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Originally published In Press as doi:10.1074/jbc.M109930200 on November 7, 2001

J. Biol. Chem., Vol. 277, Issue 2, 1593-1598, January 11, 2002
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Sensing of Cytoplasmic pH by Bacterial Chemoreceptors Involves the Linker Region That Connects the Membrane-spanning and the Signal-modulating Helices*

Tohru UmemuraDagger §, Yumi MatsumotoDagger , Kouhei Ohnishi||, Michio HommaDagger , and Ikuro KawagishiDagger **

From the Dagger  Division of Biological Science, Graduate School of Science, Nagoya University, Chikusa-ku, Nagoya 464-8602 and  Kamaishi Laboratory, Marine Biotechnology Institute, Kamaishi, Iwate 026-0001, Japan

The two major chemoreceptors of Escherichia coli, Tsr and Tar, mediate opposite responses to the same changes in cytoplasmic pH (pHi). We set out to identify residues involved in pHi sensing to gain insight into the general mechanisms of signaling employed by the chemoreceptors. Characterization of various chimeras of Tsr and Tar localized the pHi-sensing region to Arg259-His267 of Tar and Gly261-Asp269 of Tsr. This region of Tar contains three charged residues (Arg259-Ser261, Asp263, and His267) that have counterparts of opposite charge in Tsr (Gly261-Glu262, Arg265, and Asp269). The replacement of all of the three charged residues in Tar or Arg259-Ser260 alone by the corresponding residues of Tsr reversed the polarity of pHi response, whereas the replacement of Asp263 or His267 did not change the polarity but altered the time course of pHi response. These results suggest that the electrostatic properties of a short cytoplasmic region within the linker region that connects the second transmembrane helix to the first methylation helix is critical for switching the signaling state of the chemoreceptors during pH sensing. Similar conformational changes of this region in response to external ligands may be critical components of transmembrane signaling.

* This work was supported in part by grants-in-aid for scientific research from the Japan Society for the Promotion of Science (to T. U. and I. K.) and from the Takeda Science Foundation (to I. K.).The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

§ Present address: The Waksman Institute, 190 Frelinghuysen Rd., Piscataway, NJ 08854.

|| Present address: The Center for Gene Research, Kochi University, Nangoku-shi, Kochi 783-8502, Japan.

** To whom correspondence should be addressed. Tel.: 81-52-789-2993; Fax: 81-52-789-3001; E-mail: i45406a@cc.nagoya-u.ac.jp.

Copyright © 2002 by The American Society for Biochemistry and Molecular Biology, Inc.
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