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Chapter 8 : Periplasmic Binding Proteins Involved in Bacterial Iron Uptake

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Periplasmic Binding Proteins Involved in Bacterial Iron Uptake, Page 1 of 2

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Abstract:

This chapter focuses on the structural biology of periplasmic binding proteins (PBPs) in general and, more specifically, on the iron binding PBPs whose structures have been solved: ferric ion binding proteins (FbpA), siderophore-binding protein (FhuD), and vitamin B12 binding protein (BtuF). It also discusses some studies of the TroA protein, which is structurally related to FhuD. Although not involved in iron transport or iron transport-related events, maltose binding protein (MBP) is one of the best-characterized PBPs and is therefore a good mechanistic model of periplasmic transport. A portion of the chapter describes different experimental techniques which have been used to characterize the motions that MBP undergoes on ligand association or dissociation. Although the binding pocket of FhuA is deeper than that of FhuD, it still could accommodate a more bulky ligand such as albomycin. Albomycin consists of an antibiotic group attached to a hydroxamate siderophore via an amino acyl linker. Although rational design of a novel, efficient antibiotic by chemical conjugation is challenging, the Trojan horse design may become increasingly important due to the growing problem of antibiotic resistance.

Citation: Krewulak K, Peacock R, Vogel H. 2004. Periplasmic Binding Proteins Involved in Bacterial Iron Uptake, p 113-132. In Crosa J, Mey A, Payne S, Iron Transport in Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555816544.ch8

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Outer Membrane Proteins
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Figures

Image of FIGURE 1
FIGURE 1

Topological arrangement of PBPs. (A) Two-strand linker as represented by ferric ion binding protein. (B) Three-strand linker as represented by L-arabinose binding protein. (C) Helix linker as represented by ferrihydroxamate uptake binding protein (FhuD).

Citation: Krewulak K, Peacock R, Vogel H. 2004. Periplasmic Binding Proteins Involved in Bacterial Iron Uptake, p 113-132. In Crosa J, Mey A, Payne S, Iron Transport in Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555816544.ch8
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Image of FIGURE 2
FIGURE 2

Conformational change of MBP on ligand binding. apo MBP (A) and MBP bound to maltose (B) are shown. Domain closure when MBP binds its ligand demonstrates the term “Venus flytrap mechanism.” Note that although the structure of the N- and C-terminal domains remains unchanged on ligand binding, their orientation with respect to each other changes drastically. This hinge motion is very efficient since it requires changes in the orientation of only a few residues in the region connecting the two domains. As in all subsequent structural figures, the coordinates for the protein structures were obtained from the protein database.

Citation: Krewulak K, Peacock R, Vogel H. 2004. Periplasmic Binding Proteins Involved in Bacterial Iron Uptake, p 113-132. In Crosa J, Mey A, Payne S, Iron Transport in Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555816544.ch8
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Image of FIGURE 3
FIGURE 3

Conformational change of FbpA on ligand binding. Fe-free FbpA, (A) and Fe3_-bound FbpA (B) are shown. The most dramatic difference on binding of Fe is a 21° rotation about a central β-sheet hinge that separates the two structural domains. The same structure is seen for the C-terminal domain in both the apo and holo forms of FbpA. Some reorganization of key residues in the N-terminal domain occurs on iron binding.

Citation: Krewulak K, Peacock R, Vogel H. 2004. Periplasmic Binding Proteins Involved in Bacterial Iron Uptake, p 113-132. In Crosa J, Mey A, Payne S, Iron Transport in Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555816544.ch8
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Image of FIGURE 4
FIGURE 4

Comparison of Fe binding sites of FbpA (A) and the N lobe of lactoferrin (B). Similar ligands coordinate the Feion in each binding site. As in the transferrin superfamily, six ligands coordinate the Feion in FbpA. FbpA contributes two oxygen ligands from Tyr195 and Tyr196, a carboxylate ion ligand from Glu57, and an imidazole nitrogen ligand from His9. A water molecule and a phosphate ion contribute the two remaining oxygen ligands, thus fulfilling the octahedral geometry preferred by Fe.

Citation: Krewulak K, Peacock R, Vogel H. 2004. Periplasmic Binding Proteins Involved in Bacterial Iron Uptake, p 113-132. In Crosa J, Mey A, Payne S, Iron Transport in Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555816544.ch8
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Image of FIGURE 5
FIGURE 5

Ribbon representation of Zn(II)-bound (A) and Zn(II)-free (B) TroA. On binding Zn(II), TroA adopts a more open conformation due to a 4° tilt of the C-terminal domain. Two C-terminal domain loops collapse into the Zn(II) binding cavity, thus decreasing the cavity volume from 97.2 to 59.3Å. The α-helix that connects the two domains of TroA is structurally different from the typical β-strands that connect two domains in non-metal-binding PBPs. The poorly flexible helix may explain why ligand binding and release by TroA differs from the Venus flytrap mechanism seen in other PBPs.

Citation: Krewulak K, Peacock R, Vogel H. 2004. Periplasmic Binding Proteins Involved in Bacterial Iron Uptake, p 113-132. In Crosa J, Mey A, Payne S, Iron Transport in Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555816544.ch8
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Image of FIGURE 6
FIGURE 6

Overview of the ferric siderophore transport pathway for gram-negative bacteria. Siderophores secreted from bacteria chelate iron from host proteins (e.g., TF, LF, and heme proteins) or the environment (e.g., free iron or iron hydroxide precipitates). These ferric siderophores are transported through specific outer membrane receptors into the periplasmic space. A periplasmic protein carries the ferric siderophore across the periplasm to an inner membrane receptor. With the assistance of an associated ATPase protein, the intact ferric siderophore is transported through this receptor into the cytoplasm, and iron is released for bacterial survival.

