Formation of a Distinctive Complex between the Inducible Bacterial Lysine Decarboxylase and a Novel AAA+ ATPase

Snider, Jamie; Gutsche, Irina; Lin, Michelle I.; Baby, Sabulal; Cox, Brian; Butland, Gareth; Greenblatt, Jack; Emili, Andrew; Houry, Walid

doi:10.1074/jbc.m511172200

Cited by 54 publications

(127 citation statements)

References 67 publications

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“…However, how these proteins act is not clear. In Escherichia coli, the ravA gene is in an operon with another gene of unknown function, which we termed viaA, and the operon is under the control of σ S promoter, suggesting a function of RavA and ViaA under stress conditions (12). This is further substantiated by our discovery that RavA physically interacts with the inducible lysine decarboxylase enzyme, LdcI/CadA, a key enzyme in the bacterial acid stress response.…”

supporting

confidence: 51%

“…This is further substantiated by our discovery that RavA physically interacts with the inducible lysine decarboxylase enzyme, LdcI/CadA, a key enzyme in the bacterial acid stress response. We have visualized the LdcI-RavA complex by negative staining electron microscopy and found it to form a large, about 3.3 MDa, unusual cagelike structure consisting of two LdcI decamers that are linked by up to five RavA hexamers (12). Because LdcI is fivefold symmetric whereas RavA is sixfold symmetric, understanding the construction of this complex is important to understanding how the symmetry mismatch was used in forming the cage-like structure.…”

mentioning

confidence: 99%

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Structure of RavA MoxR AAA+ protein reveals the design principles of a molecular cage modulating the inducible lysine decarboxylase activity

Bakkouri

Gutsche

Kanjee

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

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The MoxR family of AAA+ ATPases is widespread throughout bacteria and archaea but remains poorly characterized. We recently found that the Escherichia coli MoxR protein, RavA (Regulatory ATPase variant A), tightly interacts with the inducible lysine decarboxylase, LdcI/CadA, to form a unique cage-like structure. Here, we present the X-ray structure of RavA and show that the αβα and all-α subdomains in the RavA AAA+ module are arranged as in magnesium chelatases rather than as in classical AAA+ proteins. RavA structure also contains a discontinuous triple-helical domain as well as a β-barrel-like domain forming a unique fold, which we termed the LARA domain. The LARA domain was found to mediate the interaction between RavA and LdcI. The RavA structure provides insights into how five RavA hexamers interact with two LdcI decamers to form the RavA-LdcI cage-like structure.acid stress | alarmone P roteins of the AAA+ superfamily (ATPases Associated with diverse cellular Activities) are highly ubiquitous and found in all kingdoms of life. These proteins are characterized by the structural conservation of a central ATPase domain of about 250 amino acids called the AAA+ module (1, 2). AAA+ ATPases employ the energy derived from ATP hydrolysis to remodel proteins, DNA, or RNA. Typically, the AAA+ domain can be divided into two structural subdomains, an N-terminal P-loop NTPase αβα subdomain that is connected to a smaller C-terminal all-α subdomain. The αβα subdomain adopts a Rossman fold and contains several motifs involved in ATP binding and hydrolysis, including Walker A, Walker B, and Sensor 1 signature sequences (3-6). The all-α subdomain, which contains the Sensor 2 motif (7), is much less conserved across AAA+ proteins.AAA+ proteins form oligomers, usually hexameric rings, in the presence of nucleotides (8). The ATP-binding pocket is located at the interface between two neighboring subunits. A highly conserved arginine from one subunit, called an "arginine finger," contacts the γ-phosphate of bound ATP of the neighboring subunit (9). AAA+ proteins typically go through a cycle of ATP binding, hydrolysis, and release of products. This reaction cycle results in a series of conformational changes and mechanical movements that allow these proteins to exert their activity either directly or through domains attached to the AAA+ domain (3, 10).The RavA protein (Regulatory ATPase Variant A) belongs to the MoxR AAA+ family (11). Limited experimental data suggest a function of MoxR AAA+ proteins as chaperones in the assembly of multimeric complexes and a possible role in small molecule cofactor insertion/removal (11). However, how these proteins act is not clear. In Escherichia coli, the ravA gene is in an operon with another gene of unknown function, which we termed viaA, and the operon is under the control of σ S promoter, suggesting a function of RavA and ViaA under stress conditions (12). This is further substantiated by our discovery that RavA physically interacts with the inducible lysine decarboxylase enzyme, LdcI/CadA...

