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Chapter 7 : Making, Breaking, and Sensing of Cyclic Di-GMP: Structural, Thermodynamic, and Evolutionary Principles

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Abstract:

This chapter begins with a discussion on a cyclic-di-GMP (c-di-GMP), a self-associating messenger molecule. The proteins involved in c-di-GMP formation, recognition, and degradation are drawn primarily from large gene families which have multiple representatives encoded by most bacterial genomes. Degradation of c-di-GMP is mediated by two families of specific PDEs called EAL and HDGYP proteins based on a stereotyped amino acid sequence and these proteins once again have a broad and frequently redundant phylogenetic distribution. motif present in their active sites. The chapter focuses on the EAL proteins that are most abundant and structurally best characterized. The exact separation between the c-di-GMP switch and the N-terminal β-strand of the PilZ domain varies in different family members, as does the conformation of this β-strand in some family members, which enables the switch to effect distinct changes in interdomain interactions in different PilZ domain-containing receptors. Ironically, neither the PilZ protein nor the XC1028 protein binds c-di-GMP in biochemical assays, and the structure of XC1028 does not contain either c-di-GMP binding motif described. Nuclear magnetic resonance (NMR) spectroscopy was used to determine the structure of PA4608 from , which provided the first view of PilZ domain architecture. c-di-GMP is an exquisite multivalent molecule that can immobilize disordered protein segments or change the relative orientation of protein domains.

Citation: Kim D, Hunt J, Schirmer T. 2010. Making, Breaking, and Sensing of Cyclic Di-GMP: Structural, Thermodynamic, and Evolutionary Principles, p 76-95. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch7

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Figures

Image of Figure 1.
Figure 1.

Cyclic di-GMP. (A) Chemical structure. (B) Crystal structure ( ) showing a dimer with intercalated bases. The same arrangement has been found in complex with PleD (PDB codes 1w25 and 2v0n) and WspR (3bre). (C) Molecular surfaces of the c-di-GMP monomer and dimer, shaded as in panel B.

Citation: Kim D, Hunt J, Schirmer T. 2010. Making, Breaking, and Sensing of Cyclic Di-GMP: Structural, Thermodynamic, and Evolutionary Principles, p 76-95. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch7
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Image of Figure 2.
Figure 2.

Concentration of c-di-GMP monomer and dimer as a function of total c-di-GMP concentration, expressed as a ratio relative to the for dimerization. Note that is not yet known, although it is likely to be in the micromolar range at physiological salt concentration. Given a reversible dimerization reaction (2 monomers ↔ dimer) and defining = [monomer]/[dimer], the monomer concentration is given by [monomer]/ (–1 + (1 + 8[c-di-GMP]/K))/4, while the dimer concentration is given by [dimer]/ = [monomer]/K

Citation: Kim D, Hunt J, Schirmer T. 2010. Making, Breaking, and Sensing of Cyclic Di-GMP: Structural, Thermodynamic, and Evolutionary Principles, p 76-95. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch7
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Image of Figure 3.
Figure 3.

Schematic diagrams illustrating the modulation of interdomain interactions by c-di-GMP binding to representative DGC proteins (top) or PilZ receptors (bottom). Domain nomenclature is explained in the text.

Citation: Kim D, Hunt J, Schirmer T. 2010. Making, Breaking, and Sensing of Cyclic Di-GMP: Structural, Thermodynamic, and Evolutionary Principles, p 76-95. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch7
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Image of Figure 4.
Figure 4.

Structure of PleD from (A) Native PleD ( ). Loose dimer contacts are mediated by the Rec and Rec′ domains to form the stem at the bottom. The active sites (A-site) of the two GGDEF domains (top) are well separated. (B) BeF3-activated PleD ( ). Note that the stem is tightened up due to the modification at the P-sites (Asp53). The GGDEF domains are in a different orientation with respect to the stem compared to native PleD (panel A). (C) Model of the catalytically competent GGDEF dimer constellation with GTP bound to each domain. View along molecular twofold with the stem (not shown) beneath the projection plane. Figure reprinted from reference with permission.

