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J. Biol. Chem., Vol. 280, Issue 50, 41387-41394, December 16, 2005

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The Osmotic Activation of Transporter ProP Is Tuned by Both Its C-terminal Coiled-coil and Osmotically Induced Changes in Phospholipid Composition^*

Yonit Tsatskis1, Jumana Khambati2, Martina Dobson, Mikhail Bogdanov, William Dowhan, and Janet M. Wood3

From the Department of Molecular and Cellular Biology, University of Guelph, Guelph, Ontario N1G 2W1, Canada and the Department of Biochemistry and Molecular Biology, University of Texas-Houston Medical School, Houston, Texas 77030

Transporter ProP of Escherichia coli (ProPEc) senses extracellular osmolality and mediates osmoprotectant uptake when it is rising or high. A replica of the ProPEc C terminus (Asp⁴⁶⁸–Arg⁴⁹⁷) forms an intermolecular -helical coiled-coil. This structure is implicated in the osmoregulation of intact ProPEc, in vivo. Like that from Corynebacterium glutamicum (ProPCg), the ProP orthologue from Agrobacterium tumefaciens (ProPAt) sensed and responded to extracellular osmolality after expression in E. coli. The osmotic activation profiles of all three orthologues depended on the osmolality of the bacterial growth medium, the osmolality required for activation rising as the growth osmolality approached 0.7 mol/kg. Thus, each could undergo osmotic adaptation. The proportion of cardiolipin in a polar lipid extract from E. coli increased with extracellular osmolality so that the osmolality activating ProPEc was a direct function of membrane cardiolipin content. Group A ProP orthologues (ProPEc, ProPAt) share the C-terminal coiled-coil domain and were activated at low osmolalities. Like variant ProPEc-R488I, in which the C-terminal coiled-coil is disrupted, ProPEc derivatives that lack the coiled-coil and Group B orthologue ProPCg required a higher osmolality to activate. The amplitude of ProPEc activation was reduced 10-fold in its deletion derivatives. The coiled-coil structure is not essential for osmotic activation of ProP per se. However, it tunes Group A orthologues to osmoregulate over a low osmolality range. Coiled-coil lesions may impair both coiled-coil formation and interaction of ProPEc with amplifier protein ProQ. Cardiolipin may contribute to ProP adaptation by altering bulk membrane properties or by acting as a ProP ligand.

Received for publication, July 29, 2005 , and in revised form, October 4, 2005.

^* This work was supported in part by Natural Sciences and Engineering Research Council of Canada Grant OPG0000508 (to J. M. W.) and National Institutes of Health Grant R37 GM20487 (to W. D.). 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.

¹ Present address: Samuel Lunenfeld Research Institute, Toronto, Ontario M5G 1X5, Canada.

² Present address: Dept. of Biological Sciences, University of Calgary, Calgary, Alberta T2N 1N4, Canada.

³ To whom correspondence should be addressed: Dept. of Molecular and Cellular Biology, University of Guelph, Guelph, Ontario N1G 2W1, Canada. Tel.: 519-824-4120 (ext. 53866); Fax: 519-837-1802; E-mail: jwood{at}uoguelph.ca.

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