ROLE OF NITRIC OXIDE IN INFLAMMATORY PERIODONTAL DISEASES: A REVIEW

Year 2014, 2014: Supplement 9, 74 - 84, 11.02.2015

Cenk Çanakçı Gülnihal Doğan

https://doi.org/10.17567/dfd.10482

Abstract

Nitric oxide (NO) is a unique molecule for biological organisms, and has also very important effects on various pathologic and physiologic mechanisms. Many cell types can generate NO during different pathological and physiologic conditions. Recently, many authors have been reported the connections between NO and inflammatory diseases. Periodontal pathologies are characterized with specific periodontal inflammation and host tissues damage around the teeth, and additional factors such as force application on teeth. However, the production of NO and the role of NO in the development of periodontal pathologies are unclear. On the other hand, many evidences from previous studies indicates a close relationship between NO and periodontal pathologies. In this review, we want to discuss; overproduction of NO during inflammation and mechanical stress of force application on teeth, which directly cause progression of periodontal pathologies, and the possible effects of NO overproduction in periodontal diseases

Keywords

Nitric pathologies, inflammation, force application on tooth

NİTRİK OKSİDİN İNFLAMATUAR PERIODONTAL HASTALIKLARDA ROLÜ : DERLEME

Abstract

Nitric oxide (NO) is a unique molecule for biological organisms, and has also very important effects on various pathologic and physiologic mechanisms. Many cell types can generate NO during different pathological and physiologic conditions. Recently, many authors have been reported the connections between NO and inflammatory diseases. Periodontal pathologies are characterized with specific periodontal inflammation and host tissues damage around the teeth, and additional factors such as force application on teeth. However, the production of NO and the role of NO in the development of periodontal pathologies are unclear. On the other hand, many evidences from previous studies indicates a close relationship between NO and periodontal pathologies. In this review, we want to discuss; overproduction of NO during inflammation and mechanical stress of force application on teeth, which directly cause progression of periodontal pathologies, and the possible effects of NO overproduction in periodontal diseases.

Keywords

Nitrik oksit, periodontal patolojiler, inflamasyon, dişler üzerine kuvvet uygulaması

