Nicotinic acetylcholine receptor activation mediates nicotine-induced enhancement of experimental periodontitis

Journal of Periodontal Research

Volumn 44, Issue 3, 2009, Pages 297-304

  Breivik, T ^a,b,c   Gundersen, Y ^c   Gjermo, P ^b   Von Horsten S ^d   Opstad, P K ^c  

^a University of Oslo ^*  (Norway)

^b UNIVERSITY OF OSLO   (Norway)

^c NORWEGIAN DEFENCE RESEARCH ESTABLISHMENT FFI   (Norway)

^d UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

Acetylcholine receptor; Cytokine; Lipopolysaccharide; Nicotine; Periodontal disease; Rat

Indexed keywords

CORTICOSTERONE; INTERLEUKIN 10; LIPOPOLYSACCHARIDE; MECAMYLAMINE; NICOTINE; NICOTINIC RECEPTOR; NICOTINIC RECEPTOR BLOCKING AGENT; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL; ARTICLE; BLOOD; CHEMICALLY INDUCED DISORDER; DISEASE PREDISPOSITION; DRUG ANTAGONISM; DRUG EFFECT; FISCHER 344 RAT; IMMUNITY; IMMUNOLOGY; MALE; METABOLISM; OSTEOLYSIS; PERIODONTAL DISEASE; PERIODONTITIS; RAT;

ALVEOLAR BONE LOSS; ANIMALS; CORTICOSTERONE; DISEASE SUSCEPTIBILITY; IMMUNITY; INTERLEUKIN-10; LIPOPOLYSACCHARIDES; MALE; MECAMYLAMINE; NICOTINE; NICOTINIC ANTAGONISTS; PERIODONTAL ATTACHMENT LOSS; PERIODONTITIS; RATS; RATS, INBRED F344; RECEPTORS, NICOTINIC; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR-ALPHA;

EID: 65349141209     PISSN: 00223484     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1600-0765.2009.01223.x     Document Type: Article

References (46)

