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Originally published In Press as doi:10.1074/jbc.M304709200 on June 3, 2003

J. Biol. Chem., Vol. 278, Issue 34, 32313-32316, August 22, 2003
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Genome-based Identification and Analysis of Collagen-related Structural Motifs in Bacterial and Viral Proteins*

Magnus Rasmussen {ddagger} §, Micael Jacobsson ¶ and Lars Björck {ddagger}

From the {ddagger}Department of Cell and Molecular Biology, Section for Molecular Pathogenesis, Lund University, S-221 84 Lund, Sweden and Biovitrum AB, SE-112 76 Stockholm and the Department of Medical Chemistry, Uppsala University, SE-751 23 Uppsala, Sweden

Collagens are extended trimeric proteins composed of the repetitive sequence glycine-X-Y. A collagen-related structural motif (CSM) containing glycine-X-Y repeats is also found in numerous proteins often referred to as collagen-like proteins. Little is known about CSMs in bacteria and viruses, but the occurrence of such motifs has recently been demonstrated. Moreover, bacterial CSMs form collagen-like trimers, even though these organisms cannot synthesize hydroxyproline, a critical residue for the stability of the collagen triple helix. Here we present 100 novel proteins of bacteria and viruses (including bacteriophages) containing CSMs identified by in silico analyses of genomic sequences. These CSMs differ significantly from human collagens in amino acid content and distribution; bacterial and viral CSMs have a lower proline content and a preference for proline in the X position of GXY triplets. Moreover, the CSMs identified contained more threonine than collagens, and in 17 of 53 bacterial CSMs threonine was the dominating amino acid in the Y position. Molecular modeling suggests that threonines in the Y position make direct hydrogen bonds to neighboring backbone carbonyls and thus substitute for hydroxyproline in the stabilization of the collagen-like triple-helix of bacterial CSMs. The majority of the remaining CSMs were either rich in proline or rich in charged residues. The bacterial proteins containing a CSM that could be functionally annotated were either surface structures or spore components, whereas the viral proteins generally could be annotated as structural components of the viral particle. The limited occurrence of CSMs in eubacteria and lower eukaryotes and the absence of CSMs in archaebacteria suggests that DNA encoding CSMs has been transferred horizontally, possibly from multicellular organisms to bacteria.


Received for publication, May 6, 2003 , and in revised form, June 2, 2003.

* This work was supported by grants from the Swedish Research Council (projects 7480 and 14379), the Medical Faculty, Lund University, the Foundations of Kock and Österlund, and Hansa Medical AB. 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.

§ To whom correspondence should be addressed: Section for Molecular Pathogenesis, Dept. of Cell and Molecular Biology, Lund University, BMC, B14, Tornavägen 10, S-221 84 Lund, Sweden. Tel.: 46-46-2224489; Fax: 46-46-157756; E-mail: Magnus.Rasmussen{at}medkem.lu.se.


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