Analysis of differential expression of tight junction proteins in cultured oral epithelial cells altered by Porphyromonas gingivalis, Porphyromonas gingivalis lipopolysaccharide, and extracellular adenosine triphosphate

Abstract

Defences against gum disease are bolstered via increased expression of the proteins that seal the gaps between oral epithelial cells. Previous work has indicated that these tight junction proteins are involved in gum disease, but their role is unknown. ZhongHao Liu from Binzhou Medical University, Yantai, China, and colleagues investigated how Porphyromonas gingivalis, the most common bacteria associated with gum disease, affects the expression of tight junction proteins in cultured oral epithelial cells. In the early stages of infection, the expression of several tight junction proteins increased, particularly in the presence of extracellular ATP, an indicator of nearby cell damage. The findings provide insight into the early host response to P. gingivalis, the increased expression of tight junction proteins strengthening the seal between cells as a defence against bacterial invasion.

Keywords

junctional epithelium / periodontitis / Porphyromonas gingivalis / tight junctions

References

[1] Kirschner N, Houdek P, Fromm M. Tight junctions form a barrier in human epidermis. Eur J Cell Biol, 2010, 89(11): 839-842.

[2] Balda MS, Matter K. Tight junctions. J Cell Sci, 1998, 111(5): 541-547.

[3] Sawada N. Tight junction-related human diseases. Pathol Int, 2013, 63(1): 1-12.

[4] McNeil E, Capaldo CT, Macara IG. Zonula occludens-1 function in the assembly of tight junctions in Madin-Darby canine kidney epithelial cells. Mol Biol Cell, 2006, 17(4): 1922-1932.

[5] Umeda K, Ikenouchi J, Katahira-Tayama S. ZO-1 and ZO-2 independently determine where claudins are polymerized in tight-junction strand formation. Cell, 2006, 126(4): 741-754.

[6] Monteiro AC, Parkos CA. Intracellular mediators of JAM-A-dependent epithelial barrier function. Ann N Y Acad Sci, 2012, 1257(1): 115-124.

[7] Severson EA, Parkos CA. Structural determinants of junctional adhesion molecule A (JAM-A) function and mechanisms of intracellular signaling. Curr Opin Cell Biol, 2009, 21(5): 701-707.

[8] Tsukita S, Furuse M. Occludin and claudins in tight-junction strands: leading or supporting players?. Trends Cell Biol, 1999, 9(7): 268-273.

[9] Furuse M, Tsukita S. Claudins in occluding junctions of humans and flies. Trends Cell Biol, 2006, 16(4): 181-188.

[10] Gürsoy UK, Zeidán-Chuliá F, Yilmaz D. Analyses of gingival adhesion molecules in periodontitis: theoretical in silico, comparative in vivo, and explanatory in vitro models. J Periodontol, 2016, 87(2): 193-202.

[11] Williams RC, Offenbacher S. Periodontal medicine: the emergence of a new branch of periodontology. Periodontol, 2000, 23(23): 9-12.

[12] Lindhe J, Ranney R, Lamster I. Consensus report: chronic periodontitis. Ann Periodontol, 1999, 4(1): 38.

[13] Ji S, Kim Y, Min BM. Innate immune responses of gingival epithelial cells to nonperiodontopathic and periodontopathic bacteria. J Periodontal Res, 2007, 42(6): 503-510.

[14] Guo W, Wang P, Liu ZH. The activation of pyrin domain-containing-3 inflammasome depends on lipopolysaccharide from Porphyromonas gingivalis and extracellular adenosine triphosphate in cultured oral epithelial cells. BMC Oral Health, 2015, 15(1): 133-144.

[15] Prime SS, Nixon SV, Crane IJ. The behaviour of human oral squamous cell carcinoma in cell culture. J Pathol, 1990, 160(3): 259-269.

[16] Ye P, Nadkarni MA, Hunter N. Regulation of E-cadherin and TGF-beta3 expression by CD24 in cultured oral epithelial cells. Biochem Biophys Res Commun, 2006, 349(1): 229-235.

[17] Swierenga SH, MacManus JP. Preparation of low calcium growth medium suitable for determination of tumorigenicity of cultured cells. J Tissue Culture Methods, 1982, 7(7): 1-3.

[18] Lamont RJ, Chan A, Belton CM. Porphyromonas gingivalis invasion of gingival epithelial cells. Infect Immun, 1995, 63(10): 3878-3885.

[19] Ye P. Modulation of epithelial tight junctions by TGF-beta 3 in cultured oral epithelial cells. Aust Dent J, 2012, 57(1): 11-17.