References

• Ignarro LJ, Buga GM, Wood KS, Byrns RE, Chaudhuri G. Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc Natl Acad Sci U S A 1987; 84: 9265-9.
• Bredt DS, Snyder SH. Nitric oxide mediates glutamate-linked enhancement of cGMP levels in the cerebellum. Proc Natl Acad Sci U S A 1989; 86: 9030-3.
• Stoclet JC, Muller B, Andriantsitohaina R, Kleschyov A. Overproduction
• pathophysiology of blood vessels. Biochemistry of
• (Mosc) 1998; 63: 826-32. nitric oxide
• Hibbs JB, Jr., Taintor RR, Vavrin Z, Rachlin EM. Nitric oxide: a cytotoxic activated macrophage effector molecule. Biochem Biophys Res Commun 1988; 157: 87-94.
• Wright CD, Mulsch A, Busse R, Osswald H. Generation of nitric oxide by human neutrophils. Biochem Biophys Res Commun 1989; 160: 813-9.
• Wang R, Ghahary A, Shen YJ, Scott PG, Tredget EE. Human dermal fibroblasts produce nitric oxide and express both constitutive and inducible nitric oxide synthase isoforms. J Invest Dermatol 1996; 106: 419-27.
• Curran RD, Billiar TR, Stuehr DJ, Hofmann K, Simmons RL. Hepatocytes produce nitrogen oxides from L-arginine in response to inflammatory products of Kupffer cells. J Exp Med 1989; 170:
• Stadler J, Stefanovic-Racic M, Billiar TR, Curran RD, McIntyre LA, Georgescu HI, Simmons RL, Evans CH. Articular chondrocytes synthesize nitric oxide in response to cytokines and lipopolysaccharide. J Immunol 1991; 147: 3915-20.
• Grabowski PS, Wright PK, Van 't Hof RJ, Helfrich MH, Ohshima H, Ralston SH. Immunolocalization of inducible nitric oxide synthase in synovium and cartilage in rheumatoid arthritis and osteoarthritis. Br J Rheumatol 1997; 36: 651-5.
• Moncada S, Palmer RM, Higgs EA. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol Rev 1991; 43: 109-42.
• Mayer B, Hemmens B. Biosynthesis and action of nitric oxide in mammalian cells. Trends Biochem Sci 1997; 22: 477-81.
• Butler AR, Flitney FW, Williams DL. NO, nitrosonium ions, nitroxide ions, nitrosothiols and iron-nitrosyls in biology: a chemist's perspective. Trends Pharmacol Sci 1995; 16: 18-22.
• Knowles RG, Moncada S. Nitric oxide synthases in mammals. Biochem J 1994; 298 ( Pt 2): 249-58.
• Vallance P. Nitric oxide: therapeutic opportunities. Fundam Clin Pharmacol 2003; 17: 1-10.
• Kendall HK, Marshall RI, Bartold PM. Nitric oxide and tissue destruction. Oral Dis 2001; 7: 2-10.
• Özcan E, Özdemir A, Çanakçı CF. The Role Of Reactive Oxygen Species In Periodontal Tissue Destruction. J Dent Fac Atatürk Uni 2011; 21: 255-61.
• Batista AC, Silva TA, Chun JH, Lara VS. Nitric oxide synthesis and severity of human periodontal disease. Oral Dis 2002; 8: 254-60.
• Kroncke KD, Fehsel K, Kolb-Bachofen V. Nitric oxide: cytotoxicity versus cytoprotection--how, why, when, and where? Nitric Oxide 1997; 1: 107- 20.
• Brunet LR. Nitric oxide in parasitic infections. Int Immunopharmacol 2001; 1: 1457-67.
• Laurent M, Lepoivre M, Tenu JP. Kinetic modelling of the nitric oxide gradient generated in vitro by adherent cells expressing inducible nitric oxide synthase. Biochem J 1996; 314 ( Pt 1): 109-13.
• Lohinai Z, Szabo, C. Role of nitric oxide in physiology and patophysiology of periodontal tissues. Med Sci Monit 1998; 4: 1089-95.
• Ralston SH, Ho LP, Helfrich MH, Grabowski PS, Johnston PW, Benjamin N. Nitric oxide: a cytokine- induced regulator of bone resorption. J Bone Miner Res 1995; 10: 1040-9.
• Ralston SH. The Michael Mason Prize Essay 1997. Nitric oxide and bone: what a gas Br J Rheumatol 1997; 36: 831-8.
• Evans DM, Ralston SH. Nitric oxide and bone. J Bone Miner Res 1996; 11: 300-5.
• Chae HJ, Park RK, Chung HT, Kang JS, Kim MS, Choi DY, Bang BG, Kim HR. Nitric oxide is a regulator of bone remodelling. J Pharm Pharmacol 1997; 49: 897-902.
• Ohashi M, Iwase M, Nagumo M. Elevated production of salivary nitric oxide in oral mucosal diseases. J Oral Pathol Med 1999; 28: 355-9.
