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Functional expression of α7 nicotinic acetylcholine receptors in human periodontal ligament fibroblasts and rat periodontal tissues

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Abstract

Tobacco smoking is the main risk factor associated with chronic periodontitis, but the mechanisms that underlie this relationship are largely unknown. Recent reports proposed that nicotine plays an important role in tobacco-related morbidity by acting through the nicotinic acetylcholine receptors (nAChRs) expressed by non-neuronal cells. The aim of this study was to investigate whether α7 nAChR was expressed in periodontal tissues and whether it functions by regulating IL-1β in the process of periodontitis. In vitro, human periodontal ligament (PDL) cells were cultured with 10−12 M of nicotine and/or 10−9 M of alpha-bungarotoxin (α-Btx), a α7 nAChR antagonist. The expression of α7 nAChR and IL-1β in PDL cells and the effects of nicotine/α-Btx administration on their expression were explored. In vivo, an experimental periodontitis rat model was established, and the effects of nicotine/α-Btx administration on expression of α7 nAChR and development of periodontitis were evaluated. We found that α7 nAChR was present in human PDL cells and rat periodontal tissues. The expressions of α7 nAChR and IL-1β were significantly increased by nicotine administration, whereas α-Btx treatment partially suppressed these effects. This study was the first to demonstrate the functional expression of α7 nAChR in human PDL cells and rat periodontal tissues. Our results may be pertinent to a better understanding of the relationships among smoking, nicotine, and periodontitis.

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References

  • Agarwal S, Chandra CS, Piesco NP, Langkamp HH, Bowen L, Baran C (1998) Regulation of periodontal ligament cell functions by interleukin-1beta. Infect Immun 66:932–937

    CAS  PubMed  Google Scholar 

  • Arredondo J, Nguyen VT, Chernyavsky AI, Jolkovsky DL, Pinkerton KE, Grando SA (2001) A receptor-mediated mechanism of nicotine toxicity in oral keratinocytes. Lab Invest 81:1653–1668

    CAS  PubMed  Google Scholar 

  • Arredondo J, Chernyavsky AI, Marubio LM, Beaudet AL, Jolkovsky DL, Pinkerton KE, Grando SA (2005) Receptor-mediated tobacco toxicity: regulation of gene expression through alpha3beta2 nicotinic receptor in oral epithelial cells. Am J Pathol 166:597–613

    CAS  PubMed  Google Scholar 

  • Arredondo J, Chernyavsky AI, Jolkovsky DL, Pinkerton KE, Grando SA (2007) Receptor-mediated tobacco toxicity: alterations of the NF-kappaB expression and activity downstream of alpha7 nicotinic receptor in oral keratinocytes. Life Sci 80:2191–2194

    Article  CAS  PubMed  Google Scholar 

  • Bergstrom J (2004) Tobacco smoking and chronic destructive periodontal disease. Odontology 92:1–8

    Article  CAS  PubMed  Google Scholar 

  • Chernyavsky AI, Arredondo J, Karlsson E, Wessler I, Grando SA (2005) The Ras/Raf-1/MEK1/ERK signaling pathway coupled to integrin expression mediates cholinergic regulation of keratinocyte directional migration. J Biol Chem 280:39220–39228

    Article  CAS  PubMed  Google Scholar 

  • Do LG, Slade GD, Roberts-Thomson KF, Sanders AE (2008) Smoking-attributable periodontal disease in the Australian adult population. J Clin Periodontol 35:398–404

    Article  PubMed  Google Scholar 

  • En-Nosse M, Hartmann S, Trinkaus K, Alt V, Stigler B, Heiss C, Kilian O, Schnettler R, Lips KS (2009) Expression of non-neuronal cholinergic system in osteoblast-like cells and its involvement in osteogenesis. Cell Tissue Res 338:203–215

    Article  CAS  PubMed  Google Scholar 

  • Fujii T, Takada-Takatori Y, Kawashima K (2008) Basic and clinical aspects of non-neuronal acetylcholine: expression of an independent, non-neuronal cholinergic system in lymphocytes and its clinical significance in immunotherapy. J Pharmacol Sci 106:186–192

    Article  CAS  PubMed  Google Scholar 

  • Fukushima H, Jimi E, Okamoto F, Motokawa W, Okabe K (2005) IL-1-induced receptor activator of NF-[kappa]B ligand in human periodontal ligament cells involves ERK-dependent PGE2 production. Bone 36:267–275

    Article  CAS  PubMed  Google Scholar 

  • Grando SA (2008) Basic and clinical aspects of non-neuronal acetylcholine: biological and clinical significance of non-canonical ligands of epithelial nicotinic acetylcholine receptors. J Pharmacol Sci 106:174–179

    Article  CAS  PubMed  Google Scholar 

  • Ho YC, Yang SF, Huang FM, Chang YC (2009) Up-regulation of osteolytic mediators in human osteosarcoma cells stimulated with nicotine. J Periodontal Res 44:760–766

    Article  CAS  PubMed  Google Scholar 

  • Kawashima K, Fujii T (2008) Basic and clinical aspects of non-neuronal acetylcholine: overview of non-neuronal cholinergic systems and their biological significance. J Pharmacol Sci 106:167–173