Citation: Kim D, Hunt J, Schirmer T. 2010. Making, Breaking, and Sensing of Cyclic Di-GMP: Structural, Thermodynamic, and Evolutionary Principles, p 76-95. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch7
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Image of Figure 5.
Figure 5.

Schematic scheme of PleD catalysis and regulation, adapted from reference . (Upper row) The three-domain (Rec-Rec′ -GGDEF) protein is monomeric in solution (left). Dimerization via the Rec-Rec′ stem is induced upon phosphorylation of the Rec domains, allowing formation of the catalytically competent GGDEF dimer ( Fig. 4C ) to catalyze formation of two symmetric phosphodiester bonds between two GTP (G-R-P-P-P) molecules (right). (Lower row) Binding of (c-di-GMP) to PleD causes either GGDEF-Rec′ (left, 1w25) or GGDEF-GGDEF cross-linking (right, 2v0n) and prevents encounter of the active sites, shown here with bound GTP.

Citation: Kim D, Hunt J, Schirmer T. 2010. Making, Breaking, and Sensing of Cyclic Di-GMP: Structural, Thermodynamic, and Evolutionary Principles, p 76-95. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch7
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Image of Figure 6.
Figure 6.

Crystal structure of WspR from ( ) (3bre). (A) Two dimers (ribbon and thin line representation, respectively) are related by a twofold symmetry axis that runs approximately along the viewing direction. The common twofold axis of the dimers is oriented vertically. Each protomer is composed of a Rec and a GGDEF domain. The Rec domains maintain the intradimeric contact, whereas the two dimers are joined together by four (c-di-GMP) molecules (shown in full and marked with asterisks), each cross-linking an Ip-site with Arg198 of an adjacent dimer. (B) Schematic representation of the WspR tetramer and the elongated dimer proposed to represent the inhibited state ( ).

Citation: Kim D, Hunt J, Schirmer T. 2010. Making, Breaking, and Sensing of Cyclic Di-GMP: Structural, Thermodynamic, and Evolutionary Principles, p 76-95. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch7
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Image of Figure 7.
Figure 7.

Crystal structures of EAL proteins in complex with c-di-GMP. (A) Ribbon diagram of the BLUF-EAL PDE BlrP1 from ( ) (3gfz). The two chains of the homodimer are drawn in light and dark grey. The molecular twofold symmetry axis is oriented vertically. The c-di-GMP molecules bound to the EAL domain and the flavin mononucleotide (FMN) chromophore bound to the BLUF domain are drawn as van der Waals spheres. (B) Detailed view of the active site with bound c-di-GMP, Mn ions (metals M1 and M2), and active site residues shown in full. Also shown is the water (Wat) molecule (small sphere) that is coordinated by both metal ions and well positioned for nucleophilic attack on the phosphorus in line with the scissile phosphodiester bond (approximately vertical). (C) Ribbon diagram of the EAL-PAS protein YkuI from ( ) (2w27). Representation is as described for panel A.

Citation: Kim D, Hunt J, Schirmer T. 2010. Making, Breaking, and Sensing of Cyclic Di-GMP: Structural, Thermodynamic, and Evolutionary Principles, p 76-95. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch7
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Image of Figure 8.
Figure 8.

Crystallographic studies show a large conformation change in PlzD upon c-di-GMP binding (PDB code 2rde). The PlzD protein from has an N-terminal YcgR-N* domain fused to a C-terminal PilZ domain (PDB no. 1YLN) ( ). Although there is no significant sequence similarity between them, both domains form structurally homologous six-stranded β-barrels. (A) The structure (i.e., in the absence of c-di-GMP, PDB code 1YLN) shows no contacts between the YcgR-N* and PilZ domains in each protomer because the c-di-GMP switch that links them adopts an extended conformation. (B) c-di-GMP binding produces a 123° rotation of each PilZ domain toward the YcgR-N* in the same protomer. The c-di-GMP molecule is sandwiched between the two domains and held into place by contacts from the c-di-GMP switch as well as conserved residues in the β-barrel core of the PilZ domain. (C) Superposition of the (dark) and c-di-GMP-bound (light) structures based on least-squares alignments of the YcgR-N* domains.