[20] Ye P, Nadkarni MA, Simonian M. CD24 regulated gene expression and distribution of tight junction proteins is associated with altered barrier function in oral epithelial monolayers. BMC Cell Biol, 2009, 10(2): 1-16.

[21] Guo W, Ye P, Yu H. CD24 activates the NLRP3 inflammasome through c-Src kinase activity in a model of the lining epithelium of inflamed periodontal tissues. Immun Inflamm Dis, 2014, 2(4): 239-253.

[22] Belibasakis GN, Kast JI, Thurnheer T. The expression of gingival epithelial junctions in response to subgingival biofilms. Virulence, 2015, 6(7): 704-709.

[23] Hajishengallis G, Lambris JD. Microbial manipulation of receptor crosstalk in innate immunity. Nat Rev Immunol, 2011, 11(3): 187-200.

[24] Hajishengallis G, Lamont RJ. Breaking bad: manipulation of the host response by Porphyromonas gingivalis. Eur J Immunol, 2014, 44(2): 328-338.

[25] Bostanci N, Bao K, Wahlander A. Secretome of gingival epithelium in response to subgingival biofilms. Mol Oral Microbiol, 2015, 30(4): 323-335.

[26] Bosshardt DD, Lang NP. The junctional epithelium: from health to disease. J Dent Res, 2005, 84(1): 9-20.

[27] Furuse M, Fujita K, Hiiragi T. Claudin-1 and -2: novel integral membrane proteins localizing at tight junctions with no sequence similarity to occludin. J Cell Biol, 1998, 141(7): 1539-1550.

[28] Günzel D, Yu AS. Claudins and the modulation of tight junction permeability. Physiol Rev, 2013, 93(2): 525-569.

[29] Günzel D, Fromm M. Claudins and other tight junction proteins. Comp Physiol, 2012, 2(3): 1819-1852.

[30] Randers-Eichhorn L, Bartlett RA, Frey DD. Noninvasive oxygen measurements and mass transfer considerations in tissue culture flasks. Biotechnol Bioeng, 1996, 51(4): 466-478.

[31] Pettersen EO, Larsen LH, Ramsing NB. Pericellular oxygen depletion during ordinary tissue culturing, measured with oxygen microsensors. Cell Prolif, 2005, 38(4): 257-267.

[32] Lewis JP, Iyer D, Anaya-Bergman C. Adaptation of Porphyromonas gingivalis to microaerophilic conditions involves increased consumption of formate and reduced utilization of lactate. Microbiology, 2009, 155(Pt 11): 3758-3774.

[33] Yilmaz O, Verbeke P, Lamont RJ. Intercellular spreading of Porphyromonas gingivalis infection in primary gingival epithelial cells. Infect Immun, 2006, 74(1): 703-710.

[34] Houalet-Jeanne S, Pellen-Mussi P, Tricot-Doleux S. Assessment of internalization and viability of Porphyromonas gingivalis in KB epithelial cells by confocal microscopy. Infect Immun, 2001, 69(11): 7146-7151.

[35] Chiang CY, Kyritsis G, Graves DT. Interleukin-1 and tumor necrosis factor activities partially account for calvarial bone resorption induced by local injection of lipopolysaccharide. Infect Immun, 1999, 67(8): 4231-4236.

[36] Garner AD, Tucci MA, Benghuzzi HA. The effectiveness of potent dental adhesives on the viability of LPS challenged human gingival fibroblasts. Biomed Sci Instrum, 2014, 50(2): 41-46.

[37] Tamura A, Kitano Y, Hata M. Megaintestine in claudin-15-deficient mice. Gastroenterology, 2008, 134(134): 523-534.

[38] Rehder D, Iden S, Nasdala I. Junctional adhesion molecule-a participates in the formation of apicobasal polarity through different domains. Exp Cell Res, 2006, 312(17): 3389-3403.

[39] Hajishengallis G. Porphyromonas gingivalis-host interactions: open war or intelligent guerilla tactics?. Microbes Infect, 2009, 11(6-7): 637-645.

[40] Yilmaz O, Sater AA, Yao L. ATP-dependent activation of an inflammasome in primary gingival epithelial cells infected by Porphyromonas gingivalis. Cell Microbiol, 2010, 12(2): 188-198.

[41] Menu P, Vince JE. The NLRP3 inflammasome in health and disease: the good, the bad and the ugly. Clin Exp Immunol, 2011, 166(1): 1-15.