TNF-α augmented Porphyromonas gingivalis invasion in human gingival epithelial cells through Rab5 and ICAM-1

BMC Microbiology

Kenji Matsushita²  Toshihide Noguchi¹  Naoyuki Ishida¹  Toshinori Komatsu²  Shinsuke Sugiura¹  Ryutaro Isoda²  Yuichi Ishihara¹  Makoto Hagiwara²  Yoshiko Kato¹ 

[1] Department of Periodontology, Aichigakuin University, Nagoya, Aichi, Japan;Department of Oral Disease Research, National Center of Geriatrics and Gerontology, Obu 747-8511, Aichi, Japan

关键词: Persistent infection;    ICAM-1;    Rab5;    TNF-?;    Endocytosis;    Porphyromonas gingivalis;   

Others  :  1170543
DOI  :  10.1186/s12866-014-0229-z

 received in 2014-02-03, accepted in 2014-08-19,  发布年份 2014

【 摘 要 】

Background

Tumor necrosis factor alpha (TNF-?) plays a central role in the initiation and maintenance of immune responses to periodontopathic bacteria. However, excess TNF-? leads to dysregulated immune responses and progression of periodontitis. Porphyromonas gingivalis (P. gingivalis) invades gingival epithelial cells and then multiplies and survives for a long period. Additionally, increment of TNF-? in periodontal sites is associated with a high prevalence of gram-negative anaerobes such as P. gingivalis. However, it has not been determined whether TNF-? affects invasion of P. gingivalis in periodontal tissues.

Results

We examined the effect of TNF-? on invasion of P. gingivalis in gingival epithelial cells and clarified the mechanism by which TNF-? augments invasion of P. gingivalis. Invasion of P. gingivalis into Ca9-22 cells was augmented by stimulation with TNF-? and it was inhibited by treatment with an antibody to TNF receptor-1. TNF-? increased production of ICAM-1, and P. gingivalis invasion was inhibited by an antibody to ICAM-1 in Ca9-22 cells. Silencing of Rab5 mRNA inhibited P. gingivalis invasion. Furthermore, the JNK inhibitor SP600125 inhibited invasion of P. gingivalis and also decreased the active form of Rab5 in Ca9-22 cells.

Conclusion

TNF-? augments invasion of P. gingivalis in human gingival epithelial cells through increment of ICAM-1 and activation of Rab5. These phenomena may contribute to persistent infection of P. ginigvalis and prolongation of immune responses in periodontal tissues.

