DOI: 10.1128/jb.185.17.5158-5165.2003. Determination of the InvE Binding Site Required for Expression of IpaB of the <i>Shigella sonnei</i> Virulence Plasmid: Involvement of a ParB BoxA-Like Sequence

Determination of the InvE Binding Site Required for Expression of IpaB of the Shigella sonnei Virulence Plasmid: Involvement of a ParB BoxA-Like Sequence

10.1128/jb.185.17.5158-5165.2003

Crossref journal-article

American Society for Microbiology

Journal of Bacteriology (235)

Abstract

ABSTRACT The InvE protein positively regulates the expression of virulence genes ipaBCD in Shigella sonnei . The InvE has significant homology with ParB of plasmid P1, which is known as a plasmid partitioning factor with DNA binding ability. Although the DNA binding activity of InvE has been predicted, it is not known whether the DNA binding activity is necessary for type III secretion system-associated gene expression. In this study, we determined the transcription start site of the icsB-ipaBCD operon ( ipa operon) and constructed a series of deletions of the icsB promoter region in the Escherichia coli K-12 background. The deletion study revealed that an 86-bp region upstream of the icsB transcription start site was essential for expression of the ipa operon, where the ParB binding motif (ParB BoxA-like sequence) was observed. Purified glutathione S -transferase-InvE fusion protein bound directly to the −93 to −54 region (designating the icsB transcription start site as nucleotide +1) containing the ParB BoxA-like sequence. These results indicated that InvE bound directly to the promoter region.

Bibliography

Taniya, T., Mitobe, J., Nakayama, S., Mingshan, Q., Okuda, K., & Watanabe, H. (2003). Determination of the InvE Binding Site Required for Expression of IpaB of the Shigella sonnei Virulence Plasmid: Involvement of a ParB BoxA-Like Sequence. Journal of Bacteriology, 185(17), 5158â5165.

Authors 6

Takayuki Taniya (first)
Jiro Mitobe (additional)
Shu-ichi Nakayama (additional)
Qi Mingshan (additional)
Kenji Okuda (additional)
Haruo Watanabe (additional)

