The read-through transcription-mediated autoactivation circuit for virulence regulator expression drives robust type III secretion system 2 expression in Vibrio parahaemolyticus

Anggramukti, Dhira Saraswati; Ishii, Eiji; Pratama, Andre; Kadi, Mohamad Al; Iida, Tetsuya; Kodama, Toshio; Matsuda, Shigeaki

doi:https://doi.org/10.1371/journal.ppat.1012094

The read-through transcription-mediated autoactivation circuit for virulence regulator expression drives robust type III secretion system 2 expression in Vibrio parahaemolyticus

Anggramukti, Dhira Saraswati; Ishii, Eiji; Pratama, Andre et al.

PLoS Pathogens, 2024, 20(3), e1012094

Number of Access:1,067（2025-09-29 10:04 Counts）

Identifier to cite or link to this item: https://hdl.handle.net/11094/97806

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Title	The read-through transcription-mediated autoactivation circuit for virulence regulator expression drives robust type III secretion system 2 expression in Vibrio parahaemolyticus
Creator	CreatorName Anggramukti, Dhira Saraswati
	NRID 1000010835698 1000010835698 ORCID 0000-0001-7899-252X 0000-0001-7899-252X researchmap permalink eishii0322 eishii0322 Scopus Author ID 56890709800 56890709800 CreatorName Ishii, Eiji
	NRID 1000030972319 1000030972319 researchmap permalink Andre_Pratama Andre_Pratama ORCID 0000-0001-5384-4475 0000-0001-5384-4475 CreatorName Pratama, Andre
	NRID 1000070963883 1000070963883 researchmap permalink malkadi malkadi CreatorName Kadi, Mohamad Al
	NRID 1000090221746 1000090221746 researchmap permalink iidatetsuya iidatetsuya Scopus Author ID 7402683497 7402683497 CreatorName Iida, Tetsuya
	NRID 1000020346133 1000020346133 researchmap permalink read0092252 read0092252 CreatorName Kodama, Toshio
	NRID 1000030506499 1000030506499 researchmap permalink shigeakimatsuda shigeakimatsuda Scopus Author ID 22135321100 22135321100 ORCID 0000-0001-8430-9723 0000-0001-8430-9723 CreatorName Matsuda, Shigeaki
Description	Anggramukti D.S., Ishii E., Pratama A., et al. (2004) The read-through transcription-mediated autoactivation circuit for virulence regulator expression drives robust type III secretion system 2 expression in Vibrio parahaemolyticus. PLoS Pathogens 20(3): e1012094. doi.org/10.1371/journal.ppat.1012094.
Abstract	Vibrio parahaemolyticus is the leading cause of seafood-borne gastroenteritis in humans worldwide. The major virulence factor responsible for the enteropathogenicity of this pathogen is type III secretion system 2 (T3SS2), which is encoded on the 80-kb V. parahaemolyticus pathogenicity island (Vp-PAI), the gene expression of which is governed by the OmpR-family transcriptional regulator VtrB. Here, we found a positive autoregulatory feature of vtrB transcription, which is often observed with transcriptional regulators of bacteria, but the regulation was not canonically dependent on its own promoter. Instead, this autoactivation was induced by heterogeneous transcripts derived from the VtrB-regulated operon upstream of vtrB. VtrB-activated transcription overcame the intrinsic terminator downstream of the operon, resulting in transcription read-through with read-in transcription of the vtrB gene and thus completing the autoregulatory loop for vtrB gene expression. The dampening of readthrough transcription with an exogenous strong terminator reduced vtrB gene expression. Furthermore, a V. parahaemolyticus mutant with defects in the vtrB autoregulatory loop also showed compromises in T3SS2 expression and T3SS2-dependent cytotoxicity in vitro and enterotoxicity in vivo, indicating that this autoregulatory loop is essential for sustained vtrB activation and the consequent robust expression of T3SS2 genes for pathogenicity. Taken together, these findings demonstrate that the regulatory loop for vtrB gene expression based on read-through transcription from the upstream operon is a crucial pathway in T3SS2 gene regulatory network to ensure T3SS2-mediated virulence of V. parahaemolyticus.
Publisher	Public Library of Science
Source Title	PLoS Pathogens
Volume (Issue)	20(3)
Page	e1012094
Date of Issued	2024-03-27
Language	English
Handle URL	https://hdl.handle.net/11094/97806
PISSN	15537366
eISSN	15537374
Relation.isIdenticalTo	DOI (Publisher Version) https://doi.org/10.1371/journal.ppat.1012094
Access Rights	open access
CopyRight	This article is licensed under a Creative Commons Attribution 4.0 International License.
oaire:version	Version of Record
Category	学術雑誌論文 Journal Article