• Kinane DF, Podmore M, Murray MC, Hodge PJ, Ebersole J. Etiopathogenesis of periodontitis in children and adolescents. Periodontol 2000 2001; 26: 54-91.
• Lappin DF, Kjeldsen M, Sander L, Kinane DF. Inducible nitric oxide synthase expression in periodontitis. J Periodontal Res 2000; 35: 369-73.
• Kendall HK, Haase HR, Li H, Xiao Y, Bartold PM. Nitric oxide synthase type-II is synthesized by human gingival tissue and cultured human gingival fibroblasts. J Periodontal Res 2000; 35: 194-200.
• Lohinai Z, Benedek P, Feher E, Gyorfi A, Rosivall L, Fazekas A, Salzman AL, Szabo C. Protective effects of mercaptoethylguanidine, a selective inhibitor of inducible nitric oxide synthase, in ligature-induced periodontitis in the rat. Br J Pharmacol 1998; 123: 353-60.
• Arany I, Brysk MM, Brysk H, Tyring SK. Regulation of inducible nitric oxide synthase mRNA levels by differentiation keratinocytes. Biochem Biophys Res Commun 1996; 220: 618-22. cytokines in human
• Sirsjo A, Karlsson M, Gidlof A, Rollman O, Torma H. Increased expression of inducible nitric oxide synthase in psoriatic skin and cytokine-stimulated cultured keratinocytes. Br J Dermatol 1996; 134: 643-8.
• Robbins RA, Springall DR, Warren JB, Kwon OJ, Buttery LD, Wilson AJ, Adcock IM, Riveros-Moreno V, Moncada S, Polak J, et al. Inducible nitric oxide synthase is increased in murine lung epithelial cells by cytokine stimulation. Biochem Biophys Res Commun 1994; 198: 835-43.
• Gross SS, Jaffe EA, Levi R, Kilbourn RG. Cytokine- activated endothelial cells express an isotype of nitric oxide synthase which is tetrahydrobiopterin- dependent, calmodulin-independent and inhibited by arginine analogs with a rank-order of potency characteristic of activated macrophages. Biochem Biophys Res Commun 1991; 178: 823-9.
• Blix IJ, Helgeland K. LPS from Actinobacillus actinomycetemcomitans and production of nitric oxide in murine macrophages J774. Eur J Oral Sci 1998; 106: 576-81.
• Chakravortty D, Kumar KS. Induction of cell proliferation and collagen synthesis in human small intestinal lipopolysaccharide: possible involvement of nitric oxide. Biochem Biophys Res Commun 1997; 240: 458-63. fibroblasts by
• Krischel V, Bruch-Gerharz D, Suschek C, Kroncke KD, Ruzicka T, Kolb-Bachofen V. Biphasic effect of exogenous nitric oxide on proliferation and differentiation in skin derived keratinocytes but not fibroblasts. J Invest Dermatol 1998; 111: 286-91.
• Andrew PJ, Harant H, Lindley IJ. Up-regulation of interleukin-1beta-stimulated interleukin-8 in human keratinocytes by nitric oxide. Biochem Pharmacol 1999; 57: 1423-9.
• Akopov SE, Kankanian AP. [Nitric oxide (NO) inactivation by polymorphonuclear leukocytes as a mechanism for the development of periodontal lesions]. Stomatologiia (Mosk) 1996; 75: 12-4.
• Aurer A, Aleksic J, Ivic-Kardum M, Aurer J, Culo F. Nitric oxide synthesis is decreased in periodontitis. J Clin Periodontol 2001; 28: 565-8.
• Oppenheim A. Tissue changes particularly of the bone. 1911; 30: 227-328.
• Hughes B, King GJ. Effect of orthodontic appliance reactivation during the period of peak expansion in the osteoclast population. Anat Rec 1998; 251: 80- 6.
• Schroeder EH. In Handbook of Microscopic Anatomy. Springer-Verlag, Berlin 1986; 5: 1-409.
• Mabuchi R, Matsuzaka K, Shimono M. Cell proliferation and cell death in periodontal ligaments during orthodontic tooth movement. J Periodontal Res 2002; 37: 118-24.
• Brogan JM, Kang KJ, Koyama E, Tuncay OC. Localization of nitric oxide synthase in the periodontal tissues of orthodontically moved and stationary teeth. Prog Orthod 2002; 3: 12-6.
• Warita H, Watarai H, Soma K. Nitric oxide synthase expression is increased by occlusal force in rat periodontal ligament. Orthod Craniofac Res 2004; 7: 122-6.
• Fermin A, Carranza, J.R., Saglie, F.R. The gingiva in. 11 ed. St. Louis, Missouri; 2011.
• Greenwald RA, Kirkwood K. Adult periodontitis as a model for rheumatoid arthritis (with emphasis on treatment strategies). J Rheumatol 1999; 26: 1650-3.