Citation: Kim D, Hunt J, Schirmer T. 2010. Making, Breaking, and Sensing of Cyclic Di-GMP: Structural, Thermodynamic, and Evolutionary Principles, p 76-95. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch7
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Image of Figure 9.
Figure 9.

A cooperative hydrogen-bonding network stabilizes c-di-GMP in the binding pocket of PlzD (PDB code 2rde). The c-di-GMP binding pocket in PlzD is formed by the c-di-GMP switch (residues 134 to 140) and several β-strands containing residues conserved in PilZ domains (residues 162 to 170 and 219 to 221) ( ). A single c-di-GMP molecule (black) binds in a conformation with its two guanine bases stacked parallel to one another. (A) The invariant arginine residues in the c-di-GMP switch make critical interactions with the ligand. Arg136 contacts the guanine base, while Arg140 hydrogen bonds with one of the phosphate groups and simultaneously makes π-π interactions with one base. The other guanine base is stabilized by hydrogen bonds to residues Asp162 and Ser164 in the dΦSXXG motif, while the Cα of Gly167 in this motif contacts its surface. This base and a backbone phosphate group are contacted by Asn208, a residue present in VCA0042 and a minor fraction of other PilZ domains ( ). (B) Comparison of the (dark grey) and c-di-GMP-bound (light grey) structures shows the conformational change in the c-di-GMP switch, which moves the core of the PilZ domain and the other key elements of the binding pocket away from the YcgR-N* domain. The conformation of the switch in the state is clearly incompatible with c-di-GMP binding.

Citation: Kim D, Hunt J, Schirmer T. 2010. Making, Breaking, and Sensing of Cyclic Di-GMP: Structural, Thermodynamic, and Evolutionary Principles, p 76-95. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch7
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Image of Figure 10.
Figure 10.

Binding mode of monomeric c-di-GMP to PlzD (left) (PDB code 2rde) and of a self-intercalated c-di-GMP dimer to the allosteric inhibition site of PleD (right) (PDB code 2v0n). In each case, two arginine side chains (PlzD, R136 and R140; PleD, R313′ and R359) extend at right angles and are involved in ligand binding. H-bonds between the guanidino groups and the O-6, N-7 (non-Watson-Crick) edge of the guanyl bases are shown as dashed lines.

Citation: Kim D, Hunt J, Schirmer T. 2010. Making, Breaking, and Sensing of Cyclic Di-GMP: Structural, Thermodynamic, and Evolutionary Principles, p 76-95. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch7
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Image of Figure 11.
Figure 11.

Structural divergence near the c-di-GMP switch in PP4397. Superposition of protomers from the crystal structures of PP4397 (black, PDB code 2rde) and PlzD (gray, PDB code 2GJG) based on least-squares alignment of their N-terminal YcgR-N* domains. The PP4397 protein contains an N-terminal YcgR-N* domain and a C-terminal PilZ domain, both of which show strong structural homology to the corresponding domains in PlzD. However, PP4397 has an eight-residue insertion between the core of the PilZ domain and the c-di-GMP switch. The interdomain geometry in PP4397 is dramatically different, and its c-di-GMP switch adopts a different conformation in the absence of c-di-GMP (i.e., an α-helix in PP4397 versus an unstructured loop in PlzD).

Citation: Kim D, Hunt J, Schirmer T. 2010. Making, Breaking, and Sensing of Cyclic Di-GMP: Structural, Thermodynamic, and Evolutionary Principles, p 76-95. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch7
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Tables

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Table 1

Structures of representative c-di-GMP-related proteins

Citation: Kim D, Hunt J, Schirmer T. 2010. Making, Breaking, and Sensing of Cyclic Di-GMP: Structural, Thermodynamic, and Evolutionary Principles, p 76-95. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch7

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