Skip to main content
NCBI home page
Clinical Molecular Pathology logoLink to Clinical Molecular Pathology
. 1996 Oct;49(5):M247–M255. doi: 10.1136/mp.49.5.m247

Role of free radicals and antioxidants in the pathogenesis of the inflammatory periodontal diseases

Iain L C Chapple 1
PMCID: PMC408069  PMID: 16696085

Full text

PDF
M247

Images in this article

M248Image
on p.M248

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Amano S., Hanazawa S., Hirose K., Ohmori Y., Kitano S. Stimulatory effect on bone resorption of interleukin-1-like cytokine produced by an osteoblast-rich population of mouse calvarial cells. Calcif Tissue Int. 1988 Aug;43(2):88–91. doi: 10.1007/BF02555152. [DOI] [PubMed] [Google Scholar]
  2. Ames B. N., Cathcart R., Schwiers E., Hochstein P. Uric acid provides an antioxidant defense in humans against oxidant- and radical-caused aging and cancer: a hypothesis. Proc Natl Acad Sci U S A. 1981 Nov;78(11):6858–6862. doi: 10.1073/pnas.78.11.6858. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Aruoma O. I., Halliwell B., Dizdaroglu M. Iron ion-dependent modification of bases in DNA by the superoxide radical-generating system hypoxanthine/xanthine oxidase. J Biol Chem. 1989 Aug 5;264(22):13024–13028. [PubMed] [Google Scholar]
  4. Aruoma O. I., Halliwell B., Dizdaroglu M. Iron ion-dependent modification of bases in DNA by the superoxide radical-generating system hypoxanthine/xanthine oxidase. J Biol Chem. 1989 Aug 5;264(22):13024–13028. [PubMed] [Google Scholar]
  5. Asman B., Engström P. E., Olsson T., Bergström K. Increased luminol enhanced chemiluminescence from peripheral granulocytes in juvenile periodontitis. Scand J Dent Res. 1984 Jun;92(3):218–223. doi: 10.1111/j.1600-0722.1984.tb00882.x. [DOI] [PubMed] [Google Scholar]
  6. Baeuerle P. A., Baltimore D. Activation of DNA-binding activity in an apparently cytoplasmic precursor of the NF-kappa B transcription factor. Cell. 1988 Apr 22;53(2):211–217. doi: 10.1016/0092-8674(88)90382-0. [DOI] [PubMed] [Google Scholar]
  7. Bartold P. M., Wiebkin O. W., Thonard J. C. The effect of oxygen-derived free radicals on gingival proteoglycans and hyaluronic acid. J Periodontal Res. 1984 Jul;19(4):390–400. doi: 10.1111/j.1600-0765.1984.tb01012.x. [DOI] [PubMed] [Google Scholar]
  8. Bernard G. R. N-acetylcysteine in experimental and clinical acute lung injury. Am J Med. 1991 Sep 30;91(3C):54S–59S. doi: 10.1016/0002-9343(91)90284-5. [DOI] [PubMed] [Google Scholar]
  9. Bertolini D. R., Nedwin G. E., Bringman T. S., Smith D. D., Mundy G. R. Stimulation of bone resorption and inhibition of bone formation in vitro by human tumour necrosis factors. Nature. 1986 Feb 6;319(6053):516–518. doi: 10.1038/319516a0. [DOI] [PubMed] [Google Scholar]
  10. Breimer L. H. Repair of DNA damage induced by reactive oxygen species. Free Radic Res Commun. 1991;14(3):159–171. doi: 10.3109/10715769109088945. [DOI] [PubMed] [Google Scholar]
  11. Carlsson J., Larsen J. T., Edlund M. B. Peptostreptococcus micros has a uniquely high capacity to form hydrogen sulfide from glutathione. Oral Microbiol Immunol. 1993 Feb;8(1):42–45. doi: 10.1111/j.1399-302x.1993.tb00541.x. [DOI] [PubMed] [Google Scholar]
  12. Carlsson J., Larsen J. T., Edlund M. B. Utilization of glutathione (L-gamma-glutamyl-L-cysteinylglycine) by Fusobacterium nucleatum subspecies nucleatum. Oral Microbiol Immunol. 1994 Oct;9(5):297–300. doi: 10.1111/j.1399-302x.1994.tb00074.x. [DOI] [PubMed] [Google Scholar]
  13. Cerná H., Fiala B., Fingerová H., Pohanka J., Szwarcová E. Contribution to indication of total therapy with vitamin E in chronic periodontal disease (pilot study). Acta Univ Palacki Olomuc Fac Med. 1984;107:167–170. [PubMed] [Google Scholar]
