Porphyromonas gingivalis promotes invasion of oral squamous cell carcinoma through induction of proMMP9 and its activation

Cellular Microbiology

Volumn 16, Issue 1, 2014, Pages 131-145

  Inaba, Hiroaki ^a   Sugita, Hideyuki ^a,b   Kuboniwa, Masae ^a   Iwai, Soichi ^a   Hamada, Masakazu ^a   Noda, Takeshi ^a   Morisaki, Ichijiro ^b   Lamont, Richard J ^c   Amano, Atsuo ^a  

^a OSAKA UNIVERSITY   (Japan)

^b OSAKA UNIVERSITY DENTAL HOSPITAL   (Japan)

^c UNIVERSITY OF LOUISVILLE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYME PRECURSOR; GELATINASE B; HEAT SHOCK PROTEIN 27; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MATRIX METALLOPROTEINASE 14; MITOGEN ACTIVATED PROTEIN KINASE 1; PROTEINASE ACTIVATED RECEPTOR 2; SYNAPTOPHYSIN;

ARTICLE; CELL INVASION; CONTROLLED STUDY; ENZYME ACTIVATION; FUSOBACTERIUM NUCLEATUM; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; LYMPH NODE METASTASIS; MOUTH SQUAMOUS CELL CARCINOMA; NONHUMAN; PERIODONTITIS; PORPHYROMONAS GINGIVALIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SUPERNATANT; TUMOR INVASION;

FUSOBACTERIUM NUCLEATUM; PORPHYROMONAS GINGIVALIS;

CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; ENZYME ACTIVATION; FUSOBACTERIUM NUCLEATUM; GENE EXPRESSION; HOST-PATHOGEN INTERACTIONS; HUMANS; MATRIX METALLOPROTEINASE 9; MOUTH NEOPLASMS; PORPHYROMONAS GINGIVALIS; SIGNAL TRANSDUCTION; TRANSCRIPTIONAL ACTIVATION;

EID: 84890235809     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/cmi.12211     Document Type: Article

References (78)

