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J. Biol. Chem., Vol. 282, Issue 32, 23163-23170, August 10, 2007

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Structure of the Complex of the Colicin E2 R-domain and Its BtuB Receptor

THE OUTER MEMBRANE COLICIN TRANSLOCON^*

From the Department of Biological Sciences, Lilly Hall of Life Sciences, Purdue University, West Lafayette, Indiana 47907

The crystal structure of the complex of the BtuB receptor and the 135-residue coiled-coil receptor-binding R-domain of colicin E3 (E3R135) suggested a novel mechanism for import of colicin proteins across the outer membrane. It was proposed that one function of the R-domain, which extends along the outer membrane surface, is to recruit an additional outer membrane protein(s) to form a translocon for passage colicin activity domain. A 3.5-Å crystal structure of the complex of E2R135 and BtuB (E2R135-BtuB) was obtained, which revealed E2R135 bound to BtuB in an oblique orientation identical to that previously found for E3R135. The only significant difference between the two structures was that the bound coiled-coil R-domain of colicin E2, compared with that of colicin E3, was extended by two and five residues at the N and C termini, respectively. There was no detectable displacement of the BtuB plug domain in either structure, implying that colicin is not imported through the outer membrane by BtuB alone. It was concluded that the oblique orientation of the R-domain of the nuclease E colicins has a function in the recruitment of another member(s) of an outer membrane translocon. Screening of porin knock-out mutants showed that either OmpF or OmpC can function in such a translocon. Arg⁴⁵² at the R/C-domain interface in colicin E2 was found have an essential role at a putative site of protease cleavage, which would liberate the C-terminal activity domain for passage through the outer membrane translocon.

Received for publication, April 10, 2007 , and in revised form, May 22, 2007.

^* These studies were supported by Grants GM18457 (to W. A. C.) and GM62662 (to B. L. W.) from the National Institutes of Health and the Henry Koffler Professorship (to W. A. C.). 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 atomic coordinates and structure factors (code 2YSU) have been deposited in the Protein Data Bank, Research Collaboratory for Structural Bioinformatics, Rutgers University, New Brunswick, NJ (http://www.rcsb.org/).

¹ These authors contributed equally to this work.

² Present address: Inst. for Protein Research, Osaka University, Osaka 565-0871, Japan.

³ To whom correspondence should be addressed. Tel.: 765-494-4956; Fax: 765-496-1189; E-mail: waclab{at}purdue.edu.

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