Heme-based NO sensors. HNOX: Heme-nitric oxide/oxygen binding domain/protein Bacterial
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1 Heme-based sensors HX: Heme-nitric oxide/oxygen binding domain/protein Bacterial 1
2 J. Inorg. Biochem. 99, 892 (2005). Soluble guanylate cyclase (sgc) is a nitric oxide () sensing hemoprotein that has been found in eukaryotes from Drosophila to humans. rokaryotic proteins with significant homology to the heme domain of sgc have recently been identified through genomic analysis. This family of heme proteins has been named the H-X domain, for Heme-itric oxide/xygen binding domain. The key observation from initial studies in this family is that some members, those proteins 2
3 3
4 [B] sensor protein - HnoX (4) HnoX SIGAL dissociation Fe histidine kinase HnoK HnoC, HnoD or HnoB response regulators tidine kinase AT autophosphorylation phosphotransfer UUT regulation of transcription or catalytic activity HqsK LuxU Lux tidine kinase AT autophosphorylation tidine kinase AT phosphotransfer UTUT regulation of transcription Fig. 4 4
5 IUT (signal) Binding of signal molecules hosphorylation Ion binding DA binding Light hosphodiesterase H 2 H H H H c-di GM H H H 2 Sessility (biofilm formation) Fimbrial formation Virulence Environmental persistence Cell-cell communication UTUT (phenotype) H 2 H UTUT (phenotype) H Motility Virulence hage resistance Hyphae formation Antibiotic production H H H H H pgpg or l-di GM H 2 H H H H 2 H H Fig. 7 H H H H GT H H H Diguanylate cyclase H H H H 2 IUT (signal) Binding of signal molecules hosphorylation Ion binding DA binding 5 Light
6 CqsS Lux LuxQ Lux LuxU histidine kinase AT HqsK HqsK AT AD DGC HnoX Fe E AT AD HnoK HnoK Hpt HnoC HnoB E Fur transcriptional feedback AD response regulator? 2 GT c-digm l-digm Fig. 10 HnoD DGC 6
7 The Marletta Lab. Univ. California, Berkeley, Script Research Institute Genomic analysis has recently placed sgc within a larger family of proteins with Heme itric oxide/xygen binding (H-X) domains including prokaryotic proteins with significant homology (15-40% identity) to the heme domain of sgc. redicted H-X domains were found in facultative aerobes, obligate anaerobes, and thermophiles. Genomic analysis reveals that the H-X domains may be linked to histidine kinases or diguanylate cyclases (obligate anaerobes) or methyl-accepting chemotaxis proteins (obligate anaerobes). Uncovering the biological function of these H-X domains is currently an area of intense investigation in our lab. (A) Structural features of Tt H-X. (B) Heme binding pocket.h-x proteins also exhibit remarkable diatomic ligand selectivity despite a similar protein fold. For example, the H-X domain from Vibrio cholera (a facultative aerobe) binds in a high spin 5-coordinate complex and excludes oxygen, while the H-X domain from Thermoanaerobacter tengcongensis (Tt, obligate anaerobe) has been found to bind oxygen in a low-spin 6-coordinate complex, making it the first member of the family to bind 2. Current research is focused on understanding the nature of this ligand selectivity from a molecular level and how this selectivity translates into protein function as sensors in biology. 7
8 Fig. 2. Sequence alignment selected members of the H-X family. Sequence numbering is that of Tt H-X. Invariant residues are highlighted in green and very highly conserved residues are highlighted in blue. Y140 of Tt H-X is highlighted in red. redicted distal pocket tyrosine residues that may stabilize an Fe II 2 complex in other H- X proteins are in red. Accession numbers are: Homo sapiens β1 [gi: ], Rattus norvegicus β1 [gi: ], Drosophila melangaster β1 [gi:861203], Drosophila melangaster CG14885-A [gi: ], Caenorhabditis elegans GCY-35 [gi: ], ostoc punctiforme [gi: ], Caulobacter crescentus [gi: ], Shewanella oneidensis [gi: ], Legionella pneumophila (RF2) [CUCGC_272624], Clostridium acetobutylicum [gi: ], and Thermoanaerobacter tengcongensis [gi: ]. Alignments were generated using the program MegAlign. 8
9 Fig. 3. Speculation on prokaryotic signaling pathways involving H-X domains. (a) roposed role of an H-X sensor in a facultative aerobic bacterium. The H-X domains in facultative aerobes may have evolved as sensors for derived from under conditions of low 2 concentration. The signal may be transmitted via the action of a histidine kinase. Most of the predicted H-X RFs from aerobic bacteria are contained within an operons that also contains a predicted histidine kinase, and additionally, these bacteria also contain predicted nitrate reductase proteins, consistent with this hypothesis. (b) roposed role of an H-X sensor in an obligate anaerobic bacterium. The H-X domain in obligate anaerobes is fused through a transmembrane domain (shown in gray) to a MC. Here the H-X domain may be used as an 2 sensor to signal a change in 2 concentration, regulating methylation by S-adenosyl-methionine (SAM) leading to taxis towards more favorable 2 concentrations. Aside from binding to the H-X domain of sgc, ligand binding to an H-X protein has not been conclusively linked to biological signaling processes to date. 9
10 Fig. 4. The heme environment of the Tt H-X domain[38]. (a) The conserved Y-S-R motif makes hydrogen bonding interactions with the propionic acid side chains of the heme group, which is colored yellow (porphyrin) and red (iron). (b) The conserved H102 is the proximal ligand to the heme. In Tt H-X, a distal pocket hydrogen-bonding network, involving principally Y140, stabilizes an Fe II 2 complex. This hydrogen-bonding network is predicted to be absent in the H-X proteins from sgcs and aerobic prokaryotes, suggesting this as a key molecular factor in the remarkable ligand selectivity against 2 displayed by these heme proteins. 10
11 Fig. 5. Schematic summary of the H-X family of heme-based sensors. The progenitor H-X domain has evolved to discriminate between ligands such as and 2 for specific sensing purposes. This is the first family of related heme proteins to discriminate between different physiologically relevant diatomic gaseous ligands. 11
12 Mol. Cell 46 (4) 449 (2012) Highlights A complex multicomponent bacterial H-X signaling network was mapped EAL response regulator phosphorylation stimulated c-di-gm hydrolysis activity A degenerate HD-GY response regulator inhibited the EAL response regulator induced biofilm formation through c-di-gm modulation by the signaling network 12
13 Figure 6. Model of Multicomponent Signaling etwork for -Induced Biofilm Formation as a rotection Mechanism against (A) The complex multicomponent signaling pathway is initiated by binding to the sensory H-X protein (HnoX), which then inhibits HnoK autophosphorylation. hosphotransfer establishes a branching of the network to three response regulators. HnoB and HnoD form a feed-forward loop. hosphorylation controls DE activity of HnoB, which can be finetuned by allosteric control from HnoD. -controlled repression of the DE activity leads to an increase in c-di-gm levels, which serves as a signaling cue for cellular attachment into biofilms.(b) The signal switches the bacterial motility pattern from planktonic growth to increased attachment onto surfaces. The thick layers of cells provide a protective barrier against diffusion of reactive and damaging and may protect cells in the lower 13 layers.
The official electronic file of this thesis or dissertation is maintained by the University Libraries on behalf of The Graduate School at Stony Brook
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