1. Aas, J.A., Paster, B.J., Stokes, L.N., Olsen, I., and Dewhirst, F.E. (2005) Defining the normal bacterial flora of the oral cavity. J Clin Microbiol 43: 5721-5732.
2. Ahn, J., Segers, S., and Hayes, R.B. (2012) Periodontal disease, Porphyromonas gingivalis serum antibody levels and orodigestive cancer mortality. Carcinogenesis 33: 1055-1058.
3. Andrian, E., Mostefaoui, Y., Rouabhia, M., and Grenier, D. (2007) Regulation of matrix metalloproteinases and tissue inhibitors of matrix metalloproteinases by Porphyromonas gingivalis in an engineered human oral mucosa model. J Cell Physiol 211: 56-62.
4. Baker, E.A., Leaper, D.J., Hayter, J.P., and Dickenson, A.J. (2007) Plasminogen activator system in oral squamous cell carcinoma. Br J Oral Maxillofac Surg 45: 623-627.
5. Barbolina, M.V., and Stack, M.S. (2008) Membrane type-1 matrix metalloproteinase: substrate diversity in pericellular proteolysis. Seminars in cell and developmental biology. Semin Cell Dev Biol 19: 24-33.
6. Caruso, R., Pallone, F., Fina, D., Gioia, V., Peluso, I., Caprioli, F., etal. (2006) Protease-activated receptor-2 activation in gastric cancer cells promotes epidermal growth factor receptor trans-activation and proliferation. Am J Pathol 169: 268-278.
7. Castellarin, M., Warren, R.L., Freeman, J.D., Dreolini, L., Krzywinski, M., Barnes, R., etal. (2012) Fusobacterium nucleatum infection is prevalent in human colorectal carcinoma. Genome Res 22: 299-306.
8. Chandler, K., Vance, C., Budnick, S., and Muller, S. (2011) Muscle invasion in oral tongue squamous cell carcinoma as a predictor of nodal status and local recurrence: just as effective as depth of invasion? Head Neck Pathol 5: 359-363.
9. Cheung, L.W., Leung, P.C., and Wong, A.S. (2006) Gonadotropin-releasing hormone promotes ovarian cancer cell invasiveness through c-Jun NH2-terminal kinase-mediated activation of matrix metalloproteinase (MMP)-2 and MMP-9. Cancer Res 66: 10902-10910.
10. Crawford, H.C., Scoggins, C.R., Washington, M.K., Matrisian, L.M., and Leach, S.D. (2002) Matrix metalloproteinase-7 is expressed by pancreatic cancer precursors and regulates acinar-to-ductal metaplasia in exocrine pancreas. J Clin Invest 109: 1437-1444.
11. Dejean, E., Foisseau, M., Lagarrigue, F., Lamant, L., and Prade, N. (2012) ALK+ALCLs induce cutaneous, HMGB-1-dependent IL-8/CXCL8 production by keratinocytes through NF-κB activation. Blood 119: 4698-4707.
12. Dittmer, J. (2003) The biology of the Ets1 proto-oncogene. Mol Cancer 2: 29. http://www.molecular-cancer.com/content/2/1/29.
13. Duncan, M.E., Richardson, J.P., Murray, G.I., Melvin, W.T., and Fothergill, J.E. (1998) Human matrix metalloproteinase-9: activation by limited trypsin treatment and generation of monoclonal antibodies specific for the activated form. Eur J Biochem 258: 37-43.
14. Fitzpatrick, S.G., and Katz, J. (2010) The association between periodontal disease and cancer: a review of the literature. J Dent 38: 83-95.
15. Friedl, P., and Wolf, K. (2003) Tumour-cell invasion and migration: diversity and escape mechanisms. Nat Rev Cancer 3: 362-374.
16. Fyfe, M., Bergström, M., Aspengren, S., and Peterson, A. (2005) PAR-2 activation in intestinal epithelial cells potentiates interleukin-1beta-induced chemokine secretion via MAP kinase signaling pathways. Cytokine 31: 358-367.
17. Ghosh, S., Basu, M., and Roy, S.S. (2012) ETS-1 protein regulates vascular endothelial growth factor-induced matrix metalloproteinase-9 and matrix metalloproteinase-13 expression in human ovarian carcinoma cell line SKOV-3. J Biol Chem 287: 15001-15015.