  14. Chapple I. L., Cross I. A., Glenwright H. D., Matthews J. B. Calibration and reliability of the Periotron 6000 for individual gingival crevicular fluid samples. J Periodontal Res. 1995 Jan;30(1):73–79. doi: 10.1111/j.1600-0765.1995.tb01255.x. [DOI] [PubMed] [Google Scholar]
  15. Charon J. A., Mergenhagen S. E., Gallin J. I. Gingivitis and oral ulceration in patients with neutrophil dysfunction. J Oral Pathol. 1985 Feb;14(2):150–155. doi: 10.1111/j.1600-0714.1985.tb00478.x. [DOI] [PubMed] [Google Scholar]
  16. Claesson R., Granlund-Edstedt M., Persson S., Carlsson J. Activity of polymorphonuclear leukocytes in the presence of sulfide. Infect Immun. 1989 Sep;57(9):2776–2781. doi: 10.1128/iai.57.9.2776-2781.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Cohen S. G., Greenberg M. S. Chronic oral herpes simplex virus infection in immunocompromised patients. Oral Surg Oral Med Oral Pathol. 1985 May;59(5):465–471. doi: 10.1016/0030-4220(85)90085-4. [DOI] [PubMed] [Google Scholar]
  18. Cooper B., Creeth J. M., Donald A. S. Studies of the limited degradation of mucus glycoproteins. The mechanism of the peroxide reaction. Biochem J. 1985 Jun 15;228(3):615–626. doi: 10.1042/bj2280615. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Crompton M., Costi A., Hayat L. Evidence for the presence of a reversible Ca2+-dependent pore activated by oxidative stress in heart mitochondria. Biochem J. 1987 Aug 1;245(3):915–918. doi: 10.1042/bj2450915. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Curnutte J. T., Babior B. M. Chronic granulomatous disease. Adv Hum Genet. 1987;16:229–297. doi: 10.1007/978-1-4757-0620-8_4. [DOI] [PubMed] [Google Scholar]
  21. Dean R. T., Thomas S. M., Garner A. Free-radical-mediated fragmentation of monoamine oxidase in the mitochondrial membrane. Roles for lipid radicals. Biochem J. 1986 Dec 1;240(2):489–494. doi: 10.1042/bj2400489. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Delgado W., Calderón R. Acatalasia in two Peruvian siblings. J Oral Pathol. 1979 Dec;8(6):358–368. doi: 10.1111/j.1600-0714.1979.tb01839.x. [DOI] [PubMed] [Google Scholar]
  23. Dröge W., Eck H. P., Näher H., Pekar U., Daniel V. Abnormal amino-acid concentrations in the blood of patients with acquired immunodeficiency syndrome (AIDS) may contribute to the immunological defect. Biol Chem Hoppe Seyler. 1988 Mar;369(3):143–148. doi: 10.1515/bchm3.1988.369.1.143. [DOI] [PubMed] [Google Scholar]
  24. Esterbauer H., Striegl G., Puhl H., Oberreither S., Rotheneder M., el-Saadani M., Jürgens G. The role of vitamin E and carotenoids in preventing oxidation of low density lipoproteins. Ann N Y Acad Sci. 1989;570:254–267. doi: 10.1111/j.1749-6632.1989.tb14925.x. [DOI] [PubMed] [Google Scholar]
  25. Fanger M. W., Hart D. A., Wells J. V., Nisonoff A. Enhancement by reducing agents of the transformation of human and rabbit peripheral lymphocytes. J Immunol. 1970 Oct;105(4):1043–1045. [PubMed] [Google Scholar]
  26. Fridovich I. Superoxide dismutases. An adaptation to a paramagnetic gas. J Biol Chem. 1989 May 15;264(14):7761–7764. [PubMed] [Google Scholar]
  27. Grootveld M., Halliwell B. Measurement of allantoin and uric acid in human body fluids. A potential index of free-radical reactions in vivo? Biochem J. 1987 May 1;243(3):803–808. doi: 10.1042/bj2430803. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Guarnieri C., Zucchelli G., Bernardi F., Scheda M., Valentini A. F., Calandriello M. Enhanced superoxide production with no change of the antioxidant activity in gingival fluid of patients with chronic adult periodontitis. Free Radic Res Commun. 1991;15(1):11–16. doi: 10.3109/10715769109049120. [DOI] [PubMed] [Google Scholar]