• Kawamoto S, Nagaoka E. The effect of oestrogen deficiency on the alveolar bone resorption caused by traumatic occlusion. J Oral Rehabil 2000; 27: 587-94.
• Lowenstein CJ, Snyder SH. Nitric oxide, a novel biologic messenger. Cell 1992; 70: 705-7.
• Wink DA, Mitchell JB. Chemical biology of nitric oxide: Insights into regulatory, cytotoxic, and cytoprotective mechanisms of nitric oxide. Free Radic Biol Med 1998; 25: 434-56.
• Stamler JS. Redox signaling: nitrosylation and related target interactions of nitric oxide. Cell 1994; 78: 931-6.
• Ignarro LJ. Physiology and pathophysiology of nitric oxide. Kidney Int Suppl 1996; 55: S2-5.
• Brown GC. Nitric oxide regulates mitochondrial respiration and cell functions by inhibiting cytochrome oxidase. FEBS Lett 1995; 369: 136-9.
• Stamler JS, Lamas S, Fang FC. Nitrosylation. the prototypic redox-based signaling mechanism. Cell 2001; 106: 675-83.
• Feelisch M. The biochemical pathways of nitric oxide formation from nitrovasodilators: appropriate choice of exogenous NO donors and aspects of preparation and handling of aqeous NO solutions. J Cardiovasc Pharmacol 1991; 17 (suppl 3): 25-33.
• Doyle MP, Hoekstra JW. Oxidation of nitrogen oxides by bound dioxygen in hemoproteins. J Inorg Biochem 1981; 14: 351-8.
• Russwurm M, Koesling D. Isoforms of NO-sensitive guanylyl cyclase. Mol Cell Biochem 2002; 230:
• Lepoivre M, Chenais B, Yapo A, Lemaire G, Thelander L, Tenu JP. Alterations of ribonucleotide reductase activity following induction of the nitrite- generating pathway in adenocarcinoma cells. J Biol Chem 1990; 265: 14143-9.
• Lepoivre M, Flaman JM, Henry Y. Early loss of the tyrosyl radical in ribonucleotide reductase of adenocarcinoma cells producing nitric oxide. J Biol Chem 1992; 267: 22994-3000.
• Coleman JW. Nitric oxide in immunity and inflammation. Int Immunopharmacol 2001; 1: 1397-406.
• Beckman JS, Carson M, Smith CD, Koppenol WH. ALS, SOD and peroxynitrite. Nature 1993; 364: 584.
• Pryor WA, Squadrito GL. The chemistry of peroxynitrite: a product from the reaction of nitric oxide with superoxide. Am J Physiol 1995; 268: L699-722.
• Fukuto JM, Ignarro LJ. In vivo aspects of nitric oxide (NO) chemistry- Does peroxynitrite (-OONO) play a major role in cytotoxicity. Accounts of chemical research 1997; 30: 149-52.
• Brito C, Naviliat M, Tiscornia AC, Vuillier F, Gualco G, Dighiero G, Radi R, Cayota AM. Peroxynitrite inhibits T lymphocyte activation and proliferation by phosphorylation and peroxynitrite-driven apoptotic death. J Immunol 1999; 162: 3356-66. tyrosine
• Crow JP, Beckman JS. The role of peroxynitrite in nitric oxide-mediated toxicity. Curr Top Microbiol Immunol 1995; 196: 57-73.
• Beckman JS, Koppenol WH. Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly. Am J Physiol 1996; 271: C1424-37.
• Vallance P, Charles I. Nitric oxide as an antimicrobial agent: does NO always mean NO? [ comment]. Gut 1998; 42: 313-4.
• Gyurko R, Boustany G, Huang PL, Kantarci A, Van Dyke TE, Genco CA, Gibson FC, 3rd. Mice lacking inducible nitric oxide synthase demonstrate impaired killing of Porphyromonas gingivalis. Infect Immun 2003; 71: 4917-24.
• Kato C, Mikami M, Suzuki A, Saito K. The reduction of Fusobacterium nucleatum in mice is irrelevant to the nitric oxide induced by iNOS. Microbiol Immunol 2003; 47: 27-35.
• Lomniczi A, Suburo AM, Elverdin JC, Mastronardi CA, Diaz S, Rettori V, McCann SM. Role of nitric oxide in salivary secretion. Neuroimmunomo- dulation 1998; 5: 226-33.
• Allaker RP, Silva Mendez LS, Hardie JM, Benjamin N. Antimicrobial effect of acidified nitrite on periodontal bacteria. Oral Microbiol Immunol 2001; 16: 253-6.
• Smith J, Benjamin N, Weetman DA., Mackenzei D, MacFarlane TW. The Microbial Generation of Nitric Oxide in the Human Oral Cavity. Microbial Ecology in Health and Disease 1999; 11: 23-7.