Resource Type	journal article
Local Type	Journal Article
DCTERMS.bibliographicCitation	PLoS Pathogens. 2024, 20(3), p. e1012094
DC.title	The read-through transcription-mediated autoactivation circuit for virulence regulator expression drives robust type III secretion system 2 expression in Vibrio parahaemolyticus
DC.creator	Anggramukti, Dhira Saraswati
	Ishii, Eiji
	Pratama, Andre
	Kadi, Mohamad Al
	Iida, Tetsuya
	Kodama, Toshio
	Matsuda, Shigeaki
DC.publisher	Public Library of Science
DC.language' scheme='DCTERMS.RFC1766	English
DCTERMS.issued' scheme='DCTERMS.W3CDTF	2024-03-27
DC.identifier	https://doi.org/10.1371/journal.ppat.1012094
DC.description	Anggramukti D.S., Ishii E., Pratama A., et al. (2004) The read-through transcription-mediated autoactivation circuit for virulence regulator expression drives robust type III secretion system 2 expression in Vibrio parahaemolyticus. PLoS Pathogens 20(3): e1012094. doi.org/10.1371/journal.ppat.1012094.
DCTERMS.abstract	Vibrio parahaemolyticus is the leading cause of seafood-borne gastroenteritis in humans worldwide. The major virulence factor responsible for the enteropathogenicity of this pathogen is type III secretion system 2 (T3SS2), which is encoded on the 80-kb V. parahaemolyticus pathogenicity island (Vp-PAI), the gene expression of which is governed by the OmpR-family transcriptional regulator VtrB. Here, we found a positive autoregulatory feature of vtrB transcription, which is often observed with transcriptional regulators of bacteria, but the regulation was not canonically dependent on its own promoter. Instead, this autoactivation was induced by heterogeneous transcripts derived from the VtrB-regulated operon upstream of vtrB. VtrB-activated transcription overcame the intrinsic terminator downstream of the operon, resulting in transcription read-through with read-in transcription of the vtrB gene and thus completing the autoregulatory loop for vtrB gene expression. The dampening of readthrough transcription with an exogenous strong terminator reduced vtrB gene expression. Furthermore, a V. parahaemolyticus mutant with defects in the vtrB autoregulatory loop also showed compromises in T3SS2 expression and T3SS2-dependent cytotoxicity in vitro and enterotoxicity in vivo, indicating that this autoregulatory loop is essential for sustained vtrB activation and the consequent robust expression of T3SS2 genes for pathogenicity. Taken together, these findings demonstrate that the regulatory loop for vtrB gene expression based on read-through transcription from the upstream operon is a crucial pathway in T3SS2 gene regulatory network to ensure T3SS2-mediated virulence of V. parahaemolyticus.
DC.rights	This article is licensed under a Creative Commons Attribution 4.0 International License.
DC.format	97806
citation_title	The read-through transcription-mediated autoactivation circuit for virulence regulator expression drives robust type III secretion system 2 expression in Vibrio parahaemolyticus
citation_author	Anggramukti, Dhira Saraswati
	Ishii, Eiji
	Pratama, Andre
	Kadi, Mohamad Al
	Iida, Tetsuya
	Kodama, Toshio
	Matsuda, Shigeaki
citation_publisher	Public Library of Science
citation_language	English
citation_date	2024-03-27
citation_journal_title	PLoS Pathogens
citation_volume	20
citation_issue	3
citation_firstpage	e1012094
citation_doi	https://doi.org/10.1371/journal.ppat.1012094
citation_public_url	https://hdl.handle.net/11094/97806

The read-through transcription-mediated autoactivation circuit for virulence regulator expression drives robust type III secretion system 2 expression in Vibrio parahaemolyticus

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