  29. Gutteridge J. M. Antioxidant properties of the proteins caeruloplasmin, albumin and transferrin. A study of their activity in serum and synovial fluid from patients with rheumatoid arthritis. Biochim Biophys Acta. 1986 Jan 30;869(2):119–127. doi: 10.1016/0167-4838(86)90286-4. [DOI] [PubMed] [Google Scholar]
  30. Gutteridge J. M. Biological origin of free radicals, and mechanisms of antioxidant protection. Chem Biol Interact. 1994 Jun;91(2-3):133–140. doi: 10.1016/0009-2797(94)90033-7. [DOI] [PubMed] [Google Scholar]
  31. Gutteridge J. M., Paterson S. K., Segal A. W., Halliwell B. Inhibition of lipid peroxidation by the iron-binding protein lactoferrin. Biochem J. 1981 Oct 1;199(1):259–261. doi: 10.1042/bj1990259. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Gutteridge J. M., Stocks J. Caeruloplasmin: physiological and pathological perspectives. Crit Rev Clin Lab Sci. 1981;14(4):257–329. doi: 10.3109/10408368109105866. [DOI] [PubMed] [Google Scholar]
  33. Gutteridge J. M. The antioxidant activity of haptoglobin towards haemoglobin-stimulated lipid peroxidation. Biochim Biophys Acta. 1987 Feb 14;917(2):219–223. doi: 10.1016/0005-2760(87)90125-1. [DOI] [PubMed] [Google Scholar]
  34. Halliwell B., Gutteridge J. M., Cross C. E. Free radicals, antioxidants, and human disease: where are we now? J Lab Clin Med. 1992 Jun;119(6):598–620. [PubMed] [Google Scholar]
  35. Halliwell B., Gutteridge J. M. The antioxidants of human extracellular fluids. Arch Biochem Biophys. 1990 Jul;280(1):1–8. doi: 10.1016/0003-9861(90)90510-6. [DOI] [PubMed] [Google Scholar]
  36. Halliwell B. How to characterize a biological antioxidant. Free Radic Res Commun. 1990;9(1):1–32. doi: 10.3109/10715769009148569. [DOI] [PubMed] [Google Scholar]
  37. Henry C. A., Winford T. E., Laohapund P., Yotnuengnit P. Neutrophil chemi-luminescence and opsonic activities of young people with periodontitis in Thailand. Arch Oral Biol. 1984;29(8):623–627. doi: 10.1016/0003-9969(84)90132-8. [DOI] [PubMed] [Google Scholar]
  38. Imlay J. A., Fridovich I. Assay of metabolic superoxide production in Escherichia coli. J Biol Chem. 1991 Apr 15;266(11):6957–6965. [PubMed] [Google Scholar]
  39. Jackson J. H., Gajewski E., Schraufstatter I. U., Hyslop P. A., Fuciarelli A. F., Cochrane C. G., Dizdaroglu M. Damage to the bases in DNA induced by stimulated human neutrophils. J Clin Invest. 1989 Nov;84(5):1644–1649. doi: 10.1172/JCI114342. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Jacob R. A., Omaye S. T., Skala J. H., Leggott P. J., Rothman D. L., Murray P. A. Experimental vitamin C depletion and supplementation in young men. Nutrient interactions and dental health effects. Ann N Y Acad Sci. 1987;498:333–346. doi: 10.1111/j.1749-6632.1987.tb23772.x. [DOI] [PubMed] [Google Scholar]
  41. Key L. L., Jr, Wolf W. C., Gundberg C. M., Ries W. L. Superoxide and bone resorption. Bone. 1994 Jul-Aug;15(4):431–436. doi: 10.1016/8756-3282(94)90821-4. [DOI] [PubMed] [Google Scholar]
  42. Krinsky N. I. Antioxidant functions of carotenoids. Free Radic Biol Med. 1989;7(6):617–635. doi: 10.1016/0891-5849(89)90143-3. [DOI] [PubMed] [Google Scholar]
  43. LOE H., THEILADE E., JENSEN S. B. EXPERIMENTAL GINGIVITIS IN MAN. J Periodontol. 1965 May-Jun;36:177–187. doi: 10.1902/jop.1965.36.3.177. [DOI] [PubMed] [Google Scholar]
  44. Leggott P. J., Robertson P. B., Jacob R. A., Zambon J. J., Walsh M., Armitage G. C. Effects of ascorbic acid depletion and supplementation on periodontal health and subgingival microflora in humans. J Dent Res. 1991 Dec;70(12):1531–1536. doi: 10.1177/00220345910700121101. [DOI] [PubMed] [Google Scholar]