1. Bergstrom J, Preber H. Tobacco use as a risk factor. J Periodontol 1994 5 : 545 550.
2. Martinez-Canut P, Lorca A, Magan R. Smoking and periodontal disease severity. J Clin Periodontol 1996 22 : 743 749.
3. Johnson K, Hill M. Cigarette smoking and the periodontal patient. J Periodontol 2004 75 : 196 209. (Pubitemid 38372262)
4. Scott DA, Palmer RM, Stapleton JA. Validation of smoking status in clinical research into inflammatory periodontal disease. J Clin Periodontol 2001 28 : 715 722. (Pubitemid 33761311)
5. Meisel P, Schwahn JD, Gesch D, Bernhardt O, John U, Kocher T. Dose-effect relation of smoking and the interleukin-1 gene polymorphism in periodontal disease. J Periodontol 2004 2 : 236 242. (Pubitemid 38372266)
6. Socransky SS, Haffajee AD. Dental biofilms: difficult therapeutic targets. Periodontol 2000 2002 28 : 12 55.
7. Haffajee AD, Socransky SS. Relationship of cigarette smoking to the subgingival microbiota. J Clin Periodontol 2001 28 : 377 388. (Pubitemid 33755454)
8. Ding Y, Haapasalo M, Kerosuo E, Lounatmaa K, Kotiranta A, Sorsa T. Release and activation of human neutrophil matrix metallo- and serine proteinases during phagocytosis of Fusobacterium nucleatum, Porphyromonas gingivalis and Treponema denticola. J Clin Periodontol 1997 24 : 237 248. (Pubitemid 127731520)
9. Lohinai Z, Benedek P, Fehér E et al. Protective effects of mercaptoethylguanidine, a selective inhibitor of inducible nitric oxide synthase, in ligature-induced periodontitis in the rat. Br J Pharmacol 1998 123 : 353 360. (Pubitemid 28059703)
10. Breivik T, Rook GA. Oral treatment with SR299 (killed Mycobacterium vaccae) inhibits experimental periodontal disease in Wistar rats. J Clin Periodontol 2003 30 : 931 936. (Pubitemid 38030399)
11. Ader R, Cohen N, Felten D. Psychoneuroimmunology: interactions between the nervous system and the immune system. Lancet 1995 345 : 99 103.
12. Breivik T, Thrane PS, Murison R, Gjermo P. Emotional stress effects on immunity, gingivitis and periodontitis. Eur J Oral Sci 1996 104 : 327 334. (Pubitemid 126782179)
13. Eskandari F, Sternberg EM. Neural immune interaction in health and disease. Ann N Y Acad Sci 2002 966 : 20 27. (Pubitemid 34729157)
14. Breivik T, Opstad PK, Gjermo P, Thrane PS. Effects of hypothalamic-pituitary-adrenal axis reactivity on periodontal tissue destruction in rats. Eur J Oral Sci 2000 108 : 115 122.
15. Breivik T, Thrane PS, Gjermo P, Opstad PK. Glucocorticoid receptor antagonist RU-486 treatment reduces periodontitis in Fischer 344 rats. J Periodont Res 2000 35 : 285 290.
16. Breivik T, Thrane PS, Gjermo P, Opstad PK, Pabst R, von Horsten S. Hypothalamic-pituitary-adrenal axis activation by experimental periodontal disease in rats. J Periodont Res 2001a 36 : 295 300. (Pubitemid 33641094)
17. Breivik T, Gundersen Y, Opstad PK, Fonnum F. Chemical sympathectomy inhibits periodontal disease in Fischer 344 rats. J Periodont Res 2005 40 : 325 330. (Pubitemid 40977307)
18. Breivik T, Thrane PS. Psychoneuroimmune interactions in periodontal disease. In : Ader R, Felten DL, Cohen N, eds. Psychoneuroimmunlogy, 3rd edition. San Diego, CA : Academic Press, 2001 : Chapter 63, 627 644.
19. Breivik T, Gundersen Y, Myhrer T et al. Enhanced susceptibility to periodontitis in an animal model of depression: reversed by chronic treatment with the antidepressant tianeptine. J Clin Periodontol 2006 33 : 469 477.
20. Trent MS, Stead CM, Tran AX, Hankins JV. Diversity of endotoxin and its impact on pathogenesis. J Endotoxin Res 2006 12 : 205 223.
21. Hollis JH, Evans AK, Bruce KPE, Lightman SL, Lowry CH. Lipopolysaccharide has indomethacin-sensitive actions on Fos expression in topographically organized subpopulations of serotonergic neurons. Brain Behav Immun 2006 20 : 569 577. (Pubitemid 44540334)
22. Pavlov VA, Tracey KJ. The cholinergic anti-inflammatory pathway. Brain Behav Immun 2005 19 : 493 499. (Pubitemid 41407697)
23. Tracey KJ. Physiology and immunology of the cholinergic anti-inflammatory pathway. J Clin Invest 2007 117 : 289 296. (Pubitemid 46203953)
24. Wang H, Liao H, Ochani M et al. Cholinergic agonists inhibit HMGB1 release and improve survival in experimental sepsis. Nat Med 2004 10 : 1216 1221. (Pubitemid 39540438)
25. Saeed RW, Varm S, Peng-Nemeroff T et al. Cholinergic stimulation blocks endothelial cell activation and leukocyte recruitment during inflammation. J Exp Med 2005 201 : 1113 1123. (Pubitemid 40524679)