【 授权许可】

   
2014 Kato et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Zhang W, Ju J, Rigney T, Tribble G: Integrin alpha5beta1-fimbriae binding and actin rearrangement are essential for Porphyromonas gingivalis invasion of osteoblasts and subsequent activation of the JNK pathway. BMC Microbiol 2013, 13:5.
• [2]Stafford P, Higham J, Pinnock A, Murdoch C, Douglas CW, Stafford GP, Lambert DW: Gingipain-dependent degradation of mammalian target of rapamycin pathway proteins by the periodontal pathogen Porphyromonas gingivalis during invasion. Mol Oral Microbiol 2013, 28(5):366-378.
• [3]Inaba H, Sugita H, Kuboniwa M, Iwai S, Hamada M, Noda T, Morisaki I, Lamont RJ, Amano A: Porphyromonas gingivalis promotes invasion of oral squamous cell carcinoma through induction of proMMP9 and its activation. Cell Microbiol 2014, 16(1):131-145.
• [4]Lamont RJ, Jenkinson HF: Life below the gum line: pathogenic mechanisms of Porphyromonas gingivalis. Microbiol Mol Biol Rev 1998, 62(4):1244-1263.
• [5]Lamont RJ, Yilmaz O: In or out: the invasiveness of oral bacteria. Periodontol 2000 2002, 30:61-69.
• [6]Hutagalung AH, Novick PJ: Role of Rab GTPases in membrane traffic and cell physiology. Physiol Rev 2011, 91(1):119-149.
• [7]Mukherjee K, Parashuraman S, Raje M, Mukhopadhyay A: SopE acts as an Rab5-specific nucleotide exchange factor and recruits non-prenylated Rab5 on Salmonella-containing phagosomes to promote fusion with early endosomes. J Biol Chem 2001, 276(26):23607-23615.
• [8]Mallo GV, Espina M, Smith AC, Terebiznik MR, Aleman A, Finlay BB, Rameh LE, Grinstein S, Brumell JH: SopB promotes phosphatidylinositol 3-phosphate formation on Salmonella vacuoles by recruiting Rab5 and Vps34. J Cell Biol 2008, 182(4):741-752.
• [9]Madan R, Krishnamurthy G, Mukhopadhyay A: SopE-mediated recruitment of host Rab5 on phagosomes inhibits Salmonella transport to lysosomes. Methods Mol Biol 2008, 445:417-437.
• [10]Clemens DL, Lee BY, Horwitz MA: Deviant expression of Rab5 on phagosomes containing the intracellular pathogens Mycobacterium tuberculosis and Legionella pneumophila is associated with altered phagosomal fate. Infect Immun 2000, 68(5):2671-2684.
• [11]Alvarez-Dominguez C, Barbieri AM, Beron W, Wandinger-Ness A, Stahl PD: Phagocytosed live Listeria monocytogenes influences Rab5-regulated in vitro phagosome-endosome fusion. J Biol Chem 1996, 271(23):13834-13843.
• [12]Preshaw PM, Taylor JJ: How has research into cytokine interactions and their role in driving immune responses impacted our understanding of periodontitis? J Clin Periodontol 2011, 38(Suppl 11):60-84.
• [13]Deo V, Bhongade ML: Pathogenesis of periodontitis: role of cytokines in host response. Dent Today 2010, 29(9):60-62. 64¿66; quiz 68¿69
• [14]Andrukhov O, Ulm C, Reischl H, Nguyen PQ, Matejka M, Rausch-Fan X: Serum cytokine levels in periodontitis patients in relation to the bacterial load. J Periodontol 2011, 82(6):885-892.
• [15]El Oudi M, Bouguerra C, Aouni Z, Mazigh C, Bellaaj R, Machghoul S: Homocysteine and inflammatory biomarkers plasma levels, and severity of acute coronary syndrome. Ann Biol Clin (Paris) 2011, 69(2):175-180.
• [16]Goldberg RB: Cytokine and cytokine-like inflammation markers, endothelial dysfunction, and imbalanced coagulation in development of diabetes and its complications. J Clin Endocrinol Metab 2009, 94(9):3171-3182.
• [17]Gotsman I, Stabholz A, Planer D, Pugatsch T, Lapidus L, Novikov Y, Masrawa S, Soskolne A, Lotan C: Serum cytokine tumor necrosis factor-alpha and interleukin-6 associated with the severity of coronary artery disease: indicators of an active inflammatory burden? Isr Med Assoc J 2008, 10(7):494-498.
• [18]Spranger J, Kroke A, Mohlig M, Hoffmann K, Bergmann MM, Ristow M, Boeing H, Pfeiffer AF: Inflammatory cytokines and the risk to develop type 2 diabetes: results of the prospective population-based European Prospective Investigation into Cancer and Nutrition (EPIC)-Potsdam Study. Diabetes 2003, 52(3):812-817.
• [19]Gigante A, Gasperini ML, Afeltra A, Barbano B, Margiotta D, Cianci R, De Francesco I, Amoroso A: Cytokines expression in SLE nephritis. Eur Rev Med Pharmacol Sci 2011, 15(1):15-24.