  45. Liang C. M., Lee N., Cattell D., Liang S. M. Glutathione regulates interleukin-2 activity on cytotoxic T-cells. J Biol Chem. 1989 Aug 15;264(23):13519–13523. [PubMed] [Google Scholar]
  46. Libermann T. A., Baltimore D. Activation of interleukin-6 gene expression through the NF-kappa B transcription factor. Mol Cell Biol. 1990 May;10(5):2327–2334. doi: 10.1128/mcb.10.5.2327. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Lunec J., Blake D. R. The determination of dehydroascorbic acid and ascorbic acid in the serum and synovial fluid of patients with rheumatoid arthritis (RA). Free Radic Res Commun. 1985;1(1):31–39. doi: 10.3109/10715768509056534. [DOI] [PubMed] [Google Scholar]
  48. Maly F. E. The B lymphocyte: a newly recognized source of reactive oxygen species with immunoregulatory potential. Free Radic Res Commun. 1990;8(3):143–148. doi: 10.3109/10715769009087987. [DOI] [PubMed] [Google Scholar]
  49. Marucha P. T., Zeff R. A., Kreutzer D. L. Regulation of IL-1 beta gene expression in human peripheral blood PMN. J Periodontal Res. 1991 May;26(3 Pt 2):264–267. doi: 10.1111/j.1600-0765.1991.tb01654.x. [DOI] [PubMed] [Google Scholar]
  50. McCord J. M., Fridovich I. Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J Biol Chem. 1969 Nov 25;244(22):6049–6055. [PubMed] [Google Scholar]
  51. Meichle A., Schütze S., Hensel G., Brunsing D., Krönke M. Protein kinase C-independent activation of nuclear factor kappa B by tumor necrosis factor. J Biol Chem. 1990 May 15;265(14):8339–8343. [PubMed] [Google Scholar]
  52. Meyle J., Kapitza K. Assay of ascorbic acid in human crevicular fluid from clinically healthy gingival sites by high-performance liquid chromatography. Arch Oral Biol. 1990;35(4):319–323. doi: 10.1016/0003-9969(90)90049-g. [DOI] [PubMed] [Google Scholar]
  53. Moore S., Calder K. A., Miller N. J., Rice-Evans C. A. Antioxidant activity of saliva and periodontal disease. Free Radic Res. 1994 Nov-Dec;21(6):417–425. doi: 10.3109/10715769409056594. [DOI] [PubMed] [Google Scholar]
  54. Morris P. E., Bernard G. R. Significance of glutathione in lung disease and implications for therapy. Am J Med Sci. 1994 Feb;307(2):119–127. doi: 10.1097/00000441-199402000-00010. [DOI] [PubMed] [Google Scholar]
  55. Morrow J. D., Hill K. E., Burk R. F., Nammour T. M., Badr K. F., Roberts L. J., 2nd A series of prostaglandin F2-like compounds are produced in vivo in humans by a non-cyclooxygenase, free radical-catalyzed mechanism. Proc Natl Acad Sci U S A. 1990 Dec;87(23):9383–9387. doi: 10.1073/pnas.87.23.9383. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Niki E. Lipid antioxidants: how they may act in biological systems. Br J Cancer Suppl. 1987 Jun;8:153–157. [PMC free article] [PubMed] [Google Scholar]
  57. Pacht E. R., Timerman A. P., Lykens M. G., Merola A. J. Deficiency of alveolar fluid glutathione in patients with sepsis and the adult respiratory distress syndrome. Chest. 1991 Nov;100(5):1397–1403. doi: 10.1378/chest.100.5.1397. [DOI] [PubMed] [Google Scholar]
  58. Page R. C., Schroeder H. E. Pathogenesis of inflammatory periodontal disease. A summary of current work. Lab Invest. 1976 Mar;34(3):235–249. [PubMed] [Google Scholar]
  59. Persson S., Edlund M. B., Claesson R., Carlsson J. The formation of hydrogen sulfide and methyl mercaptan by oral bacteria. Oral Microbiol Immunol. 1990 Aug;5(4):195–201. doi: 10.1111/j.1399-302x.1990.tb00645.x. [DOI] [PubMed] [Google Scholar]
  60. Pryor W. A. Oxy-radicals and related species: their formation, lifetimes, and reactions. Annu Rev Physiol. 1986;48:657–667. doi: 10.1146/annurev.ph.48.030186.003301. [DOI] [PubMed] [Google Scholar]
