EscC is a chaperone for the Edwardsiella tarda type III secretion system putative translocon components EseB and EseD

Zheng, Jun; Li, Nan; Tan, Yee Pin; Sivaraman, J.; Mok, Yu Keung; Mo, Zhao Lan; Leung, Ka Yin

doi:10.1099/mic.0.2006/004952-0

Microbiology

2007

DOI: 10.1099/mic.0.2006/004952-0

|View full text |Cite

EscC is a chaperone for the Edwardsiella tarda type III secretion system putative translocon components EseB and EseD

Jun Zheng

Nan Li

Yee Pin Tan

et al.

Help me understand this report

Search citation statements

Order By: Relevance

Paper Sections

Select...

Citation Types

Supporting

Mentioning

Contrasting

Year Published

2007

2016

Publication Types

Select...

Article8

Relationship

Self Cite1

Independent7

Authors

Journals

Cited by 31 publications

(24 citation statements)

References 52 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…While a putative effector gene called eseE has been identified through sequence analysis of the E. tarda T3SS (6), its function remains elusive (16). In the present study, EseE is found to be another chaperone for EseC.…”

mentioning

confidence: 60%

“…SseB, SseC, and SseD, secreted by a T3SS called Salmonella pathogenicity island 2 (SPI-2), predominantly assemble into a large complex, SseBCD, that functions as a translocon to deliver effectors into host cells (15). Similarly, EseB, EseC, and EseD can form a large protein complex, EseBCD, suggesting that they are also translocon components (16). Mutation of eseB, eseC, or eseD leads to reduced bacterial survival and growth in fish phagocytes, as well as increased 50% lethal dose (LD 50 ) values in blue gourami fish.…”

mentioning

confidence: 99%

“…EscA is the chaperone for EseC, whereas EscC is the chaperone for EseB and EseD. Both EscA and EscC prevent the degradation of their target substrates (16,19). EscB, the chaperone for EseG, is required for intracellular EseG stability (17).…”

mentioning

confidence: 99%

See 2 more Smart Citations

EseE of Edwardsiella tarda Augments Secretion of Translocon Protein EseC and Expression of the escC - eseE Operon

et al. 2016

View full text Add to dashboard Cite

Edwardsiella tarda is an important Gram-negative pathogen that employs a type III secretion system (T3SS) to deliver effectors into host cells to facilitate bacterial survival and replication. These effectors are translocated into host cells through a translocon complex composed of three secreted proteins, namely, EseB, EseC, and EseD. The secretion of EseB and EseD requires a chaperone protein called EscC, whereas the secretion of EseC requires the chaperone EscA. In this study, we identified a novel protein (EseE) that also regulates the secretion of EseC. An eseE deletion mutant secreted much less EseC into supernatants, accompanied by increased EseC levels within bacterial cells. We also demonstrated that EseE interacted directly with EseC in a pulldown assay. Interestingly, EseC, EseE, and EscA were able to form a ternary complex, as revealed by pulldown and gel filtration assays. Of particular importance, the deletion of eseE resulted in decreased levels of EseB and EseD proteins in both the bacterial pellet and supernatant fraction. Furthermore, real-time PCR assays showed that EseE positively regulated the transcription of the translocon operon escC-eseE, comprising escC, eseB, escA, eseC, eseD, and eseE. These effects of EseE on the translocon components/operon appeared to have a functional consequence, since the ⌬eseE strain was outcompeted by wild-type E. tarda in a mixed infection in blue gourami fish. Collectively, our results demonstrate that EseE not only functions as a chaperone for EseC but also acts as a positive regulator controlling the expression of the translocon operon escC-eseE, thus contributing to the pathogenesis of E. tarda in fish.T he type III secretion system (T3SS) is a contact-dependent translocation system. It forms a syringe-like structure spanning the inner and outer membranes of bacteria and induces pore formation on host cells (1). Through these pores, an array of bacterial proteins (effectors) are delivered into host cells, where they manipulate host cell signaling pathways to promote bacterial survival (2).Edwardsiella tarda is a Gram-negative intracellular pathogen that can cause hemorrhagic septicemia in fish (3), as well as gastroand extraintestinal infections in humans (4, 5). The T3SS is well known to be one of the most important virulence factors in E. tarda (6, 7). It facilitates the survival and replication of E. tarda in host cells (6-9). E. tarda T3SS contains 34 open reading frames (ORFs), which encode the apparatus, chaperones, effectors, and regulators (6, 10). The expression of E. tarda T3SS is controlled by many factors, such as the two-component system esrA-esrB (6) and esrC (11) inside the T3SS gene cluster, as well as phoP-phoQ (12) and phoR-phoB (13) located outside the T3SS gene cluster. Intriguingly, our group recently showed that a type III secretion system-secreted protein (EscE) also functions as a regulator controlling the injection of effectors and secretion of translocators (14).EseB, EseC, and EseD, secreted by the E. tarda T3SS, are homologous ...