Citation: Krewulak K, Peacock R, Vogel H. 2004. Periplasmic Binding Proteins Involved in Bacterial Iron Uptake, p 113-132. In Crosa J, Mey A, Payne S, Iron Transport in Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555816544.ch8
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Image of FIGURE 7
FIGURE 7

Clustering of selected PBPs from cluster 1 iron binding proteins and cluster 8 and cluster 9 proteins. A dendrogram of a selection of proteins thought to be members of the FBP family or of the cluster 8 or cluster 9 families of PBPs is shown. Within cluster 8 and cluster 9, the sequence identities between proteins is often very low—around 10%. In general, the proteins cluster into the families that they should, although ZnuA and TroA are comparatively homologous to some of the cluster 8 proteins. Notice that two FBPs cluster almost as well with the cluster 8 proteins as with the other FBPs in cluster 1. This may simply be a case of incorrect annotation in sequencing projects. Abbreviations: Aac, ; Bsu, ; Bha, ; Bja, ; Cje, ; Eco, ; Hin, ; Lmo, ; Mha, ; Mlo, ; Mmo, ; Mtu, , Nme, ; Ngo, ; Pae, ; Pmu, ; Sau, ; Sgo, ; Sma, ; Smu, ; Spa, ; Spn, ; Spy, ; Syn, sp.; Tpa, ; Van, ; Vch, ; Yen, ; Ype, .

Citation: Krewulak K, Peacock R, Vogel H. 2004. Periplasmic Binding Proteins Involved in Bacterial Iron Uptake, p 113-132. In Crosa J, Mey A, Payne S, Iron Transport in Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555816544.ch8
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Image of FIGURE 8
FIGURE 8

Chemical structures of various hydroxamate-type siderophores. The chemical structures of albomycin (a), coprogen (b), and Desferal (c) are shown with FhuD side chain residues. Interactions are indicated by dotted lines (distance indicated). Reprinted from Clarke, Braun, et al. (2002) with permission from the publisher.

Citation: Krewulak K, Peacock R, Vogel H. 2004. Periplasmic Binding Proteins Involved in Bacterial Iron Uptake, p 113-132. In Crosa J, Mey A, Payne S, Iron Transport in Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555816544.ch8
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Image of FIGURE 9
FIGURE 9

Structures of FhuD bound to gallichrome (A) and BtuF bound to vitamin B12 (B). Although these two proteins have little sequence homology, they have a surprisingly similar fold. Both have two topologically similar domains consisting of a central five-strand β- sheet surrounded by helices. The domains are connected by an α-helix that spans the length of the protein. A similar fold is seen in the TroA and PsaA proteins (discussed in the text) from cluster 9.

Citation: Krewulak K, Peacock R, Vogel H. 2004. Periplasmic Binding Proteins Involved in Bacterial Iron Uptake, p 113-132. In Crosa J, Mey A, Payne S, Iron Transport in Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555816544.ch8
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Image of FIGURE 10
FIGURE 10

Space-filling models of FhuD bound to various hydroxamate siderophores. FhuD bound to gallichrome (A), albomycin (B), coprogen (C), and desferal (D) is shown. Although these hydroxamatetype siderophores are structurally different, all are transported by the same periplasmic protein, FhuD.

Citation: Krewulak K, Peacock R, Vogel H. 2004. Periplasmic Binding Proteins Involved in Bacterial Iron Uptake, p 113-132. In Crosa J, Mey A, Payne S, Iron Transport in Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555816544.ch8
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Image of FIGURE 11
FIGURE 11

Proposed interaction of FhuD with its ABC transporter, FhuBC. The negatively charged Glu-111 and Asp- 225 on the apex of each lobe of FhuD (shown in ball-and-stick) can potentially interact with the positively charged arginine pockets of FhuB (shown in ball-andstick), revealing a path for transport of ferrichrome from FhuD to the cytoplasm. The FhuBC structure is a homology model made by using the BtuCD crystal structure as a template.

Citation: Krewulak K, Peacock R, Vogel H. 2004. Periplasmic Binding Proteins Involved in Bacterial Iron Uptake, p 113-132. In Crosa J, Mey A, Payne S, Iron Transport in Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555816544.ch8
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Image of FIGURE 12
FIGURE 12

Comparison of the binding modes of albomycin in FhuA (A) and FhuD (B). The hydrogen bonds from the side chain residues to albomycin are shown. It can be seen that FhuA interacts with the antibiotic portion of albomycin but FhuD does not. Reprinted from Clarke, Braun, et al. (2002) with permission from the publisher.

Citation: Krewulak K, Peacock R, Vogel H. 2004. Periplasmic Binding Proteins Involved in Bacterial Iron Uptake, p 113-132. In Crosa J, Mey A, Payne S, Iron Transport in Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555816544.ch8
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Tables

Generic image for table
TABLE 1

The nine PBP clusters

Citation: Krewulak K, Peacock R, Vogel H. 2004. Periplasmic Binding Proteins Involved in Bacterial Iron Uptake, p 113-132. In Crosa J, Mey A, Payne S, Iron Transport in Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555816544.ch8

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