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J. Biol. Chem., Vol. 283, Issue 9, 5738-5747, February 29, 2008

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Involvement of RNA-binding Protein Hfq in the Post-transcriptional Regulation of invE Gene Expression in Shigella sonnei^*

Jiro Mitobe, Tomoko Morita-Ishihara, Akira Ishihama, and Haruo Watanabe¹

From the Department of Bacteriology, National Institute of Infectious Diseases, Shinjuku, Tokyo 162-8640 and the Department of Frontier Bioscience, Hosei University, Koganei, Tokyo 184-8584, Japan

The temperature-dependent regulation of Shigella virulence genes is believed to be accomplished at the transcriptional stage by the regulators VirF and InvE. Several lines of evidence herein described indicate that post-transcriptional regulation of InvE expression plays a key role in the temperature-dependent regulation of virulence gene expression: (i) a considerable amount of invE mRNA continues to be transcribed under low temperature conditions, where the production of InvE protein is tightly repressed; (ii) the stability of invE mRNA markedly decreases, because its decay rate is significantly increased under the repressing conditions. Strikingly, in the hfq mutant of Shigella sonnei, a considerable amount of InvE protein was produced even at low temperature. This increase in the InvE level was found to be associated with the improved stability of invE mRNA, in agreement with the finding that the RNA chaperon Hfq influences post-transcriptional regulations of various genes. Consistently, overexpression of the Hfq protein decreased the production of InvE protein even under the expressing condition at 37 °C. The binding in vitro of purified Hfq protein to invE RNA was shown to be stronger at 30 °C than at 37 °C in two experiments, gel shift analysis and surface plasmon resonance (Biacore) analysis. These results altogether suggest that Hfq plays an important role in the temperature-dependent regulation of invE expression at the post-transcriptional step.

Received for publication, December 11, 2007

^* This work was supported by Ministry of Health, Labor, and Welfare Grant-in-aid H19· kokusai-igaku and by the Ministry of Education, Science and Technology of the Japanese Government. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains supplemental Table S1.

¹ To whom correspondence should be addressed. Tel.: 81-3-5285-1111 (ext. 2201); Fax: 81-3-5285-1171; E-mail: haruwata{at}nih.go.jp.

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