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J. Biol. Chem., Vol. 280, Issue 10, 8668-8677, March 11, 2005

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Identification of a New Membrane-associated Protein That Influences Transport/Maturation of Gingipains and Adhesins of Porphyromonas gingivalis^*

Keiko Sato, Eiko Sakai, Paul D. Veith¶, Mikio Shoji, Yuichiro Kikuchi, Hideharu Yukitake, Naoya Ohara, Mariko Naito, Kuniaki Okamoto, Eric C. Reynolds¶, and Koji Nakayama||

From the Divisions of Microbiology and Oral Infection and Oral Molecular Pharmacology, Department of Developmental and Reconstructive Medicine, Nagasaki University Graduate School of Biomedical Sciences, 1-7-1 Sakamoto, Nagasaki 852-8588, Japan and the ^¶Cooperative Research Centre for Oral Health Science, School of Dental Science, The University of Melbourne, Victoria, 3010, Australia

The dual membrane envelopes of Gram-negative bacteria provide two barriers of unlike nature that regulate the transport of molecules into and out of organisms. Organisms have developed several systems for transport across the inner and outer membranes. The Gram-negative periodontopathogenic bacterium Porphyromonas gingivalis produces proteinase and adhesin complexes, gingipains/adhesins, on the cell surface and in the extracellular milieu as one of the major virulence factors. Gingipains and/or adhesins are encoded by kgp, rgpA, rgpB, and hagA on the chromosome. In this study, we isolated a P. gingivalis mutant (porT), which showed very weak activities of gingipains in the cell lysates and culture supernatants. Subcellular fractionation and immunoblot analysis demonstrated that precursor forms of gingipains and adhesins were accumulated in the periplasmic space of the porT mutant cells. Peptide mass fingerprinting and N-terminal amino acid sequencing of the precursor proteins and the kgp'-'rgpB chimera gene product in the porT mutant indicated that these proteins lacked the signal peptide regions, consistent with their accumulation in the periplasm. The PorT protein seemed to be membrane-associated and exposed to the periplasmic space, as revealed by subcellular fractionation and immunoblot analysis using anti-PorT antiserum. These results suggest that the membrane-associated protein PorT is essential for transport of the kgp, rgpA, rgpB, and hagA gene products across the outer membrane from the periplasm to the cell surface, where they are processed and matured.

Received for publication, December 2, 2004 , and in revised form, December 27, 2004.

^* This work was supported by Grants-in-aid 14370585 and 16017282 for Scientific Research from the Ministry of Education, Science, Sports, Culture and Technology, Japan. 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 supplementary data.

The nucleotide sequence(s) reported in this paper has been submitted to the GenBank^TM/EBI Data Bank with accession number(s) AB016085.

^|| To whom correspondence should be addressed. Tel.: 81-95-849-7648; Fax: 81-95-849-7650; E-mail: knak{at}net.nagasaki-u.ac.jp.

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