show abstract

mentioning

confidence: 60%

mentioning

confidence: 99%

See 1 more Smart Citation

EseE of Edwardsiella tarda Augments Secretion of Translocon Protein EseC and Expression of the escC - eseE Operon

et al. 2016

View full text Add to dashboard Cite

show abstract

“…In Salmonella, similar observations are reported where the sseC mutant causes downregulation of the expression of SseD and the sseD mutant results in the down-regulation of SseC (Chakravortty et al 2005). However, we cannot rule out the possibility that disappearance of the secretion of the 55 kDa protein (EseC) may also be due to polar effects on the 25 kDa protein (EseB) since the eseC gene is located downstream of the eseB gene (Tan et al 2005), and in another report, the deletion mutant of ΔeseB in a different strain did not affect the secretion of EseC and EseD (Zheng et al 2007). On the other hand, the eseC gene is located upstream of the eseD gene (Tan et al 2005); therefore, the observation of reduced secretion of the 55 kDa protein (EseC) may not be due to polar effects on the 22 kDa protein (EseD), but may be similar to the observation reported previously, where, in Salmonella, the sseD mutant results in the down-regulation of SseC (Chakravortty et al 2005).…”

mentioning

confidence: 99%

Characterization of proteins secreted from a Type III secretion system of Edwardsiella tarda and their roles in macrophage infection

Okuda¹,

Kiriyama²,

Suzaki³

et al. 2009

Dis. Aquat. Org.

View full text Add to dashboard Cite

The Type III secretion system is essential for intracellular replication of Edwardsiella tarda in phagocytes of fish and mammals. We identified the secreted proteins of the Type III secretion system by comparing the wild-type strain and the Type III mutant mET1229. The wild-type strain secreted 55, 25, and 22 kDa proteins into the culture supernatant, whereas the Type III mutant did not. These proteins were identified as EseB, EseC, and EseD and are similar in sequence to Salmonella SseB, SseC, and SseD that function as a translocon. The EseB, EseC, and EseD knockout mutants did not replicate in murine macrophages, suggesting that these proteins are essential for intracellular replication of E. tarda. Highest secretion of EseBCD proteins was observed when bacterial cells were cultured in neutral and alkaline pHs but not in acidic pH. When the pH of the phagosomes was examined using an acidotropic probe, the phagosomes containing the wild-type strain showed neutral pH, whereas those containing the Type III mutant exhibited acidic pH. These results suggest that the Type III-dependent interference with formation of the acidic environment in phagosomes is essential for intracellular replication of bacteria in murine macrophages. KEY WORDS: Edwardsiella tarda · EseBCD proteins · Translocon · Phagosomal pH · Macrophage Resale or republication not permitted without written consent of the publisherDis Aquat Org 84: [115][116][117][118][119][120][121] 2009 macrophages is important for efficient intracellular growth of bacteria in the macrophages (Okuda et al. 2006). However, only scant information is available on the pathogenicity of E. tarda.Many gram-negative pathogenic bacteria use a conserved protein secretion machinery termed 'Type III secretion system' (TTSS) to transport virulence factors and cause disease. The TTSS apparatus consists of approximately 20 to 25 proteins. The unique feature of the TTSS is a needle-like structure through which particular proteins (termed 'effectors') are injected into host cells. Effectors play an important role in the pathogenic relationship between host and bacterium. Injection of effectors into host cells occurs through pores (termed 'translocons)' formed in the host cell membrane by the TTSS using Type III-secreted proteins (Ghosh 2004). The TTSS encoded within Salmonella pathogenicity island 2 (SPI2) is essential for its intracellular accumulation in macrophages. SseB, SseC, and SseD proteins secreted from the TTSS encoded within SPI2 are reported to function as translocons (Nikolaus et al. 2001). Using TnphoA transposon tagging and the proteomics approach, a TTSS was found in Edwardsiella tarda that was similar to that encoded within SPI2 of Salmonella (Srinivasa Rao et al. 2003, Tan et al. 2005. Three TTSS proteins of E. tarda, homologous to SseBCD were identified and these proteins were designated as EseB, EseC, and EseD (Srinivasa Rao et al. 2004, Tan et al. 2005. We reported that, similar to Salmonella, the TTSS encoded within E. tarda is required for its intra...

