Matrix remodeling response of human periodontal tissue cells toward fibrosis upon nicotine exposure
Shigaku = Odontology - 2014
Tóm tắt
It is widely accepted that fibrosis is frequently observed in the gingiva of smokers. However, the mechanisms by which smoking results in pathological changes in periodontal tissue that lead to fibrosis are not entirely clear. Our former report showed that type I collagen synthesis was promoted by nicotine via CCN family protein 2 in human periodontal tissue cells. Here, we evaluated other aspects of nicotine function from a viewpoint of extracellular matrix (ECM) remodeling. Human gingival fibroblasts (n = 4) and periodontal ligament cells (n = 3) were isolated. The cells were treated with nicotine at a variety of concentrations for 12–48 h. Modulators of matrix remodeling were measured using enzyme-linked immunosorbent assays. Cell migration and morphology were also evaluated. As a result, following treatment with 1 μg/ml nicotine, tissue inhibitor of metalloproteinase-1 and transforming growth factor-β1 production in both cell lysates and supernatants, and matrix metalloproteinases-1 production in cell lysates, were significantly increased (p < 0.05). Compared to controls, cell migration was significantly inhibited (p < 0.005) by nicotine in a time-dependent manner. Electron microscopic analysis revealed the presence of a number of vacuoles in nicotine-treated cells. These results indicate that nicotine not only impairs fibroblast motility, and induces cellular degenerative changes, but also alters ECM-remodeling systems of periodontal cells. Induction of matrix remodeling molecules, combined with type I collagen accumulation, may account for the molecular mechanism of nicotine-induced periodontal fibrosis.
Từ khóa
Tài liệu tham khảo
Richard P, Mena S. Clinical periodontology and implant dentistry fifth edition chapter 12 modifying factors. In: Jan L, Niklaus PL, Thorkild K, editors. Copenhagen: Blackwell Munksgaard; 2008.
Linden GJ, Mullally BH. Cigarette smoking and periodontal destruction in young adults. J Periodontol. 1994;65:718–23.
Krall EA, Hayes C, Garvey AJ, Garcia RI. Study finds a correlation between smoking and tooth loss. J Mass Dent Soc. 1997;46:20–3.
Barbour SE, Nakashima K, Zhang JB, et al. Tobacco and smoking: environmental factors that modify the host response (immune system) and have an impact on periodontal health. Crit Rev Oral Biol Med. 1997;4:437–60.
American Academy of Periodontology. Position paper: tobacco use and the periodontal patient. J Periodontol. 1996;67:51–6.
Bergström J. Tobacco smoking and chronic destructive periodontal disease. Odontology. 2004;92:1–8.
Alomari Q, Barrieshi-Nusair K, Said K. Smoking prevalence and its effect on dental health attitudes and behavior among dental students. Med Princ Pract. 2006;15:195–9.
Araki S, Murata K, Ushio K, Sakai R. Dose-response relationship between tobacco consumption and melanin pigmentation in the attached gingiva. Arch Environ Health. 1983;8:375–8.
Gültekin SE, Sengüven B, Karaduman B. The effect of smoking on epithelial proliferation in healthy and periodontally diseased marginal gingival epithelium. J Periodontol. 2008;79:1444–50.
Takeuchi H, Kubota S, Murakashi E, et al. Nicotine-induced CCN2: from smoking to periodontal fibrosis. J Dent Res. 2010;89:34–9.
Wynn TA. Cellular and molecular mechanisms of fibrosis. J Pathol. 2008;214:199–210.
Pelosi P, Rocco PR, Negrini D, Passi A. The extracellular matrix of the lung and its role in edema formation. An Acad Bras Cienc. 2007;79:285–97.
Alexakis C, Maxwell P, Bou-Gharios G. Organ-specific collagen expression: implications for renal disease. Nephron Exp Nephrol. 2006;102:71–5.
Parsons CJ, Takashima M, Rippe RA. Molecular mechanisms of hepatic fibrogenesis. J Gastroenterol Hepatol. 2007;22:79–84.
Chakraborti S, Mandal M, Das S, Mandal A, Chakraborti T. Regulation of matrix metalloproteinases: an overview. Mol Cell Biochem. 2003;253:269–85.
Visse R, Nagase H. Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry. Circ Res. 2003;92:827–39.
Border WA, Noble NA, Yamamoto T, et al. Natural inhibitor of transforming growth factor-beta protects against scarring in experimental kidney disease. Nature. 1992;360:361–4.
Kaviratne M, Hesse M, Leusink M, et al. IL-13 activates a mechanism of tissue fibrosis that is completely TGF-beta independent. J Immunol. 2004;173:4020–9.
Takeuchi H, Kubota S, Murakashi E, et al. Effect of transforming growth factor-beta 1 on expression of the connective tissue growth factor (CCN2/CTGF) gene in normal human gingival fibroblasts and periodontal ligament cells. J Periodontal Res. 2009;44:161–9.
Johnson GK, Hill M. Cigarette smoking and the periodontal patient. J Periodontol. 2004;75:196–209.