    Article  CAS  PubMed  Google Scholar 

  • Li XW, Wang H (2006) Non-neuronal nicotinic alpha 7 receptor, a new endothelial target for revascularization. Life Sci 78:1863–1870

    Article  CAS  PubMed  Google Scholar 

  • Listgarten MA (1987) Nature of periodontal diseases: pathogenic mechanisms. J Periodontal Res 22:172–178

    Article  CAS  PubMed  Google Scholar 

  • Makino A, Yamada S, Okuda K, Kato T (2008) Nicotine involved in periodontal disease through influence on cytokine levels. FEMS Immunol Med Microbiol 52:282–286

    Article  CAS  PubMed  Google Scholar 

  • Matta SG, Balfour DJ, Benowitz NL, Boyd RT, Buccafusco JJ, Caggiula AR, Craig CR, Collins AC, Damaj MI, Donny EC, Gardiner PS, Grady SR, Heberlein U, Leonard SS, Levin ED, Lukas RJ, Markou A, Marks MJ, McCallum SE, Parameswaran N, Perkins KA, Picciotto MR, Quik M, Rose JE, Rothenfluh A, Schafer WR, Stolerman IP, Tyndale RF, Wehner JM, Zirger JM (2007) Guidelines on nicotine dose selection for in vivo research. Psychopharmacology (Berl) 190:269–319

    Article  CAS  Google Scholar 

  • Nguyen VT, Hall LL, Gallacher G, Ndoye A, Jolkovsky DL, Webber RJ, Buchli R, Grando SA (2000) Choline acetyltransferase, acetylcholinesterase, and nicotinic acetylcholine receptors of human gingival and esophageal epithelia. J Dent Res 79:939–949

    Article  CAS  PubMed  Google Scholar 

  • Nogueira-Filho Gda R, Rosa BT, Cesar-Neto JB, Tunes RS, Tunes Uda R (2007) Low- and high-yield cigarette smoke inhalation potentiates bone loss during ligature-induced periodontitis. J Periodontol 78:730–735

    Article  PubMed  Google Scholar 

  • Ojima M, Hanioka T, Tanaka K, Inoshita E, Aoyama H (2006) Relationship between smoking status and periodontal conditions: findings from national databases in Japan. J Periodontal Res 41:573–579

    Article  CAS  PubMed  Google Scholar 

  • Rivera-Hidalgo F (2003) Smoking and periodontal disease. Periodontol 2000(32):50–58

    Article  Google Scholar 

  • Rosa GM, Lucas GQ, Lucas ON (2008) Cigarette smoking and alveolar bone in young adults: a study using digitized radiographs. J Periodontol 79:232–244

    Article  PubMed  Google Scholar 

  • Sallette J, Pons S, Devillers-Thiery A, Soudant M, Prado de Carvalho L, Changeux J-P, Corringer PJ (2005) Nicotine upregulates its own receptors through enhanced intracellular maturation. Neuron 46:595–607

    Article  CAS  PubMed  Google Scholar 

  • Torrungruang K, Nisapakultorn K, Sutdhibhisal S, Tamsailom S, Rojanasomsith K, Vanichjakvong O, Prapakamol S, Premsirinirund T, Pusiri T, Jaratkulangkoon O, Kusump S, Rajatanavin R (2005) The effect of cigarette smoking on the severity of periodontal disease among older Thai adults. J Periodontol 76:566–572

    Article  PubMed  Google Scholar 

  • Watts TL (2006) Smoking, Helicobacter pylori, and periodontitis. BMJ 332:1513

    Article  PubMed  Google Scholar 

  • Yamamoto Y, Nishida N, Tanaka M, Hayashi N, Matsuse R, Nakayama K, Morimoto K, Shizukuishi S (2005) Association between passive and active smoking evaluated by salivary cotinine and periodontitis. J Clin Periodontol 32:1041–1046

    Article  CAS  PubMed  Google Scholar 

  • Ylostalo P, Sakki T, Laitinen J, Jarvelin MR, Knuuttila M (2004) The relation of tobacco smoking to tooth loss among young adults. Eur J Oral Sci 112:121–126

    Article  PubMed  Google Scholar 

  • Yoshida M, Masunaga K, Satoji Y, Maeda Y, Nagata T, Inadome A (2008) Basic and clinical aspects of non-neuronal acetylcholine: expression of non-neuronal acetylcholine in urothelium and its clinical significance. J Pharmacol Sci 106:193–198

    Article  CAS  PubMed  Google Scholar 

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Correspondence to Xiao-Jing Wang.

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Xiao-Jing Wang and Ying-Feng Liu contributed equally to this work.

This investigation was supported in part by research grants from the Japan Sasakawa Fellowship and the National Natural Science Foundation of China (NSFC grants 30572045 and 30973315).

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Wang, XJ., Liu, YF., Wang, QY. et al. Functional expression of α7 nicotinic acetylcholine receptors in human periodontal ligament fibroblasts and rat periodontal tissues. Cell Tissue Res 340, 347–355 (2010). https://doi.org/10.1007/s00441-010-0949-9

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  • DOI: https://doi.org/10.1007/s00441-010-0949-9

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