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- Publisher
- Wiley
- Copyright
- "© 2018 John Wiley & Sons Ltd"
- ISSN
- 1462-5814
- eISSN
- 1462-5822
- D.O.I.
- 10.1111/cmi.12837
- Publisher site
- See Article on Publisher Site
Abstract
Porphyromonas gingivalis is a keystone pathogen in chronic periodontitis. Its expression of gingipain proteases (Kgp and RgpA/B) is central to the stimulation of chronic inflammation. In this study, we investigated the inflammatory response of oral epithelial cells to P. gingivalis. The cells responded by upregulating the expression of the orphan chemokine CXCL14. The stimulation of CXCL14 expression was largely triggered by the gingipain proteases and was dependent on the host protease‐activated receptor PAR‐3. Significantly, CXCL14 expression was transcriptionally repressed in response to epidermal growth factor (EGF)‐induced activation of the MEK‐ERK1/2 pathway. P. gingivalis overcomes the repression of CXCL14 via the gingipain protease‐mediated degradation of EGF. Therefore, P. gingivalis not only directly stimulates CXCL14 expression via PAR‐3 but also promotes its expression by antagonising EGF signalling. In addition to chemotactic activity, some chemokines also have antimicrobial activities. CXCL14 was demonstrated to have bactericidal activity, against commensal oral streptococci associated with health. Notably though, P. gingivalis was not susceptible to killing by CXCL14, potentially because the gingipain proteases can degrade CXCL14. This suggests that the stimulation of dysregulated CXCL14 expression by P. gingivalis may help promote dysbiosis and the development of chronic periodontitis.
Journal
Cellular Microbiology – Wiley
Published: Jul 1, 2018
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References
-
Defining the normal bacterial flora of the oral cavityAas, J. A.; Paster, B. J.; Stokes, L. N.; Olsen, I.; Dewhirst, F. E.
-
RANTES: A versatile and controversial chemokineAppay, V.; Rowland‐Jones, S. L.
-
Evidence for functionally active protease‐activated receptor‐3 (PAR‐3) in human vascular smooth muscle cellsBretschneider, E.; Spanbroek, R.; Lotzer, K.; Habenicht, A. J.; Schror, K.
-
Molecular cloning and characterization of a novel CXC chemokine macrophage inflammatory protein‐2 gamma chemoattractant for human neutrophils and dendritic cellsCao, X.; Zhang, W.; Wan, T.; He, L.; Chen, T.; Yuan, Z.; Chen, G.
-
Degradation of human alpha‐ and beta‐defensins by culture supernatants of Porphyromonas gingivalis strain 381Carlisle, M. D.; Srikantha, R. N.; Brogden, K. A.
-
Epidermal growth factor in gingival crevicular fluid and its binding capacity in inflamed and non‐inflamed human gingivaChang, K. M.; Lehrhaupt, N.; Lin, L. M.; Feng, J.; Wu‐Wang, C. Y.; Wang, S. L.
-
Differential utilization of nuclear factor‐kappaB signaling pathways for gingival epithelial cell responses to oral commensal and pathogenic bacteriaChung, W. O.; Dale, B. A.
-
Protease‐activated receptor signaling increases epithelial antimicrobial peptide expressionChung, W. O.; Hansen, S. R.; Rao, D.; Dale, B. A.
-
Epithelial chemokine CXCL14 synergizes with CXCL12 via allosteric modulation of CXCR4Collins, P. J.; McCully, M. L.; Martinez‐Munoz, L.; Santiago, C.; Wheeldon, J.; Caucheteux, S.; Moser, B.
-
CXCL14 displays antimicrobial activity against respiratory tract bacteria and contributes to clearance of Streptococcus pneumoniae pulmonary infectionDai, C.; Basilico, P.; Cremona, T. P.; Collins, P.; Moser, B.; Benarafa, C.; Wolf, M.
-
Antimicrobial peptides in the oral environment: Expression and function in health and diseaseDale, B. A.; Fredericks, L. P.