• [20]McDevitt H, Munson S, Ettinger R, Wu A: Multiple roles for tumor necrosis factor-alpha and lymphotoxin alpha/beta in immunity and autoimmunity. Arthritis Res 2002, 4(Suppl 3):S141-S152.
• [21]Jing Y, Ma N, Fan T, Wang C, Bu X, Jiang G, Li R, Gao L, Li D, Wu M, Wei L: Tumor necrosis factor-alpha promotes tumor growth by inducing vascular endothelial growth factor. Cancer Invest 2011, 29(7):485-493.
• [22]Grimm M, Lazariotou M, Kircher S, Hofelmayr A, Germer CT, von Rahden BH, Waaga-Gasser AM, Gasser M: Tumor necrosis factor-alpha is associated with positive lymph node status in patients with recurrence of colorectal cancer-indications for anti-TNF-alpha agents in cancer treatment. Cell Oncol 2011, 34(4):315-326.
• [23]Kurtis B, Tuter G, Serdar M, Akdemir P, Uygur C, Firatli E, Bal B: Gingival crevicular fluid levels of monocyte chemoattractant protein-1 and tumor necrosis factor-alpha in patients with chronic and aggressive periodontitis. J Periodontol 2005, 76(11):1849-1855.
• [24]Gorska R, Gregorek H, Kowalski J, Laskus-Perendyk A, Syczewska M, Madalinski K: Relationship between clinical parameters and cytokine profiles in inflamed gingival tissue and serum samples from patients with chronic periodontitis. J Clin Periodontol 2003, 30(12):1046-1052.
• [25]Havemose-Poulsen A, Sorensen LK, Stoltze K, Bendtzen K, Holmstrup P: Cytokine profiles in peripheral blood and whole blood cell cultures associated with aggressive periodontitis, juvenile idiopathic arthritis, and rheumatoid arthritis. J Periodontol 2005, 76(12):2276-2285.
• [26]Bradley JR: TNF-mediated inflammatory disease. J Pathol 2008, 214(2):149-160.
• [27]Berk BC, Abe JI, Min W, Surapisitchat J, Yan C: Endothelial atheroprotective and anti-inflammatory mechanisms. Ann N Y Acad Sci 2001, 947:93-109. discussion 109¿111
• [28]Yehuda H, Szuchman-Sapir A, Khatib S, Musa R, Tamir S: Human atherosclerotic plaque lipid extract promotes expression of proinflammatory factors in human monocytes and macrophage-like cells. Atherosclerosis 2011, 218(2):339-343.
• [29]Schett G: Effects of inflammatory and anti-inflammatory cytokines on the bone. Eur J Clin Invest 2011, 41(12):1361-1366.
• [30]Ungvari Z, Csiszar A, Edwards JG, Kaminski PM, Wolin MS, Kaley G, Koller A: Increased superoxide production in coronary arteries in hyperhomocysteinemia: role of tumor necrosis factor-alpha, NAD (P) H oxidase, and inducible nitric oxide synthase. Arterioscler Thromb Vasc Biol 2003, 23(3):418-424.
• [31]Sandros J, Karlsson C, Lappin DF, Madianos PN, Kinane DF, Papapanou PN: Cytokine responses of oral epithelial cells to Porphyromonas gingivalis infection. J Dent Res 2000, 79(10):1808-1814.
• [32]Vandenabeele P, Declercq W, Beyaert R, Fiers W: Two tumour necrosis factor receptors: structure and function. Trends Cell Biol 1995, 5(10):392-399.
• [33]Tartaglia LA, Goeddel DV: Two TNF receptors. Immunol Today 1992, 13(5):151-153.
• [34]Hannigan MO, Huang CK, Wu DQ: Roles of PI3K in neutrophil function. Curr Top Microbiol Immunol 2004, 282:165-175.
• [35]Nizamutdinova IT, Jeong JJ, Xu GH, Lee SH, Kang SS, Kim YS, Chang KC, Kim HJ: Hesperidin, hesperidin methyl chalone and phellopterin from Poncirus trifoliata (Rutaceae) differentially regulate the expression of adhesion molecules in tumor necrosis factor-alpha-stimulated human umbilical vein endothelial cells. Int Immunopharmacol 2008, 8(5):670-678.
• [36]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(10):6290-6298.
• [37]Bucci C, Lutcke A, Steele-Mortimer O, Olkkonen VM, Dupree P, Chiariello M, Bruni CB, Simons K, Zerial M: Co-operative regulation of endocytosis by three Rab5 isoforms. FEBS Lett 1995, 366(1):65-71.
• [38]Sturgill-Koszycki S, Schaible UE, Russell DG: Mycobacterium-containing phagosomes are accessible to early endosomes and reflect a transitional state in normal phagosome biogenesis. EMBO J 1996, 15(24):6960-6968.
• [39]Alvarez-Dominguez C, Stahl PD: Increased expression of Rab5a correlates directly with accelerated maturation of Listeria monocytogenes phagosomes. J Biol Chem 1999, 274(17):11459-11462.
• [40]Watanabe K, Yilmaz O, Nakhjiri SF, Belton CM, Lamont RJ: Association of mitogen-activated protein kinase pathways with gingival epithelial cell responses to Porphyromonas gingivalis infection. Infect Immun 2001, 69(11):6731-6737.
