Barbara M
Banerjee Srijib
Stampler Johanna
Soudi Monika
Furtmüller Paul G
Rovira Carme
Fita Ignacio
Obinger Christian
References (34)
34 references, click to expand
-
Myeloperoxidase: a target for new drug development?
Br J Pharmacol. 2007 Nov;152(6):838-54
PMID: 17592500
-
Disruption of the aspartate to heme ester linkage in human myeloperoxidase: impact on ligand binding, redox chemistry, and interconversion of redox intermediates.
J Biol Chem. 2007 Jun 8;282(23):17041-52
PMID: 17438335
-
Role of the covalent glutamic acid 242-heme linkage in the formation and reactivity of redox intermediates of human myeloperoxidase.
Biochemistry. 2005 May 3;44(17):6482-91
PMID: 15850382
-
Kinetics of oxidation of tyrosine and dityrosine by myeloperoxidase compounds I and II. Implications for lipoprotein peroxidation studies.
J Biol Chem. 1995 Dec 22;270(51):30434-40
PMID: 8530471
-
Refinement of macromolecular structures by the maximum-likelihood method.
Acta Crystallogr D Biol Crystallogr. 1997 May 1;53(Pt 3):240-55
PMID: 15299926
-
Processing of X-ray diffraction data collected in oscillation mode.
Methods Enzymol. 1997;276:307-26
PMID: 27754618
-
Scalable molecular dynamics with NAMD.
J Comput Chem. 2005 Dec;26(16):1781-802
PMID: 16222654
-
X-ray crystal structure of canine myeloperoxidase at 3 A resolution.
J Mol Biol. 1992 Jul 5;226(1):185-207
PMID: 1320128
-
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
-
X-ray crystal structure and characterization of halide-binding sites of human myeloperoxidase at 1.8 A resolution.
J Biol Chem. 2000 Apr 21;275(16):11964-71
PMID: 10766826
-
Structural and biological properties of human recombinant myeloperoxidase produced by Chinese hamster ovary cell lines.
Eur J Biochem. 1991 May 8;197(3):605-14
PMID: 1851479
-
Heme to protein linkages in mammalian peroxidases: impact on spectroscopic, redox and catalytic properties.
Nat Prod Rep. 2007 Jun;24(3):571-84
PMID: 17534531
-
Active site structure and catalytic mechanisms of human peroxidases.
Arch Biochem Biophys. 2006 Jan 15;445(2):199-213
PMID: 16288970
-
Human myeloperoxidase: structure of a cyanide complex and its interaction with bromide and thiocyanate substrates at 1.9 A resolution.
Biochemistry. 2001 Nov 20;40(46):13990-7
PMID: 11705390
-
Development and testing of a general amber force field.
J Comput Chem. 2004 Jul 15;25(9):1157-74
PMID: 15116359
-
A new technique for the assay of infectivity of human adenovirus 5 DNA.
Virology. 1973 Apr;52(2):456-67
PMID: 4705382
-
Prokaryotic origins of the non-animal peroxidase superfamily and organelle-mediated transmission to eukaryotes.
Genomics. 2007 May;89(5):567-79
PMID: 17355904
-
Characterization of cDNA clones for human myeloperoxidase: predicted amino acid sequence and evidence for multiple mRNA species.
Nucleic Acids Res. 1987 Mar 11;15(5):2013-28
PMID: 3031585
-
Myeloperoxidase: friend and foe.
J Leukoc Biol. 2005 May;77(5):598-625
PMID: 15689384
-
Biosynthesis, processing, and sorting of human myeloperoxidase.
Arch Biochem Biophys. 2006 Jan 15;445(2):214-24
PMID: 16183032
-
A modified version of the Cornell et al. force field with improved sugar pucker phases and helical repeat.
J Biomol Struct Dyn. 1999 Feb;16(4):845-62
PMID: 10217454
-
Thyroid peroxidase and thyroxine biosynthesis.
Recent Prog Horm Res. 1970;26:189-247
PMID: 4919091
-
The reduction potential of lactoperoxidase.
Acta Chem Scand B. 1983;37(10):917-21
PMID: 6675378
-
A transient kinetic study on the reactivity of recombinant unprocessed monomeric myeloperoxidase.
FEBS Lett. 2001 Aug 17;503(2-3):147-50
PMID: 11513872
-
Identification of the colored guaiacol oxidation product produced by peroxidases.
Anal Biochem. 1997 Jul 15;250(1):10-7
PMID: 9234893
-
Crystal structure of lactoperoxidase at 2.4 A resolution.
J Mol Biol. 2008 Feb 29;376(4):1060-75
PMID: 18191143
-
Granules of the human neutrophilic polymorphonuclear leukocyte.
Blood. 1997 May 15;89(10):3503-21
PMID: 9160655
-
The role of the sulfonium linkage in the stabilization of the ferrous form of myeloperoxidase: a comparison with lactoperoxidase.
Biochim Biophys Acta. 2008 May;1784(5):843-9
PMID: 18359301
-
The peroxidase-cyclooxygenase superfamily: Reconstructed evolution of critical enzymes of the innate immune system.
Proteins. 2008 Aug;72(2):589-605
PMID: 18247411
-
Eosinophils and human disease.
Int Arch Allergy Appl Immunol. 1989;88(1-2):59-62
PMID: 2651320
-
Redox thermodynamics of the Fe(III)/Fe(II) couple of human myeloperoxidase in its high-spin and low-spin forms.
Biochemistry. 2006 Oct 24;45(42):12750-5
PMID: 17042493
-
Biochemical evidence for heme linkage through esters with Asp-93 and Glu-241 in human eosinophil peroxidase. The ester with Asp-93 is only partially formed in vivo.
J Biol Chem. 1999 Jun 11;274(24):16953-8
PMID: 10358043
-
Molecular evolution of thyroid peroxidase.
Biochimie. 1999 May;81(5):557-62
PMID: 10403190
-
The mechanism of myeloperoxidase-dependent chlorination of monochlorodimedon.
Biochim Biophys Acta. 1988 Nov 23;957(2):185-91
PMID: 2847800