-
Localized antimicrobial peptide expression in human gingivaDale, B. A.; Kimball, J. R.; Krisanaprakornkit, S.; Roberts, F.; Robinovitch, M.; O'Neal, R.; Weinberg, A.
-
Periodontitis: A polymicrobial disruption of host homeostasisDarveau, R. P.
-
Local chemokine paralysis, a novel pathogenic mechanism for Porphyromonas gingivalisDarveau, R. P.; Belton, C. M.; Reife, R. A.; Lamont, R. J.
-
Human keratinocytes that express hTERT and also bypass a p16(INK4a)‐enforced mechanism that limits life span become immortal yet retain normal growth and differentiation characteristicsDickson, M. A.; Hahn, W. C.; Ino, Y.; Ronfard, V.; Wu, J. Y.; Weinberg, R. A.; Rheinwald, J. G.
-
Protease‐activated receptor 2 mediates human beta‐defensin 2 and CC chemokine ligand 20 mRNA expression in response to proteases secreted by Porphyromonas gingivalisDommisch, H.; Chung, W. O.; Rohani, M. G.; Williams, D.; Rangarajan, M.; Curtis, M. A.; Dale, B. A.
-
In vivo expression of the novel CXC chemokine BRAK in normal and cancerous human tissueFrederick, M. J.; Henderson, Y.; Xu, X.; Deavers, M. T.; Sahin, A. A.; Wu, H.; Clayman, G. L.
-
Constitutive and inflammation‐dependent antimicrobial peptides produced by epithelium are differentially processed and inactivated by the commensal Finegoldia magna and the pathogen Streptococcus pyogenesFrick, I. M.; Nordin, S. L.; Baumgarten, M.; Morgelin, M.; Sorensen, O. E.; Olin, A. I.; Egesten, A.
-
Cleavage of protease‐activated receptors on an immortalized oral epithelial cell line by Porphyromonas gingivalis gingipainsGiacaman, R. A.; Asrani, A. C.; Ross, K. F.; Herzberg, M. C.
-
Chemokines, a family of chemotactic cytokinesGraves, D. T.; Jiang, Y.
-
CXCR3 ligands: Redundant, collaborative and antagonistic functionsGroom, J. R.; Luster, A. D.
-
Periodontitis: From microbial immune subversion to systemic inflammationHajishengallis, G.
-
Pathogen induction of CXCR4/TLR2 cross‐talk impairs host defense functionHajishengallis, G.; Wang, M.; Liang, S.; Triantafilou, M.; Triantafilou, K.
-
Improved silver staining procedure for fast staining in PhastSystem Development Unit. I. Staining of sodium dodecyl sulfate gelsHeukeshoven, J.; Dernick, R.
-
CCL28 has dual roles in mucosal immunity as a chemokine with broad‐spectrum antimicrobial activityHieshima, K.; Ohtani, H.; Shibano, M.; Izawa, D.; Nakayama, T.; Kawasaki, Y.; Yoshie, O.
-
Microbiome profiles in periodontitis in relation to host and disease characteristicsHong, B. Y.; Furtado Araujo, M. V.; Strausbaugh, L. D.; Terzi, E.; Ioannidou, E.; Diaz, P. I.
-
Propeptide‐mediated inhibition of cognate gingipain proteinasesHuq, N. L.; Seers, C. A.; Toh, E. C.; Dashper, S. G.; Slakeski, N.; Zhang, L.; Reynolds, E. C.
-
IRF6 regulates the expression of IL‐36gamma by human oral epithelial cells in response to Porphyromonas gingivalisHuynh, J.; Scholz, G. M.; Aw, J.; Kwa, M. Q.; Achuthan, A.; Hamilton, J. A.; Reynolds, E. C.
-
Arg‐gingipain acts as a major processing enzyme for various cell surface proteins in Porphyromonas gingivalisKadowaki, T.; Nakayama, K.; Yoshimura, F.; Okamoto, K.; Abe, N.; Yamamoto, K.
-
P. gingivalis interactions with epithelial cellsKinane, D. F.; Galicia, J. C.; Gorr, S. U.; Stathopoulou, P. G.; Benakanakere, M.