18. Groeger, S., Domann, E., Gonzales, J.R., Chakraborty, T., and Meyle, J. (2011) B7-H1 and B7-DC receptors of oral squamous carcinoma cells are upregulated by Porphyromonas gingivalis. Immunobiology 216: 1302-1310.
19. Guo, D., Zhou, H., Wu, Y., Zhou, F., Xu, G., Wen, H., and Zhang, X. (2011) Involvement of ERK1/2/NF-κB signal transduction pathway in TF/FVIIa/PAR2-induced proliferation and migration of colon cancer cell SW620. Tumour Biol 32: 921-930.
20. Guo, K., Liu, Y., Zhou, H., Dai, Z., Zhang, J., Sun, R., etal. (2008) Involvement of protein kinase C beta-extracellular signal-regulating kinase 1/2/p38 mitogen-activated protein kinase-heat shock protein 27 activation in hepatocellular carcinoma cell motility and invasion. Cancer Sci 99: 486-496.
21. Guo, Y., Nquyen, K.A., and Potempa, J. (2010) Dichotomy of gingipains action as virulence factors: from cleaving substrates with the precision of a surgeon's knife to a meat chopper-like brutal degradation of proteins. Periodontol 2000 54: 15-44.
22. Hahne, J.C., Okuducu, A.F., Kaminski, A., Florin, A., Soncin, F., and Wernert, N. (2005) Ets-1 expression promotes epithelial cell transformation by inducing migration, invasion and anchorage-independent growth. Oncogene 24: 5384-5388.
23. Hansen, R.K., Parra, I., Hilsenbeck, S.G., Himelstein, B., and Fuqua, S.A. (2001) HSP27-induced MMP-9 expression is influenced by the Src tyrosine protein kinase yes. Biochem Biophys Res Commun 282: 186-193.
24. Hjortoe, G.M., Petersen, L.C., Albrektsen, T., Sorensen, B.B., Norby, P.L., Mandal, S.K., etal. (2004) Tissue factor-factor VIIa-specific up-regulation of IL-8 expression in MDA-MB-231 cells is mediated by PAR-2 and results in increased cell migration. Blood 103: 3029-3037.
25. Inaba, H., Kawai, S., Nakayama, K., Okahashi, N., and Amano, A. (2004) Effect of enamel matrix derivative on periodontal ligament cells in vitro is diminished by Porphyromonas gingivalis. J Periodontol 75: 858-865.
26. Inaba, H., Kuboniwa, M., Bainbridge, B., Yilmaz, O., Katz, J., Shiverick, K.T., etal. (2009) Porphyromonas gingivalis invades human trophoblasts and inhibits proliferation by inducing G1 arrest and apoptosis. Cell Microbiol 11: 1517-1532.
27. Jaeschke, A., Karasarides, M., Ventura, J.J., Ehrhardt, A., Zhang, C., Flavell, R.A., etal. (2006) JNK2 is a positive regulator of the cJun transcription factor. Mol Cell 23: 899-911.
28. Jemal, A., Bray, F., Center, M.M., Ferlay, J., Ward, E., and Forman, D. (2011) Global cancer statistics. CA Cancer J Clin 61: 69-90.
29. Jotwani, R., Eswaran, S.V., Moonga, S., and Cutler, C.W. (2010) MMP-9/TIMP-1 imbalance induced in human dendritic cells by Porphyromonas gingivalis. FEMS Immunol Med Microbiol 58: 314-321.
30. Kanke, T., Takizawa, T., Kabeya, M., and Kawabata, A. (2005) Physiology and pathophysiology of proteinase-activated receptors (PARs): PAR-2 as a potential therapeutic target. J Pharmacol Sci 97: 38-42.
31. Kato, T., Okahashi, N., Kawai, S., Kato, T., Inaba, H., Morisaki, I., and Amano, A. (2005) Impaired degradation of matrix collagen in human gingival fibroblasts by the antiepileptic drug phenytoin. J Periodontol 76: 941-950.
32. Katz, J., Onate, M.D., Pauley, K.M., Bhattacharyya, I., and Cha, S. (2011) Presence of Porphyromonas gingivalis in gingival squamous cell carcinoma. Int J Oral Sci 3: 209-215.
