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Extracellular Proteome and Citrullinome of the Oral Pathogen Porphyromonas gingivalis

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    Extracellular Proteome and Citrullinome of the Oral Pathogen Porphyromonas gingivalis
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    † Department of Medical Microbiology, University of Groningen, University Medical Center Groningen, Groningen 9700 RB, The Netherlands
    ‡ Institute for Microbiology, Ernst-Moritz-Arndt-University Greifswald, Greifswald 17489, Germany
    § Center for Dentistry and Oral Hygiene, Department of Periodontology, University of Groningen, University Medical Center Groningen, Groningen 9700 RB, The Netherlands
    ∥ Department of Molecular Genetics, University of Groningen, Groningen 9700 AB, The Netherlands
    *E-mail: [email protected]. Phone: +31-50-3615187.
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    Journal of Proteome Research

    Cite this: J. Proteome Res. 2016, 15, 12, 4532–4543
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    https://doi.org/10.1021/acs.jproteome.6b00634
    Published October 7, 2016
    Copyright © 2016 American Chemical Society
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    Abstract

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    Porphyromonas gingivalis is an oral pathogen associated with the inflammatory disease periodontitis. Periodontitis and P. gingivalis have been associated with rheumatoid arthritis. One of the hallmarks of rheumatoid arthritis is the loss of tolerance against citrullinated proteins. Citrullination is a post-translational modification of arginine residues, leading to a change in structure and function of the respective protein. This modification, which is catalyzed by peptidylarginine deiminases (PADs), plays a role in several physiological processes in the human body. Interestingly, P. gingivalis secretes a citrullinating enzyme, known as P. gingivalis PAD (PPAD), which targets bacterial and human proteins. Because the extent of P. gingivalis protein citrullination by PPAD was not yet known, the present study was aimed at identifying the extracellular proteome and citrullinome of P. gingivalis. To this end, extracellular proteins of two reference strains, two PPAD-deficient mutants, and three clinical isolates of P. gingivalis were analyzed by mass spectrometry. The results uncovered substantial heterogeneity in the extracellular proteome and citrullinome of P. gingivalis, especially in relation to the extracellular detection of typical cytoplasmic proteins. In contrast, the major virulence factors of P. gingivalis were identified in all investigated isolates, although their citrullination was shown to vary. This may be related to post-translational processing of the PPAD enzyme. Altogether, our findings focus attention on the possible roles of 6 to 25 potentially citrullinated proteins, especially the gingipain RgpA, in periodontitis and rheumatoid arthritis.

    Copyright © 2016 American Chemical Society

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    The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jproteome.6b00634.

    • Table S1. Overview of identified extracellular proteins in the present study with peptide and spectral count information. (XLSX)

    • Figure S1. Growth curves of P. gingivalis in liquid culture. Figure S2. LDS-PAGE of exoproteome samples Figure S3. Numbers of proteins in the exoproteomes of the P. gingivalis isolates. Figure S4. Localization prediction of identified proteins per isolate. Figure S5. Sequence coverage and modifications of PPAD. (PDF)

    • Figure S6. Spectra and fragmentation tables of citrullinated proteins. (PDF)

    • Supplementary FASTA file. Nonredundant P. gingivalis database concatenated with common laboratory contaminants and a target-pseudoreversed decoy database. (ZIP)

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    Journal of Proteome Research

    Cite this: J. Proteome Res. 2016, 15, 12, 4532–4543
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    https://doi.org/10.1021/acs.jproteome.6b00634
    Published October 7, 2016
    Copyright © 2016 American Chemical Society
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