• Ozmeric N, Elgun S, Uraz A. Salivary arginase in patients with adult periodontitis. Clin Oral Investig 2000; 4: 21-4.
• Liew FY. Nitric oxide in infectious and autoimmune diseases. Ciba Found Symp 1995; 195: 234-9; discussion 239-44.
• Lohinai Z, Stachlewitz R, Szekely AD, Feher E, Dezsi L, Szabo C. Evidence for the expression of cyclooxygenase-2 enzyme in periodontitis. Life Sci 2001; 70: 279-90.
• Shimizu N, Ozawa Y, Yamaguchi M, Goseki T, Ohzeki K, Abiko Y. Induction of COX-2 expression by mechanical tension force in human periodontal ligament cells. J Periodontol 1998; 69: 670-7.
• Jeng JH, Ho YS, Chan CP, Wang YJ, Hahn LJ, Lei D, Hsu CC, Chang MC. Areca nut extract up- regulates cyclooxygenase-2 mRNA and protein expression of human oral keratinocytes. Carcinogenesis 2000; 21: 1365-70. production,
• Salvemini D, Misko TP, Masferrer JL, Seibert K, Currie MG, Needleman P. Nitric oxide activates cyclooxygenase enzymes. Proc Natl Acad Sci U S A 1993; 90: 7240-4.
• Landino LM, Crews BC, Timmons MD, Morrow JD, Marnett LJ. Peroxynitrite, the coupling product of nitric oxide and superoxide, activates prostaglandin biosynthesis. Proc Natl Acad Sci U S A 1996; 93: 15069-74.
• Salvemini D. Regulation of cyclooxygenase enzymes by nitric oxide. Cell Mol Life Sci 1997; 53: 576-82.
• Nagayama M, Niwa K, Nagayama T, Ross ME, Iadecola C. The cyclooxygenase-2 inhibitor NS-398 ameliorates ischemic brain injury in wild-type mice but not in mice with deletion of the inducible nitric oxide synthase gene. J Cereb Blood Flow Metab 1999; 19: 1213-9.
• Canakci CF, Cicek Y, Canakci V. Reactive oxygen species and human inflammatory periodontal diseases. Biochemistry (Mosc) 2005; 70: 619-28.
• Okamoto T, Akaike T, Nagano T, Miyajima S, Suga M, Ando M, Ichimori K, Maeda H. Activation of human neutrophil procollagenase by nitrogen dioxide and peroxynitrite: a novel mechanism for procollagenase activation involving nitric oxide. Arch Biochem Biophys 1997; 342: 261-74.
• Taskiran D, Stefanovic-Racic M, Georgescu H, Evans C. Nitric oxide mediates suppression of cartilage proteoglycan synthesis by interleukin-1. Biochem Biophys Res Commun 1994; 200: 142-8.
• Murrell GA, Jang D, Williams RJ. Nitric oxide activates metalloprotease enzymes in articular cartilage. Biochem Biophys Res Commun 1995; 206: 15-21.
• Ralston SH, Todd D, Helfrich M, Benjamin N, Grabowski PS. Human osteoblast-like cells produce nitric oxide and express inducible nitric oxide synthase. Endocrinology 1994; 135: 330-6.
• Brandi ML, Hukkanen M, Umeda T, Moradi- Bidhendi N, Bianchi S, Gross SS, Polak JM, MacIntyre I. Bidirectional regulation of osteoclast function by nitric oxide synthase isoforms. Proc Natl Acad Sci U S A 1995; 92: 2954-8.
• Hukkanen M, Hughes FJ, Buttery LD, Gross SS, Evans TJ, Seddon S, Riveros-Moreno V, Macintyre I, Polak JM. Cytokine-stimulated expression of inducible nitric oxide synthase by mouse, rat, and human osteoblast-like cells and its functional role in osteoblast metabolic activity. Endocrinology 1995; 136: 5445-53.
• Damoulis PD, Hauschka PV. Nitric oxide acts in conjunction with proinflammatory cytokines to promote cell death in osteoblasts. J Bone Miner Res 1997; 12: 412-22.
• Mancini L, Moradi-Bidhendi N, Becherini L, Martineti V, MacIntyre I. The biphasic effects of nitric oxide in primary rat osteoblasts are cGMP dependent. Biochem Biophys Res Commun 2000; 274: 477-81.
• Kim PK, Zamora R, Petrosko P, Billiar TR. The regulatory role of nitric oxide in apoptosis. Int Immunopharmacol 2001; 1: 1421-41.
• Jarnbring F, Somogyi E, Dalton J, Gustafsson A, Klinge B. Quantitative assessment of apoptotic and proliferative gingival keratinocytes in oral and sulcular epithelium in patients with gingivitis and periodontitis. J Clin Periodontol 2002; 29: 1065-71.
• Suzuki T, Kumamoto H, Ooya K, Motegi K. Expression of inducible nitric oxide synthase and heat shock proteins in periapical inflammatory lesions. J Oral Pathol Med 2002; 31: 488-93.