International Journal of Oral Biology

The Korean Academy of Oral Biology (대한구강생물학회)
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Clathrin and Lipid Raft-dependent Internalization of Porphyromonas gingivalis in Endothelial Cells

  • Kim, Sang-Yong (Department of Oral Microbiology, School of Dentistry, Chonnam National University) ;
  • Kim, So-Hee (Department of Oral Microbiology, School of Dentistry, Chonnam National University) ;
  • Choi, Eun-Kyoung (Department of Oral Microbiology, School of Dentistry, Chonnam National University) ;
  • Paek, Yun-Woong (Department of Physical Therapy, Gwangju Health University) ;
  • Kang, In-Chol (Department of Oral Microbiology, School of Dentistry, Chonnam National University)
  • Received : 2014.06.03
  • Accepted : 2014.08.28
  • Published : 2014.09.30
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Abstract

Porphyromonas gingivalis is one of the most important periodontal pathogens and has been to known to invade various types of cells, including endothelial cells. The present study investigated the mechanisms involved in the internalization of P. gingivalis in human umbilical vein endothelial cells (HUVEC). P. gingivalis internalization was reduced by clathrin and lipid raft inhibitors, as well as a siRNA knockdown of caveolin-1, a principal molecule of lipid raft-related caveolae. The internalization was also reduced by perturbation of actin rearrangement, while microtubule polymerization was not required. Furthermore, we found that Src kinases are critical for the internalization of P. gingivalis into HUVEC, while neither Rho family GTPases nor phosphatidylinositol 3-kinase are required. Taken together, this study indicated that P. gingivalis internalization into endothelial cells involves clathrin and lipid rafts and requires actin rearrangement associated with Src kinase activation.