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supporting

confidence: 51%

mentioning

confidence: 99%

Structure of RavA MoxR AAA+ protein reveals the design principles of a molecular cage modulating the inducible lysine decarboxylase activity

Bakkouri

Gutsche

Kanjee

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

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“…Adjacent to these genes are the genes/operons yohO, osmF-yehYXW, yehR, and yehLMPQ. yehL encodes a putative ATP-binding subunit of the ABC transporter family (56); yohO encodes a small membrane protein (27); and the product of the osmF-yehYXW operon is a putative ABC transporter (13). Thus far, no functions are predicted for the products of yehM, yehP, yehQ, or yehR.…”

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confidence: 99%

First Insights into the Unexplored Two-Component System YehU/YehT in Escherichia coli

et al. 2012

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“…Many sequences and motifs characteristic of RavA proteins are present in p618, including a conserved tryptophan or phenylalanine residue within the Walker B motif and a preceding Leu-Pro sequence of unknown function. Moreover, the more commonly used glycine residue in the Walker A sequence is replaced by an alanine, as occurs in RavA (25) (Fig. 1B).…”

Section: Resultsmentioning

confidence: 99%

“…Genes for the two proteins often form an operon, and sometimes the AAA and VWA protein domains are fused. RavA, the closest homolog to p618, interacts with the VWA domain-containing protein ViaA (25). The gene for p618 lies close to that for the VWA domaincontaining protein p892.…”

Section: Discussionmentioning

confidence: 99%

Chaperone Role for Proteins p618 and p892 in the Extracellular Tail Development of Acidianus Two-Tailed Virus

Scheele

Erdmann

Ungewickell

et al. 2011

J Virol

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The crenarchaeal Acidianus two-tailed virus (ATV) undergoes a remarkable morphological development, extracellularly and independently of host cells, by growing long tails at each end of a spindle-shaped virus particle. Initial work suggested that an intermediate filament-like protein, p800, is involved in this process. We propose that an additional chaperone system is required, consisting of a MoxR-type AAA ATPase (p618) and a von Willebrand domain A (VWA)-containing cochaperone, p892. Both proteins are absent from the other known bicaudavirus, STSV1, which develops a single tail intracellularly. p618 exhibits ATPase activity and forms a hexameric ring complex that closely resembles the oligomeric complex of the MoxR-like protein RavA (YieN). ATV proteins p387, p653, p800, and p892 interact with p618, and with the exception of p800, all bind to DNA. A model is proposed to rationalize the interactions observed between the different protein and DNA components and to explain their possible structural and functional roles in extracellular tail development.Acidianus two-tailed virus (ATV) is a member of the crenarchaeal Bicaudaviridae family that was isolated at Pozzuoli, Italy, from a hot, acidic spring with temperatures of 85°C to 93°C and a pH of 1.5, conditions under which its host, Acidianus convivator, grows optimally (13, 23). The only other characterized bicaudavirus is the Sulfolobus tengchongensis spindleshaped virus, STSV1, which shares a similar morphology and some homologous proteins with ATV (31). Both viruses exhibit fusiform bodies with tails of variable length, at both ends for ATV and at one end for STSV1. ATV, in contrast to all other known viruses, including STSV1, undergoes an extracellular morphological transformation that is independent of host cells (13,23). Virus particles are released from the host as tail-less fusiform structures, and within an hour to a few days, depending on temperature conditions, two tails develop in an irreversible process (13). The only other known examples of extracellular viral morphogenesis comprise initial steps of infection or final steps in particle assembly and budding, and these are triggered on the cell surface of the host (2, 22). ATV tails are assumed to facilitate virion attachment to host cell walls or membranes under harsh environmental conditions where there is a low density of potential host cells (23).Exceptionally for a crenarchaeal virus, ATV shows both a lysogenic and a lytic reproduction cycle. Infection of host cells grown under optimal conditions results in lysogeny that can be interrupted and transformed into a lytic stage by environmental stress factors. For example, ATV propagation can be induced by lowering the culture temperature from 85°C to 75°C (23).ATV and STSV1 have circular double-stranded DNA genomes of 62,730 and 75,294 bp and contain 72 and 74 predicted open reading frames (ORFs), respectively. ATV virions carry at least 11 proteins, whereas STSV1 has only 5. In both virions, the homologous DNA-binding proteins p131 of ATV and p40 ...

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Formation of a Distinctive Complex between the Inducible Bacterial Lysine Decarboxylase and a Novel AAA+ ATPase

Cited by 54 publications

References 67 publications

Structure of RavA MoxR AAA+ protein reveals the design principles of a molecular cage modulating the inducible lysine decarboxylase activity

Structure of RavA MoxR AAA+ protein reveals the design principles of a molecular cage modulating the inducible lysine decarboxylase activity

First Insights into the Unexplored Two-Component System YehU/YehT in Escherichia coli

Chaperone Role for Proteins p618 and p892 in the Extracellular Tail Development of Acidianus Two-Tailed Virus

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