-
Neutrophil infiltration and chemokinesKobayashi, Y.
-
Oral multispecies biofilm development and the key role of cell‐cell distanceKolenbrander, P. E.; Palmer, R. J.; Periasamy, S.; Jakubovics, N. S.
-
Monocyte selectivity and tissue localization suggests a role for breast and kidney‐expressed chemokine (BRAK) in macrophage developmentKurth, I.; Willimann, K.; Schaerli, P.; Hunziker, T.; Clark‐Lewis, I.; Moser, B.
-
Interferon regulatory factor 6 differentially regulates Toll‐like receptor 2‐dependent chemokine gene expression in epithelial cellsKwa, M. Q.; Nguyen, T.; Huynh, J.; Ramnath, D.; De Nardo, D.; Lam, P. Y.; Scholz, G. M.
-
Polymicrobial synergy and dysbiosis in inflammatory diseaseLamont, R. J.; Hajishengallis, G.
-
Keratinocyte growth factor‐1 expression in healthy and diseased human periodontal tissuesLi, M.; Firth, J. D.; Putnins, E. E.
-
Epidermal EGFR controls cutaneous host defense and prevents inflammationLichtenberger, B. M.; Gerber, P. A.; Holcmann, M.; Buhren, B. A.; Amberg, N.; Smolle, V.; Sibilia, M.
-
Epidermal growth factor receptor signaling to Erk1/2 and STATs control the intensity of the epithelial inflammatory responses to rhinovirus infectionLiu, K.; Gualano, R. C.; Hibbs, M. L.; Anderson, G. P.; Bozinovski, S.
-
Arginine‐specific protease from Porphyromonas gingivalis activates protease‐activated receptors on human oral epithelial cells and induces interleukin‐6 secretionLourbakos, A.; Potempa, J.; Travis, J.; D'Andrea, M. R.; Andrade‐Gordon, P.; Santulli, R.; Pike, R. N.
-
Porphyromonas gingivalis manipulates complement and TLR signaling to uncouple bacterial clearance from inflammation and promote dysbiosisMaekawa, T.; Krauss, J. L.; Abe, T.; Jotwani, R.; Triantafilou, M.; Triantafilou, K.; Hajishengallis, G.
-
Potent and broad‐spectrum antimicrobial activity of CXCL14 suggests an immediate role in skin infectionsMaerki, C.; Meuter, S.; Liebi, M.; Muhlemann, K.; Frederick, M. J.; Yawalkar, N.; Wolf, M.
-
Blockade of the EGF receptor induces a deranged chemokine expression in keratinocytes leading to enhanced skin inflammationMascia, F.; Mariani, V.; Girolomoni, G.; Pastore, S.
-
Protease‐activated receptor‐3 (PAR3) regulates PAR1 signaling by receptor dimerizationMcLaughlin, J. N.; Patterson, M. M.; Malik, A. B.
-
Involvement of arginine‐specific cysteine proteinase (Arg‐gingipain) in fimbriation of Porphyromonas gingivalisNakayama, K.; Yoshimura, F.; Kadowaki, T.; Yamamoto, K.
-
A role for fimbriae in Porphyromonas gingivalis invasion of oral epithelial cellsNjoroge, T.; Genco, R. J.; Sojar, H. T.; Hamada, N.; Genco, C. A.
-
Porphyromonas gingivalis gingipains: The molecular teeth of a microbial vampireO'Brien‐Simpson, N. M.; Veith, P. D.; Dashper, S. G.; Reynolds, E. C.
-
The protease‐activated receptor‐3 (PAR‐3) can signal autonomously to induce interleukin‐8 releaseOstrowska, E.; Reiser, G.
-
Isolation and characterization of the Porphyromonas gingivalis prtT gene, coding for protease activityOtogoto, J.; Kuramitsu, H. K.
-
Susceptibilities of periodontopathogenic and cariogenic bacteria to antibacterial peptides, {beta}‐defensins and LL37, produced by human epithelial cellsOuhara, K.; Komatsuzawa, H.; Yamada, S.; Shiba, H.; Fujiwara, T.; Ohara, M.; Sugai, M.