26. Hamano R, Takahashi HK, Iwagaki H, Yoshino T, Nishibori M, Tanaka N. Stimulation of alpha7 nicotinic acetylcholine receptor inhibits CD14 and the toll-like receptor 4 expression in human monocytes. Shock 2006 26 : 358 364. (Pubitemid 44402020)
27. Yoshikawa H, Kurokawa M, Ozaki N et al. Nicotine inhibits the production of proinflammatory mediators in human monocytes by suppression of I-kappaB phosphorylation and nuclear factor-kappaB transcriptional activity through nicotinic acetylcholine receptor alfa7. Clin Exp Immunol 2006 146 : 116 123. (Pubitemid 44393846)
28. Chi Z-L, Hayasaka S, Zhang X-Y, Cui H-S, Hayasaka Y. Acholinergic agonist attenuates endotoxin-induced uveitis in rats. Invest Ophthalmol Vis Sci 2007 48 : 2719 2725.
29. Suemaru K, Yasuda K, Umeda K et al. Nicotine blocks apomorphine-induced disruption of prepulse inhabitation of the acoustic startle in rats: possible involvement of central nicotinic α7 receptors. Brit J Pharmacol 2004 142 : 843 850. (Pubitemid 38998098)
30. ®): an old antihypertentensive with new research directions. J Hum Hypertens 2002 16 : 453 457.
31. Nociti FH Jr., Nogueira-Filho GR, Tramontina VA et al. Histometric evaluation of the effect of nicotine administration on periodontal breakdown: an in vivo study. J Periodont Res 2001 36 : 361 366. (Pubitemid 33633332)
32. Borovikova LJ, Ivanova S, Zhang M et al. Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature 2000 405 : 458 462. (Pubitemid 30367422)
33. Yoshikawa H, Kurokawa M, Ozaki N et al. Nicotine inhibits the production of proinflammatory mediators in human monocytes by suppression of I-kappaB phosphorylation and nuclear factor-kappaB transcriptional activity through nicotinic acetylcholine receptor alpha7. Clin Exp Immunol 2006 146 : 116 123. (Pubitemid 44393846)
34. Breivik T, Gundersen Y, Osmundsen H, Opstad PK, Fonnum F. Chronic treatment with the glutamate receptor antagonist MK-801 alters periodontal disease susceptibility. J Periodont Res 2005 40 : 28 35. (Pubitemid 40186623)
35. Breivik T, Gundersen Y, Osmundsen H, Fonnum F, Opstad PK. Neonatal dexamathasone and chronic tianeptine treatment inhibit ligature-induced periodontitis in adult rats. J Periodont Res 2006 41 : 23 32.
36. Breivik T, Gundersen Y, Myhrer T et al. Enhanced susceptibility to periodontitis in an animal model of depression: reversed by chronic treatment with the anti-depressant tianeptine. J Clin Periodontol 2006 33 : 469 477.
37. Bowie A, O'Neill LA. The interleukin-1 receptor/toll-lie receptor family: signal generators for pro-inflammatory interleukins and microbial products. J Leukoc Biol 2000 4 : 508 514.
38. Rook AW, Brunet LR. Microbes, immunoregulation and the gut. Gut 2006 54 : 317 320. (Pubitemid 40299080)
39. Pavlov VA, Tracey KJ. Neural regulators of innate immune responses and inflammation. Cell Mol Life Sci 2004 61 : 2322 2331. (Pubitemid 39382024)
40. Elenkov IJ, Chrousos GP. Stress hormones, Th1/Th2 patterns, pro/anti-inflammatory cytokines and susceptibility to disease. Trends Endocrinol Metab 1999 10 : 359 368. (Pubitemid 29496010)
41. Eskandari F, Sternberg EM. Neural immune interaction in health and disease. Ann N Y Acad Sci 2002 966 : 20 27. (Pubitemid 34729157)
42. Korrow NA. Activation of the hypothalamic-pituitary-adrenal axis and the autonomic nervous system during inflammation and altered programming of the neuroendocrine-immune axis during fetal and neonatal development: Lessons learned from the model inflammagen, lipopolysaccharide. Brain Behav Immun 2006 20 : 144 158. (Pubitemid 43202080)
43. Czura CJ, Tracey KJ. Autonomic neural regulation of immunity. J Intern Med 2005 247 : 156 166. (Pubitemid 40193965)
44. Cam GR, Basset JR, Cairncross JR. The action of nicotine on the pituitary-adrenal-cortical axis. Arch Int Pharmacodyn Ther 1979 237 : 49 66.
45. Cam GR, Basset JR. Effects of prolonged exposure to nicotine and stress on the pituitary-adrenocortical response: the possibility of cross-adaptation. Pharmacol Biochem Behav 1984 20 : 221 226. (Pubitemid 14167968)
46. Singh SP, Kalra R, Puttfarcken P, Kozak A, Tesfaigzi J, Sopori ML. Acute and chronic nicotine exposures modulate the immune system through different pathways. Toxicol Appl Pharmacol 2000 164 : 65 72. (Pubitemid 30198545)