33. Kida, Y., Inoue, H., Shimizu, T., and Kuwano, K. (2007) Serratia marcescens serralysin induces inflammatory responses through protease-activated receptor 2. Infect Immun 75: 164-174.
34. Krüger, A., Arlt, M.J., Gerg, M., Kopitz, C., Bernardo, M.M., Chang, M., etal. (2005) Antimetastatic activity of a novel mechanism-based gelatinase inhibitor. Cancer Res 65: 3523-3526.
35. Kumar, B., Koul, S., Petersen, J., Khandrika, L., Hwa, J.S., Meacham, R.B., etal. (2010) p38 mitogen-activated protein kinase-driven MAPKAPK2 regulates invasion of bladder cancer by modulation of MMP-2 and MMP-9 activity. Cancer Res 70: 832-841.
36. Lanzós, I., Herrera, D., Santos, S., O'Connor, A., Peña, C., Lanzós, E., and Sanz, M. (2011) Microbiological effects of an antiseptic mouthrinse in irradiated cancer patients. Med Oral Patol Oral Cir Bucal 16: e1036-e1042.
37. Lee, S.E., Kim, J.M., Jeong, S.K., Jeon, J.E., Yoon, H.J., Jeong, M.K., and Lee, S.H. (2010) Protease-activated receptor-2 mediates the expression of inflammatory cytokines, antimicrobial peptides, and matrix metalloproteinases in keratinocytes in response to Propionibacterium acnes. Arch Dermatol Res 302: 745-756.
38. Li, Z., Bian, L.J., Li, Y., Liang, Y.J., and Liang, H.Z. (2009) Expression of protease-activated receptor-2 (PAR-2) in patients with nasopharyngeal carcinoma: correlation with clinicopathological features and prognosis. Pathol Res Pract 205: 542-550.
39. Lijnen, H.R. (2001) Plasmin and matrix metalloproteinases in vascular remodeling. Thromb Haemost 86: 324-333.
40. Liu, S., Liang, Y., Huang, H., Wang, L., Li, Y., Li, J., etal. (2005) ERK-dependent signaling pathway and transcriptional factor Ets-1 regulate matrix metalloproteinase-9 production in transforming growth factor-beta1 stimulated glomerular podocytes. Cell Physiol Biochem 16: 207-216.
41. Loesch, M., Zhi, H.Y., Hou, S.W., Qi, X.M., Li, R.S., Basir, Z., etal. (2010) p38gamma MAPK cooperates with c-Jun in trans-activating matrix metalloproteinase 9. J Biol Chem 285: 15149-15158.
42. Lu, K.W., Chen, J.C., Lai, T.Y., Yang, J.S., Weng, S.W., Ma, Y.S., etal. (2011) Gypenosides inhibits migration and invasion of human oral cancer SAS cells through the inhibition of matrix metalloproteinase-2 -9 and urokinase-plasminogen by ERK1/2 and NF-kappa B signaling pathways. Hum Exp Toxicol 30: 406-415.
43. Mager, D.L., Haffajee, A.D., Devlin, P.M., Norris, C.M., Posner, M.R., and Goodson, J.M. (2005) The salivary microbiota as a diagnostic indicator of oral cancer: a descriptive, non-randomized study of cancer-free and oral squamous cell carcinoma subjects. J Transl Med 3: 27. http://www.translational-medicine.com/content/3/1/27.
44. Maruyama, T., Yamanaka, R., Yokoi, A., Ekuni, D., Tomofuji, T., Mizukawa, N., etal. (2012) Relationship between serum albumin concentration and periodontal condition in patients with head and neck cancer. J Periodontol 83: 1110-1115.
45. Miyazaki, Y., Kikuchi, K., González-Alva, P., Inoue, H., Noguchi, Y., Tsuchiya, H., etal. (2010) Association of butyric acid produced by periodontopathic bacteria with progression of oral cancer. J Cancer Sci Ther 2: 26-32.
46. Mu, C.Y., Huang, J.A., Chen, Y., Chen, C., and Zhang, X.G. (2011) High expression of PD-L1 in lung cancer may contribute to poor prognosis and tumor cells immune escape through suppressing tumor infiltrating dendritic cells maturation. Med Oncol 28: 682-688.