References 38 Referenced 37

Adler, B., C. Sasakawa, N. Okada, T. Tobe, S. Makino, K. Komatsu, and M. Yoshikawa. 1989. A dual transcriptional activation system for the 230kb plasmid genes coding for virulence-associated antigens of Shigella flexneri.Mol. Microbiol.3:627-635. (10.1111/j.1365-2958.1989.tb00210.x) / Mol. Microbiol. (1989)
Allaoui, A., P. J. Sansonetti, and C. Parsot. 1993. MxiD, an outer membrane protein necessary for the secretion of the Shigella flexneri Ipa invasins. Mol. Microbiol.7:59-1768. (10.1111/j.1365-2958.1993.tb01097.x) / Mol. Microbiol. (1993)
10.1128/iai.59.6.1997-2005.1991
Beloin, C., S. McKenna, and C. J. Dorman. 2002. Molecular dissection of VirB, a key regulator of the virulence cascade of Shigella flexneri.J. Biol. Chem.277:15333-15344. (10.1074/jbc.M111429200) / J. Biol. Chem. (2002)
Bignell, C., and C. M. Thomas. 2001. The bacterial ParA-ParB partitioning proteins. J. Biotechnol.91:1-34. (10.1016/S0168-1656(01)00293-0) / J. Biotechnol. (2001)
Chomczynski, P., and N. Sacchi. 1987. Single-step method of RNA isolation by acid guanidium thiocyanate-phenol-chloroform extraction. Anal. Biochem.162:156-159. / Anal. Biochem. (1987)
10.1073/pnas.120163297
Dorman, C. J., and M. E. Porter. 1998. The Shigella virulence gene regulatory cascade: a paradigm of bacterial gene control mechanisms. Mol. Microbiol.29:677-684. (10.1046/j.1365-2958.1998.00902.x) / Mol. Microbiol. (1998)
Funnell, B. E., and L. Gagnier. 1993. The P1 plasmid partition complex at parS. II. Analysis of ParB protein binding activity and specificity. J. Biol. Chem.268:3616-3624. (10.1016/S0021-9258(18)53738-8) / J. Biol. Chem. (1993)
10.1128/iai.40.1.340-350.1983
10.1128/iai.50.3.620-629.1985
10.1128/mr.55.2.206-224.1991
Ito, K., T. Nakajima, T. Sasaki, and H. Watanabe. 1991. Localization of IpaB protein in Escherichia coli K-12 MC1061 strain carrying Shigella sonnei form I plasmid pSS120. Microbiol. Immunol.35:335-341. (10.1111/j.1348-0421.1991.tb01563.x) / Microbiol. Immunol. (1991)
10.1128/iai.57.5.1391-1398.1989
Kwong, S. M., C. C. Yeo, and C. L. Poh. 2001. Molecular analysis of the pRA2 partitioning region: ParB autoregulates parAB transcription and forms a nucleoprotein complex with the plasmid partition site parS.Mol. Microbiol.40:621-633. (10.1046/j.1365-2958.2001.02405.x) / Mol. Microbiol. (2001)
Makino, S., C. Sasakawa, K. Kamata, and M. Yoshikawa. 1986. A genetic determinant required for continuous reinfection of adjacent cells on large plasmid in Shigella flexneri 2a. Cell46:551-555. (10.1016/0092-8674(86)90880-9) / Cell (1986)
Maniatis T. E. F. Fritsch and J. Sambrook. 1982. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Cold Spring Harbor N.Y.
Manoil, C., and J. Beckwith. 1985. TnphoA: a transposon probe for protein export signals. Proc. Natl. Acad. Sci. USA82:8129-8133. (10.1073/pnas.82.23.8129) / Proc. Natl. Acad. Sci. USA (1985)
10.1128/iai.43.1.195-201.1984
10.1128/iai.49.1.164-171.1985
Menard, R., P. J. Sansonetti, and C. Parsot. 1993. Nonpolar mutagenesis of the ipa genes defines IpaB, IpaC, and IpaD as effectors of Shigella flexneri entry into epithelial cells. J. Bacteriol.175:5899-5906. (10.1128/JB.175.18.5899-5906.1993) / J. Bacteriol. (1993)
Menard, R., P. J. Sansonetti, C. Parsot, and T. Vasselon. 1994. Extracellular association and cytoplasmic partition of IpaB and IpaC invasins of Shigella flexneri.Cell79:515-535. (10.1016/0092-8674(94)90260-7) / Cell (1994)
Miller J. H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory Cold Spring Harbor N.Y.
Parsot, C. 1994. Shigella flexneri: genetics of entry and intercellular dissemination in epithelial cells. Curr. Top. Microbiol. Immunol.192:217-241. / Curr. Top. Microbiol. Immunol. (1994)
Radnedge, L., M. A. Davis, and S. J. Austin. 1996. P1 and P7 plasmid partition: ParB protein bound to its partition site makes a separate discriminator contact with the DNA that determines species specificity. EMBO J.15:1155-1162. (10.1002/j.1460-2075.1996.tb00454.x) / EMBO J. (1996)
Sakai, T., C. Sasakawa, and M. Yoshikawa. 1988. Expression of four virulence antigens of Shigella flexneri is positively regulated at the transcriptional level by the 30kDa virF protein. Mol. Microbiol.2:589-597. (10.1111/j.1365-2958.1988.tb00067.x) / Mol. Microbiol. (1988)
Sanger, F., S. Nicklen, and A. R. Coulson. 1977. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA74:5463-5467. (10.1073/pnas.74.12.5463) / Proc. Natl. Acad. Sci. USA (1977)
10.1128/iai.35.3.852-860.1982
10.1128/jb.170.6.2480-2484.1988
Sasakawa, C., J. M. Buysse, and H. Watanabe. 1992. The large virulence plasmid of Shigella.Curr. Top. Microbiol. Immunol.180:21-44. / Curr. Top. Microbiol. Immunol. (1992)
10.1128/jb.175.8.2334-2346.1993
Sharma, R. C., and R. T. Schimke. 1996. Preparation of electrocompetent E. coli with salt-free growth medium. BioTechniques20:42-44. (10.2144/96201bm08) / BioTechniques (1996)
Smith, D. B., and K. S. Johnson. 1988. Single step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene67:31-40. (10.1016/0378-1119(88)90005-4) / Gene (1988)
Stachel, S. E., G. An, C. Flores, and E. W. Nester. 1985. A Tn3-lacZ transposon for the random generation of β-galactosidase gene fusions: application to the analysis of gene expression in Agrobacterium.EMBO J.4:891-898. (10.1002/j.1460-2075.1985.tb03715.x) / EMBO J. (1985)
Surtees, J. A., and B. E. Funnell. 2001. The DNA binding domains of P1 ParB and the architecture of the P1 plasmid partition complex. J. Biol. Chem.276:12385-12394. (10.1074/jbc.M009370200) / J. Biol. Chem. (2001)
Venkatesan, M., J. M. Buysse, and D. J. Kopecko. 1988. Characterization of invasion plasmid antigen (ipaBCD) gene from Shigella flexneri: DNA sequence analysis and control of gene expression. Proc. Natl. Acad. Sci. USA85:9317-9321. (10.1073/pnas.85.23.9317) / Proc. Natl. Acad. Sci. USA (1988)
10.1128/jb.172.2.619-629.1990
Zychlinsky, A., B. Kenny, R. Menard, M. C. Prevost, I. B. Holland, and P. J. Sansonetti. 1994. IpaB mediates macrophage apoptosis induced by Shigella flexneri.Mol. Microbiol.11:619-627. (10.1111/j.1365-2958.1994.tb00341.x) / Mol. Microbiol. (1994)

Dates

Type	When
Created	22 years ago (Aug. 15, 2003, 1:33 p.m.)
Deposited	4 years ago (July 29, 2021, 2:10 p.m.)
Indexed	2 months, 3 weeks ago (June 4, 2025, 6:29 a.m.)
Issued	21 years, 11 months ago (Sept. 1, 2003)
Published	21 years, 11 months ago (Sept. 1, 2003)
Published Print	21 years, 11 months ago (Sept. 1, 2003)

Funders 0

None

BibTeX

@article{Taniya_2003, title={Determination of the InvE Binding Site Required for Expression of IpaB of the Shigella sonnei Virulence Plasmid: Involvement of a ParB BoxA-Like Sequence}, volume={185}, ISSN={1098-5530}, url={http://dx.doi.org/10.1128/jb.185.17.5158-5165.2003}, DOI={10.1128/jb.185.17.5158-5165.2003}, number={17}, journal={Journal of Bacteriology}, publisher={American Society for Microbiology}, author={Taniya, Takayuki and Mitobe, Jiro and Nakayama, Shu-ichi and Mingshan, Qi and Okuda, Kenji and Watanabe, Haruo}, year={2003}, month=sep, pages={5158–5165} }

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