-
Characterization of the tpr gene product and isolation of a specific protease‐deficient mutant of Porphyromonas gingivalis W83Park, Y.; McBride, B. C.
-
Expression of growth‐factor receptors in normal and regenerating human periodontal cellsParkar, M. H.; Kuru, L.; Giouzeli, M.; Olsen, I.
-
Epithelial structural proteins of the skin and oral cavity: Function in health and diseasePresland, R. B.; Dale, B. A.
-
Inactivation of epidermal growth factor by Porphyromonas gingivalis as a potential mechanism for periodontal tissue damagePyrc, K.; Milewska, A.; Kantyka, T.; Sroka, A.; Maresz, K.; Koziel, J.
-
Cutaneous CXCL14 targets blood precursors to epidermal niches for Langerhans cell differentiationSchaerli, P.; Willimann, K.; Ebert, L. M.; Walz, A.; Moser, B.
-
PAR‐3 knockdown enhances adhesion rate of PANC‐1 cells via increased expression of integrinalphav and E‐cadherinSegal, L.; Katz, L. S.; Shapira, H.; Sandbank, J.; Geras‐Raaka, E.; Gershengorn, M. C.; Oron, Y.
-
BRAK/CXCL14 is a potent inhibitor of angiogenesis and a chemotactic factor for immature dendritic cellsShellenberger, T. D.; Wang, M.; Gujrati, M.; Jayakumar, A.; Strieter, R. M.; Burdick, M. D.; Frederick, M. J.
-
Genetic analyses of proteolysis, hemoglobin binding, and hemagglutination of Porphyromonas gingivalis. Construction of mutants with a combination of rgpA, rgpB, kgp, and hagAShi, Y.; Ratnayake, D. B.; Okamoto, K.; Abe, N.; Yamamoto, K.; Nakayama, K.
-
Loss of new chemokine CXCL14 in tumor tissue is associated with low infiltration by dendritic cells (DC), while restoration of human CXCL14 expression in tumor cells causes attraction of DC both in vitro and in vivoShurin, G. V.; Ferris, R. L.; Tourkova, I. L.; Perez, L.; Lokshin, A.; Balkir, L.
-
The host cytokine response to Porphyromonas gingivalis is modified by gingipainsStathopoulou, P. G.; Benakanakere, M. R.; Galicia, J. C.; Kinane, D. F.
-
The serine phosphatase SerB of Porphyromonas gingivalis suppresses IL‐8 production by dephosphorylation of NF‐kappaB RelA/p65Takeuchi, H.; Hirano, T.; Whitmore, S. E.; Morisaki, I.; Amano, A.; Lamont, R. J.
-
Gingipains from Porphyromonas gingivalis synergistically induce the production of proinflammatory cytokines through protease‐activated receptors with Toll‐like receptor and NOD1/2 ligands in human monocytic cellsUehara, A.; Imamura, T.; Potempa, J.; Travis, J.; Takada, H.
-
Microbial hijacking of complement‐toll‐like receptor crosstalkWang, M.; Krauss, J. L.; Domon, H.; Hosur, K. B.; Liang, S.; Magotti, P.; Hajishengallis, G.
-
Role of fimbriae in Porphyromonas gingivalis invasion of gingival epithelial cellsWeinberg, A.; Belton, C. M.; Park, Y.; Lamont, R. J.
-
The emerging role of the insulin‐like growth factors in oral biologyWerner, H.; Katz, J.
-
Many chemokines including CCL20/MIP‐3alpha display antimicrobial activityYang, D.; Chen, Q.; Hoover, D. M.; Staley, P.; Tucker, K. D.; Lubkowski, J.; Oppenheim, J. J.
-
Involvement of integrins in fimbriae‐mediated binding and invasion by Porphyromonas gingivalisYilmaz, O.; Watanabe, K.; Lamont, R. J.
-
Antimicrobial chemokinesYung, S. C.; Murphy, P. M.
-
IL‐8 degradation by Porphyromonas gingivalis proteasesZhang, J.; Dong, H.; Kashket, S.; Duncan, M. J.
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