47. Nakayama, K., Kadowaki, T., Okamoto, K., and Yamamoto, K. (1995) Construction and characterization of arginine-specific cysteine proteinase (Arg-gingipain)-deficient mutants of Porphyromonas gingivalis. Evidence for significant contribution of Arg-gingipain to virulence. J Biol Chem 270: 23619-23626.
48. Okamoto, K., Nakayama, K., Kadowaki, T., Abe, N., Ratnayake, D.B., and Yamamoto, K. (1998) Involvement of a lysine-specific cysteine proteinase in hemoglobin adsorption and heme accumulation by Porphyromonas gingivalis. J Biol Chem 273: 21225-21231.
49. Oliveira, M.J., Costa, A.C., Costa, A.M., Henriques, L., Suriano, G., Atherton, J.C., etal. (2006) Helicobacter pylori induces gastric epithelial cell invasion in a c-Met and type IV secretion system-dependent manner. Biol Chem 281: 34888-34896.
50. Petti, S. (2009) Lifestyle risk factors for oral cancer. Oral Oncol 45: 340-350.
51. Raffetto, J.D., and Khalil, R.A. (2008) Matrix metalloproteinases and their inhibitors in vascular remodeling and vascular disease. Biochem Pharmacol 75: 346-359.
52. Ramos-DeSimone, N., Hahn-Dantona, E., Sipley, J., Nagase, H., French, D.L., and Quigley, J.P. (1999) Activation of matrix metalloproteinase-9 (MMP-9) via a converging plasmin/stromelysin-1 cascade enhances tumor cell invasion. J Biol Chem 274: 13066-13076.
53. Ramu, P., Lobo, L.A., Kukkonen, M., Bjur, E., Suomalainen, M., Raukola, H., etal. (2008) Activation of pro-matrix metalloproteinase-9 and degradation of gelatin by the surface protease PgtE of Salmonella enterica serovar Typhimurium. Int J Med Microbiol 298: 263-278.
54. Scian, R., Barrionuevo, P., Giambartolomei, G.H., De Simone, E.A., Vanzulli, S.I., Fossati, C.A., etal. (2011) Potential role of fibroblast-like synoviocytes in joint damage induced by Brucella abortus infection through production and induction of matrix metalloproteinases. Infect Immun 79: 3619-3632.
55. Seitz, I., Hess, S., Schulz, H., Eckl, R., Busch, G., Montens, H.P., etal. (2007) Membrane-type serine protease-1/matriptase induces interleukin-6 and -8 in endothelial cells by activation of protease-activated Serratia marcescens receptor-2: potential implications in atherosclerosis. Arterioscler Thromb Vasc Biol 27: 769-775.
56. Seth, A., and Watson, D.K. (2005) ETS transcription factors and their emerging roles in human cancer. Eur J Cancer 41: 2462-2478.
57. Shi, X., Gangadharan, B., Brass, L.F., Ruf, W., and Mueller, B.M. (2004) Protease-activated receptors (PAR1 and PAR2) contribute to tumor cell motility and metastasis. Mol Cancer Res 2: 395-402.
58. Shi, Y., Ratnayake, D.B., Okamoto, K., Abe, N., Yamamoto, K., and Nakayama, K. (1999) Genetic analyses of proteolysis, hemoglobin binding, and hemagglutination of Porphyromonas gingivalis. Construction of mutants with a combination of rgpA, rgpB, kgp, and hagA. J Biol Chem 274: 17955-17960.
59. Shin, K.D., Lee, M.Y., Shin, D.S., Lee, S., Son, K.H., Koh, S., etal. (2005) Blocking tumor cell migration and invasion with biphenyl isoxazole derivative KRIBB3, a synthetic molecule that inhibits Hsp27 phosphorylation. J Biol Chem 280: 41439-41448.
60. Shindoh, M., Higashino, F., Kaya, M., Yasuda, M., Funaoka, K., Hanzawa, M., etal. (1996) Correlated expression of matrix metalloproteinases and ets family transcription factor E1A-F in invasive oral squamous-cell-carcinoma-derived cell lines. Am J Pathol 148: 693-700.
61. da Silva, S.D., Ferlito, A., Takes, R.P., Brakenhoff, R.H., and Valentin, M.D. (2011) Advances and applications of oral cancer basic research. Oral Oncol 47: 783-791.
