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J. Biol. Chem., Vol. 278, Issue 13, 11513-11519, March 28, 2003

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High Resolution Structure of an Alternate Form of the Ferric Ion Binding Protein from Haemophilus influenzae^*

Stephen R. Shouldice, Douglas R. Dougan^§, Robert J. Skene^§, Leslie W. Tari^§, Duncan E. McRee^§, Rong-hua Yu^¶, and Anthony B. Schryvers^¶

From the  Department of Biological Sciences, University of Calgary, Calgary, Alberta T2N 1N4, Canada, ^§ Syrrx Inc., San Diego, California 92121, and the ^¶ Department of Microbiology and Infectious Diseases, University of Calgary, Calgary, Alberta T2N 4N1, Canada

The periplasmic iron binding protein of pathogenic Gram-negative bacteria performs an essential role in iron acquisition from transferrin and other iron sources. Structural analysis of this protein from Haemophilus influenzae identified four amino acids that ligand the bound iron: His⁹, Glu⁵⁷, Tyr¹⁹⁵, and Tyr¹⁹⁶. A phosphate provides an additional ligand, and the presence of a water molecule is required to complete the octahedral geometry for stable iron binding. We report the 1.14-Å resolution crystal structure of the iron-loaded form of the H. influenzae periplasmic ferric ion binding protein (FbpA) mutant H9Q. This protein was produced in the periplasm of Escherichia coli and, after purification and conversion to the apo form, was iron-loaded. H9Q is able to bind ferric iron in an open conformation. A surprising finding in the present high resolution structure is the presence of EDTA located at the previously determined anion ternary binding site, where phosphate is located in the wild type holo and apo structures. EDTA contributes four of the six coordinating ligands for iron, with two Tyr residues, 195 and 196, completing the coordination. This is the first example of a metal binding protein with a bound metal·EDTA complex. The results suggest that FbpA may have the ability to bind and transport iron bound to biological chelators, in addition to bare ferric iron.

The atomic coordinates and the structure factors (code 1NNF) have been deposited in the Protein Data Bank, Research Collaboratory for Structural Bioinformatics, Rutgers University, New Brunswick, NJ (http://www.rcsb.org/).

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