• [41]Bhattacharya M, Ojha N, Solanki S, Mukhopadhyay CK, Madan R, Patel N, Krishnamurthy G, Kumar S, Basu SK, Mukhopadhyay A: IL-6 and IL-12 specifically regulate the expression of Rab5 and Rab7 via distinct signaling pathways. EMBO J 2006, 25(12):2878-2888.
• [42]Della Rocca GJ, Mukhin YV, Garnovskaya MN, Daaka Y, Clark GJ, Luttrell LM, Lefkowitz RJ, Raymond JR: Serotonin 5-HT1A receptor-mediated Erk activation requires calcium/calmodulin-dependent receptor endocytosis. J Biol Chem 1999, 274(8):4749-4753.
• [43]Vogler O, Nolte B, Voss M, Schmidt M, Jakobs KH, van Koppen CJ: Regulation of muscarinic acetylcholine receptor sequestration and function by beta-arrestin. J Biol Chem 1999, 274(18):12333-12338.
• [44]Whistler JL, von Zastrow M: Dissociation of functional roles of dynamin in receptor-mediated endocytosis and mitogenic signal transduction. J Biol Chem 1999, 274(35):24575-24578.
• [45]McPherson PS, Kay BK, Hussain NK: Signaling on the endocytic pathway. Traffic 2001, 2(6):375-384.
• [46]Nizamutdinova IT, Oh HM, Min YN, Park SH, Lee MJ, Kim JS, Yean MH, Kang SS, Kim YS, Chang KC, Kim HJ: Paeonol suppresses intercellular adhesion molecule-1 expression in tumor necrosis factor-alpha-stimulated human umbilical vein endothelial cells by blocking p38, ERK and nuclear factor-kappaB signaling pathways. Int Immunopharmacol 2007, 7(3):343-350.
• [47]Amano A: Bacterial adhesins to host components in periodontitis. Periodontol 2000 2010, 52(1):12-37.
• [48]Nakagawa I, Amano A, Kuboniwa M, Nakamura T, Kawabata S, Hamada S: Functional differences among FimA variants of Porphyromonas gingivalis and their effects on adhesion to and invasion of human epithelial cells. Infect Immun 2002, 70(1):277-285.
• [49]Chen T, Nakayama K, Belliveau L, Duncan MJ: Porphyromonas gingivalis gingipains and adhesion to epithelial cells. Infect Immun 2001, 69(5):3048-3056.
• [50]Weinberg A, Belton CM, Park Y, Lamont RJ: Role of fimbriae in Porphyromonas gingivalis invasion of gingival epithelial cells. Infect Immun 1997, 65(1):313-316.
• [51]Watarai M, Funato S, Sasakawa C: Interaction of Ipa proteins of Shigella flexneri with alpha5beta1 integrin promotes entry of the bacteria into mammalian cells. J Exp Med 1996, 183(3):991-999.
• [52]Roger P, Puchelle E, Bajolet-Laudinat O, Tournier JM, Debordeaux C, Plotkowski MC, Cohen JH, Sheppard D, de Bentzmann S: Fibronectin and alpha5beta1 integrin mediate binding of Pseudomonas aeruginosa to repairing airway epithelium. Eur Respir J 1999, 13(6):1301-1309.
• [53]Ishibashi Y, Relman DA, Nishikawa A: Invasion of human respiratory epithelial cells by Bordetella pertussis: possible role for a filamentous hemagglutinin Arg-Gly-Asp sequence and alpha5beta1 integrin. Microb Pathog 2001, 30(5):279-288.
• [54]Hellstrom U, Hallberg EC, Sandros J, Rydberg L, Backer AE: Carbohydrates act as receptors for the periodontitis-associated bacterium Porphyromonas gingivalis: a study of bacterial binding to glycolipids. Glycobiology 2004, 14(6):511-519.
• [55]Krunkosky TM, Fischer BM, Akley NJ, Adler KB: Tumor necrosis factor alpha (TNF alpha)-induced ICAM-1 surface expression in airway epithelial cells in vitro: possible signal transduction mechanisms. Ann N Y Acad Sci 1996, 796:30-37.
• [56]Hashimoto M, Shingu M, Ezaki I, Nobunaga M, Minamihara M, Kato K, Sumioki H: Production of soluble ICAM-1 from human endothelial cells induced by IL-1 beta and TNF-alpha. Inflammation 1994, 18(2):163-173.
• [57]Hagiwara M, Shirai Y, Nomura R, Sasaki M, Kobayashi K, Tadokoro T, Yamamoto Y: Caveolin-1 activates Rab5 and enhances endocytosis through direct interaction. Biochem Biophys Res Commun 2009, 378(1):73-78.
• [58]Hagiwara M, Shinomiya H, Kashihara M, Kobayashi K, Tadokoro T, Yamamoto Y: Interaction of activated Rab5 with actin-bundling proteins, L- and T-plastin and its relevance to endocytic functions in mammalian cells. Biochem Biophys Res Commun 2011, 407(3):615-619.
• [59]Lamont RJ, Chan A, Belton CM, Izutsu KT, Vasel D, Weinberg A: Porphyromonas gingivalis invasion of gingival epithelial cells. Infect Immun 1995, 63(10):3878-3885.
• [60]Liu J, Lamb D, Chou MM, Liu YJ, Li G: Nerve growth factor-mediated neurite outgrowth via regulation of Rab5. Mol Biol Cell 2007, 18(4):1375-1384.