  61. Schraufstätter I. U., Browne K., Harris A., Hyslop P. A., Jackson J. H., Quehenberger O., Cochrane C. G. Mechanisms of hypochlorite injury of target cells. J Clin Invest. 1990 Feb;85(2):554–562. doi: 10.1172/JCI114472. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Schreck R., Rieber P., Baeuerle P. A. Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-kappa B transcription factor and HIV-1. EMBO J. 1991 Aug;10(8):2247–2258. doi: 10.1002/j.1460-2075.1991.tb07761.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Schröder J. M., Mrowietz U., Morita E., Christophers E. Purification and partial biochemical characterization of a human monocyte-derived, neutrophil-activating peptide that lacks interleukin 1 activity. J Immunol. 1987 Nov 15;139(10):3474–3483. [PubMed] [Google Scholar]
  64. Shirakawa F., Chedid M., Suttles J., Pollok B. A., Mizel S. B. Interleukin 1 and cyclic AMP induce kappa immunoglobulin light-chain expression via activation of an NF-kappa B-like DNA-binding protein. Mol Cell Biol. 1989 Mar;9(3):959–964. doi: 10.1128/mcb.9.3.959. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Slade E. W., Jr, Bartuska D., Rose L. F., Cohen D. W. Vitamin E and periodontal disease. J Periodontol. 1976 Jun;47(6):352–354. doi: 10.1902/jop.1976.47.6.352. [DOI] [PubMed] [Google Scholar]
  66. Staal F. J., Roederer M., Herzenberg L. A., Herzenberg L. A. Intracellular thiols regulate activation of nuclear factor kappa B and transcription of human immunodeficiency virus. Proc Natl Acad Sci U S A. 1990 Dec;87(24):9943–9947. doi: 10.1073/pnas.87.24.9943. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Stocks J., Gutteridge J. M., Sharp R. J., Dormandy T. L. The inhibition of lipid autoxidation by human serum and its relation to serum proteins and alpha-tocopherol. Clin Sci Mol Med. 1974 Sep;47(3):223–233. doi: 10.1042/cs0470223. [DOI] [PubMed] [Google Scholar]
  68. Suthanthiran M., Anderson M. E., Sharma V. K., Meister A. Glutathione regulates activation-dependent DNA synthesis in highly purified normal human T lymphocytes stimulated via the CD2 and CD3 antigens. Proc Natl Acad Sci U S A. 1990 May;87(9):3343–3347. doi: 10.1073/pnas.87.9.3343. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Sutton H. C., Winterbourn C. C. On the participation of higher oxidation states of iron and copper in Fenton reactions. Free Radic Biol Med. 1989;6(1):53–60. doi: 10.1016/0891-5849(89)90160-3. [DOI] [PubMed] [Google Scholar]
  70. Varani J., Fligiel S. E., Till G. O., Kunkel R. G., Ryan U. S., Ward P. A. Pulmonary endothelial cell killing by human neutrophils. Possible involvement of hydroxyl radical. Lab Invest. 1985 Dec;53(6):656–663. [PubMed] [Google Scholar]
  71. Vincenti M. P., Burrell T. A., Taffet S. M. Regulation of NF-kappa B activity in murine macrophages: effect of bacterial lipopolysaccharide and phorbol ester. J Cell Physiol. 1992 Jan;150(1):204–213. doi: 10.1002/jcp.1041500127. [DOI] [PubMed] [Google Scholar]
  72. Wayner D. D., Burton G. W., Ingold K. U., Barclay L. R., Locke S. J. The relative contributions of vitamin E, urate, ascorbate and proteins to the total peroxyl radical-trapping antioxidant activity of human blood plasma. Biochim Biophys Acta. 1987 Jun 22;924(3):408–419. doi: 10.1016/0304-4165(87)90155-3. [DOI] [PubMed] [Google Scholar]
  73. Weiss S. J. Tissue destruction by neutrophils. N Engl J Med. 1989 Feb 9;320(6):365–376. doi: 10.1056/NEJM198902093200606. [DOI] [PubMed] [Google Scholar]
  74. van der Hoeven J. S., van den Kieboom C. W., Schaeken M. J. Sulfate-reducing bacteria in the periodontal pocket. Oral Microbiol Immunol. 1995 Oct;10(5):288–290. doi: 10.1111/j.1399-302x.1995.tb00156.x. [DOI] [PubMed] [Google Scholar]

Articles from Clinical Molecular Pathology are provided here courtesy of BMJ Publishing Group

RESOURCES