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References

  1. Socransky SS, Haffajee AD. The bacterial etiology of destructive periodontal disease: current concepts. J Periodontol. 1992;63:322-331. https://doi.org/10.1902/jop.1992.63.4s.322
  2. Lamont RJ, Jenkinson HF. Life below the gum line: pathogenic mechanisms of Porphyromonas gingivalis. Microbiol Mol Biol Rev. 1998;62:1244-1263.
  3. Baker PJ. The role of immune responses in bone loss during periodontal disease. Microbes infect. 2000;2: 1181-1192. https://doi.org/10.1016/S1286-4579(00)01272-7
  4. Pott J, Basler T, Duerr CU, Rohde M, Goethe R, Hornef MW. Internalization-dependent recognition of Mycobacterium avium ssp. paratuberculosis by intestinal epithelial cells. Cell Microbiol. 2009;11:1802-1815. https://doi.org/10.1111/j.1462-5822.2009.01372.x
  5. Long M, Huang SH, Wu CH, Shackleford GM, Jong A. Lipid raft/caveolae signaling is required for Cryptococcus neoformans invasion into human brain microvascular endothelial cells. J Biomed Sci. 2012;19:19. https://doi.org/10.1186/1423-0127-19-19
  6. Lemire P, Houde M, Segura M. Encapsulated group B Streptococcus modulates dendritic cell functions via lipid rafts and clathrin-mediated endocytosis. Cell Microbiol. 2012;14:1707-1719. https://doi.org/10.1111/j.1462-5822.2012.01830.x
  7. Kang IC, Kuramitsu HK. Induction of monocyte chemoattractant protein-1 by Porphyromonas gingivalis in human endothelial cells. FEMS Immunol Med Microbiol. 2002;34:311-317. https://doi.org/10.1111/j.1574-695X.2002.tb00639.x
  8. Pizarro-Cerda J, Bonazzi M, Cossart P. Clathrin-mediated endocytosis: what works for small, also works for big. Bioessays. 2010;32:496-504. https://doi.org/10.1002/bies.200900172
  9. Boisvert H, Duncan MJ. Clathrin-dependent entry of a gingipain adhesin peptide and Porphyromonas gingivalis into host cells. Cell Microbiol. 2008;10:2538-2552. https://doi.org/10.1111/j.1462-5822.2008.01228.x
  10. Dorn BR, Dunn WA, Jr., Progulske-Fox A. Invasion of human coronary artery cells by periodontal pathogens. Infect Immun. 1999;67:5792-5798.
  11. Irshad M, van der Reijden WA, Crielaard W, Laine ML. In vitro invasion and survival of Porphyromonas gingivalis in gingival fibroblasts; role of the capsule. Arch Immunol Ther Exp. 2012;60:469-476. https://doi.org/10.1007/s00005-012-0196-8
  12. Wang M, Hajishengallis G. Lipid raft-dependent uptake, signalling and intracellular fate of Porphyromonas gingivalis in mouse macrophages. Cell Microbiol. 2008;10:2029-2042. https://doi.org/10.1111/j.1462-5822.2008.01185.x
  13. Belanger M, Rodrigues PH, Dunn WA, Jr., Progulske-Fox A. Autophagy: a highway for Porphyromonas gingivalis in endothelial cells. Autophagy. 2006;2:165-170. https://doi.org/10.4161/auto.2828
  14. Mooren OL, Galletta BJ, Cooper JA. Roles for actin assembly in endocytosis. Annu Rev Biochem. 2012;81: 661-686. https://doi.org/10.1146/annurev-biochem-060910-094416
  15. Agarwal V, Hammerschmidt S. Cdc42 and the phosphatidylinositol 3-kinase-Akt pathway are essential for PspC-mediated internalization of pneumococci by respiratory epithelial cells. J Biol Chem. 2009;284: 19427-19436. https://doi.org/10.1074/jbc.M109.003442
  16. Nerlich A, Rohde M, Talay SR, Genth H, Just I, Chhatwal GS. Invasion of endothelial cells by tissue-invasive M3 type group A streptococci requires Src kinase and activation of Rac1 by a phosphatidylinositol 3-kinase- independent mechanism. J Biol Chem. 2009;284:20319-20328. https://doi.org/10.1074/jbc.M109.016501
  17. Slanina H, Hebling S, Hauck CR, Schubert-Unkmeir A. Cell invasion by Neisseria meningitidis requires a functional interplay between the focal adhesion kinase, Src and cortactin. PLoS One. 2012;7:e39613. https://doi.org/10.1371/journal.pone.0039613
  18. Amar S, Wu SC, Madan M. Is Porphyromonas gingivalis cell invasion required for atherogenesis? Pharmacotherapeutic implications. J Immunol. 2009;182:1584-1592. https://doi.org/10.4049/jimmunol.182.3.1584
  19. Choi EK, Park SA, Oh WM, Kang HC, Kuramitsu HK, Kim BG, et al. Mechanisms of Porphyromonas gingivalisinduced monocyte chemoattractant protein-1 expression in endothelial cells. FEMS Immunol Med Microbiol. 2005; 44:51-58. https://doi.org/10.1016/j.femsim.2004.12.003
  20. Tamai R, Asai Y, Ogawa T. Requirement for intercellular adhesion molecule 1 and caveolae in invasion of human oral epithelial cells by Porphyromonas gingivalis. Infect Immun. 2005;73:6290-6298. https://doi.org/10.1128/IAI.73.10.6290-6298.2005
  21. Lanzetti L, Di Fiore PP, Scita G. Pathways linking endocytosis and actin cytoskeleton in mammalian cells. Exp Cell Res. 2001;271:45-56. https://doi.org/10.1006/excr.2001.5369
  22. Lamont RJ, Chan A, Belton CM, Izutsu KT, Vasel D, Weinberg A. Porphyromonas gingivalis invasion of gingival epithelial cells. Infect Immun. 1995;63:3878-3885.
  23. Meyer DH, Mintz KP, Fives-Taylor PM. Models of invasion of enteric and periodontal pathogens into epithelial cells: a comparative analysis. Crit Rev Oral Biol Med. 1997;8:389-409. https://doi.org/10.1177/10454411970080040301
  24. Abraham S, Shin J, Malaviya R. Type 1 fimbriated Escherichia coli-mast cell interactions in cystitis. J Infect Dis. 2001;183 Suppl 1:S51-5. https://doi.org/10.1086/318853
  25. Xue Q, Jenkins SA, Gu C, Smeds E, Liu Q, Vasan R, et al. Bacillus anthracis spore entry into epithelial cells is an actin-dependent process requiring c-Src and PI3K. PLoS One. 2010;5:e11665. https://doi.org/10.1371/journal.pone.0011665
  26. Agerer F, Michel A, Ohlsen K, Hauck CR. Integrinmediated invasion of Staphylococcus aureus into human cells requires Src family protein-tyrosine kinases. J Biol Chem. 2003;278:42524-42531. https://doi.org/10.1074/jbc.M302096200
  27. Chen L, Wang ZW, Zhu JW, Zhan X. Roles of cortactin, an actin polymerization mediator, in cell endocytosis. Acta Biochim Biophys Sin. 2006;38:95-103. https://doi.org/10.1111/j.1745-7270.2006.00141.x