Shimao T, Goto Y, Aoki M, Asano M, Hatano S. Phase I study of nicotine-resin complex, a pharmaceutical aid for smoking cessation. 1. Single dose study in healthy volunteers. J. Clin. Therap. Med. 1990;6:1097–112.
Wang H, Li WS, Shi DJ, et al. Correlation of MMP(1) and TIMP (1) expression with pituitary adenoma fibrosis. J Neurooncol. 2008;90:151–6.
Friedman SL. Molecular regulation of hepatic fibrosis, an integrated cellular response to tissue injury. J Biol Chem. 2000;275:2247–50.
Scabbia A, Cho KS, Sigurdsson TJ, Kim CK, Trombelli L. Cigarette smoking negatively affects healing response following flap debridement surgery. J Periodontol. 2001;72:43–9.
Preber H, Bergström J. The effect of non-surgical treatment on periodontal pockets in smokers and non-smokers. J Clin Periodontol. 1986;13:319–23.
Nagase H, Woessner JF Jr. Matrix metalloproteinases. J Biol Chem. 1999;274:21491–4.
Milani S, Herbst H, Schuppan D, et al. Differential expression of matrix-metalloproteinase-1 and -2 genes in normal and fibrotic human liver. Am J Pathol. 1994;144:528–37.
Iredale JP, Benyon RC, Arthur MJ, et al. Tissue inhibitor of metalloproteinase-1 messenger RNA expression is enhanced relative to interstitial collagenase messenger RNA in experimental liver injury and fibrosis. Hepatology. 1996;24:176–84.
Zhang W, Fang M, Song F, Windsor LJ. Effects of cigarette smoke condensate and nicotine on human gingival fibroblast-mediated collagen degradation. J Periodontol. 2011;82:1071–9.
Ryu JH, Colby TV, Hartman TE, Vassallo R. Smoking-related interstitial lung diseases: a concise review. Eur Respir J. 2001;17:122–32.
Ma LJ, Yang H, Gaspert A, et al. Transforming growth factor-beta-dependent and -independent pathways of induction of tubulointerstitial fibrosis in beta6(−/−) mice. Am J Pathol. 2003;163:1261–73.
Eichel B, Shahrik HA. Tabacco smoke toxicity: loss of human oral leukocyte function and fluid-cell metabolism. Science. 1969;12:1424–8.
Kenney EB, Kraal JH, Saxe SR, Jones J. The effect of cigarette smoke on human oral polymorphonuclear leukocytes. J Periodontal Res. 1977;12:227–34.
Ryder MI, Fujitaki R, Johnson G, Hyun W. Alterations of neutrophil oxidative burst by in vitro smoke exposure: implications for oral and systemic diseases. Ann Periodontol. 1998;3:76–87.
Kalra J, Chaudhary AK, Prasad K. Increased production of oxygen free radicals in cigarette smokers. Int J Exp Pathol. 1991;72:1–7.
Söder B. Neutrophil elastase activity, levels of prostaglandin E2, and matrix metalloproteinase-8 in refractory periodontitis sites in smokers and non-smokers. Acta Odontol Scand. 1999;57:77–82.
Silacci P, Dayer JM, Desgeorges A, Peter R, Manueddu C, Guerne PA. Interleukin (IL)-6 and its soluble receptor induce TIMP-1 expression in synoviocytes and chondrocytes, and block IL-1-induced collagenolytic activity. J Biol Chem. 1998;273:13625–9.
Benyon RC, Iredale JP, Goddard S, Winwood PJ, Arthur MJ. Expression of tissue inhibitor of metalloproteinases 1 and 2 is increased in fibrotic human liver. Gastroenterology. 1996;110:821–31.
Alper B, Leyhausen G, Sapotnick A, Gunay H, Geurtsen W. Nicotine-induced alterations in human primary periodontal ligament and gingiva fibroblast cultures. Clin Oral Invest. 1998;2:40–6.
Hanes PJ, Schuster GS, Lubas S. Binding, uptake, and release of nicotine by human gingival fibroblasts. J Periodontol. 1991;62:147–52.
Raulin LA, McPherson JC 3rd, McQuade MJ, Hanson BS. The effect of nicotine on the attachment of human fibroblasts to glass and human root surfaces in vitro. J Periodontol. 1988;59:318–25.
Tipton DA, Dabbous MK. Effects of nicotine on proliferation and extracellular matrix production of human gingival fibroblasts in vitro. J Periodontol. 1995;66:1056–64.
Chen X, Wolff L, Aeppli D, Guo Z, Luan W, Baelum V, Fejeskov O. Cigarette smoking, salivary/gingival crevicular fluid cotinine and periodontal status. A 10-year longitudinal study. J Clin Periodontol. 2001;28:331–9.
Haley NJ, Axelrad CM, Tilton KA. Validation of self-reported smoking behavior: biochemical analyses of cotinine and thiocyanate. Am J Public Health. 1983;73:1204–7.