62. Sternlicht, M.D., and Wer, Z. (2001) How matrix metalloproteinases regulate cell behavior. Annu Rev Cell Dev Biol 17: 463-516.
63. Stewart, B.W., Greim, H., Shuker, D., and Kauppinen, T. (2003) Defence of IARC monographs. Lancet 361: 13003-13006.
64. St-Onge, M., Lagarde, S., Laflamme, C., Rollet-Labelle, E., Marois, L., Naccache, P.H., and Pouliot, M. (2010) Proteinase-activated receptor-2 up-regulation by Fcgamma-receptor activation in human neutrophils. FASEB J 24: 2116-2125.
65. Svensson, K.J., Kucharzewska, P., Christianson, H.C., Sköld, S., Löfstedt, T., Johansson, M.C., etal. (2011) Hypoxia triggers a proangiogenic pathway involving cancer cell microvesicles and PAR-2-mediated heparin-binding EGF signaling in endothelial cells. Proc Natl Acad Sci USA 108: 13147-13152.
66. Tamura, F., Nakagawa, R., Akuta, T., Okamoto, S., Hamada, S., Maeda, H., etal. (2004) Proapoptotic effect of proteolytic activation of matrix metalloproteinases by Streptococcus pyogenes thiol proteinase (Streptococcus pyrogenic exotoxin B). Infect Immun 72: 4836-4847.
67. Tancharoen, S., Sarker, K.P., Imamura, T., Biswas, K.K., Matsushita, K., Tatsuyama, S., etal. (2005) Neuropeptide release from dental pulp cells by RgpB via proteinase-activated receptor-2 signaling. J Immunol 174: 5796-5804.
68. Tezal, M., Scannapieco, F.A., Wactawski-Wende, J., Hyland, A., Marshall, J.R., Rigual, N.R., and Stoler, D.L. (2007) Chronic periodontitis and the risk of tongue cancer. Arch Otolaryngol Head Neck Surg 133: 450-454.
69. Tezal, M., Sullivan, M.A., Hyland, A., Marshall, J.R., Stoler, D., Reid, M.E., etal. (2009) Chronic periodontitis and the incidence of head and neck squamous cell carcinoma. Cancer Epidemiol Biomarkers Prev 18: 2406-2412.
70. Thompson, R.H., Dong, H., and Kwon, E.D. (2007) Implications of B7-H1 expression in clear cell carcinoma of the kidney for prognostication and therapy. Clin Cancer Res 13: 709s-715s.
71. Vliagoftis, H., Schwingshackl, A., Milne, C.D., Duszyk, M., Hollenberg, M.D., Wallace, J.L., etal. (2000) Proteinase-activated receptor-2-mediated matrix metalloproteinase-9 release from airway epithelial cells. J Allergy Clin Immunol 106: 537-545.
72. Wagner, E.F., and Nebreda, A.R. (2009) Signal integration by JNK and p38 MAPK pathways in cancer development. Nat Rev Cancer 9: 537-549.
73. Wasserman, S.A. (1993) A conserved signal transduction pathway regulating the activity of the rel-like proteins dorsal and NF-kappa B. Mol Biol Cell 4: 767-771.
74. Westermarck, J., and Kähäri, V.M. (1999) Regulation of matrix metalloproteinase expression in tumor invasion. FASEB J 13: 781-792.
75. Wilson, S.R., Gallagher, S., Warpeha, K., and Hawthorne, S.J. (2004) Amplification of MMP-2 and MMP-9 production by prostate cancer cell lines via activation of protease-activated receptors. Prostate 60: 168-174.
76. Wright, C., Pilkington, R., Callaghan, M., and McClean, S. (2011) Activation of MMP-9 by human lung epithelial cells in response to the cystic fibrosis-associated pathogen Burkholderia cenocepacia reduced wound healing in vitro. Am J Physiol Lung Cell Mol Physiol 301: L575-L586.
77. Zhang, J.Y., and Selim, M.A. (2012) The role of the c-Jun N-terminal Kinase signaling pathway in skin cancer. Am J Cancer Res 2: 691-698.
78. Zhou, J., Zhang, J., and Chao, J. (2012) Porphyromonas gingivalis promotes monocyte migration by activating MMP-9. J Periodontal Res 47: 236-242.