show abstract

“…The deletion of various single T3SS genes, such as escC, eseB, eseD, or escA, increased the 50% lethal dose (LD 50 ) by approximately 1 log unit in blue gourami (49,55). EscC has been shown to act as the chaperone for EseB and EseD, whereas EscA is the chaperone for EseC (49,55). EseB, EseC, and EseD, which are secreted in large quantities by E. tarda, are homologous to Salmonella sp.…”

mentioning

confidence: 99%

EseG, an Effector of the Type III Secretion System of Edwardsiella tarda , Triggers Microtubule Destabilization

Xie

Zheng

et al. 2010

Infect Immun

Self Cite

View full text Add to dashboard Cite

Edwardsiella tarda is a Gram-negative enteric pathogen that causes hemorrhagic septicemia in fish and both gastrointestinal and extraintestinal infections in humans. A type III secretion system (T3SS) was recently shown to contribute to pathogenesis, since deletions of various T3SS genes increased the 50% lethal dose (LD 50 ) by about 1 log unit in the blue gourami infection model. In this study, we report EseG as the first identified effector protein of T3SS. EseG shares partial homology with two Salmonella T3SS effectors (SseG and SseF) over a conserved domain (amino acid residues 142 to 192). The secretion of EseG is dependent on a functional T3SS and, in particular, requires the chaperone EscB. Experiments using TEM-1 ␤-lactamase as a fluorescence-based reporter showed that EseG was translocated into HeLa cells at 35°C. (EseG 142-192 ), since truncated versions of EseG devoid of this motif lose their ability to cause microtubule destabilization. By demonstrating the function of EseG, our study contributes to the understanding of E. tarda pathogenesis. Moreover, the approach established in this study to identify type III effectors can be used to identify and characterize more type III and possible type VI effectors in Edwardsiella. Fractionation of infected HeLa cells demonstrated that EseG was localized to the host membrane fraction after translocation. EseG is able to disassemble microtubule structures when overexpressed in mammalian cells. This phenotype may require a conserved motif of EseG

show abstract

scite is a Brooklyn-based organization that helps researchers better discover and understand research articles through Smart Citations–citations that display the context of the citation and describe whether the article provides supporting or contrasting evidence. scite is used by students and researchers from around the world and is funded in part by the National Science Foundation and the National Institute on Drug Abuse of the National Institutes of Health.

Contact Info

hi@scite.ai

10624 S. Eastern Ave., Ste. A-614

Henderson, NV 89052, USA

Blog Terms and Conditions API Terms Privacy Policy Contact Cookie Preferences Do Not Sell or Share My Personal Information

Made with 💙 for researchers

Part of the Research Solutions Family.

EscC is a chaperone for the Edwardsiella tarda type III secretion system putative translocon components EseB and EseD

Cited by 31 publications

References 52 publications

EseE of Edwardsiella tarda Augments Secretion of Translocon Protein EseC and Expression of the escC - eseE Operon

EseE of Edwardsiella tarda Augments Secretion of Translocon Protein EseC and Expression of the escC - eseE Operon

Characterization of proteins secreted from a Type III secretion system of Edwardsiella tarda and their roles in macrophage infection

EseG, an Effector of the Type III Secretion System of Edwardsiella tarda , Triggers Microtubule Destabilization

Contact Info

Product

Resources

About