Immunoregulatory control of Th1/Th2 cytokine profiles in periodontal disease
2004; Wiley; Volume: 35; Issue: 1 Linguagem: Inglês
10.1111/j.0906-6713.2004.003557.x
ISSN1600-0757
Autores Tópico(s)Oral microbiology and periodontitis research
ResumoPeriodontology 2000Volume 35, Issue 1 p. 21-41 Immunoregulatory control of Th1/Th2 cytokine profiles in periodontal disease Erica Gemmell, Erica GemmellSearch for more papers by this authorGregory J. Seymour, Gregory J. SeymourSearch for more papers by this author Erica Gemmell, Erica GemmellSearch for more papers by this authorGregory J. Seymour, Gregory J. SeymourSearch for more papers by this author First published: 23 April 2004 https://doi.org/10.1111/j.0906-6713.2004.003557.xCitations: 155Read the full textAboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onEmailFacebookTwitterLinkedInRedditWechat References 1 Akbari O, DeKruyff RH, Umetsu DT. Pulmonary dendritic cells producing IL-10 mediate tolerance induced by respiratory exposure to antigen. Nat Immunol 2001: 2: 725–731. 10.1038/90667 CASPubMedWeb of Science®Google Scholar 2 Allison JP. CD28-B7 interactions in T-cell activation. Curr Opin Immunol 1994: 6: 414–419. 10.1016/0952-7915(94)90120-1 CASPubMedWeb of Science®Google Scholar 3 Ando T, Kato T, Ishihara K, Ogiuchi H, Okuda K. Heat shock proteins in the human periodontal disease process. Microbiol Immunol 1995: 39: 321–327. 10.1111/j.1348-0421.1995.tb02208.x CASPubMedWeb of Science®Google Scholar 4 Aoyagi T, Sugawara-Aoyagi M, Yamazaki K, Hara K. Interleukin 4 (IL-4) and IL-6-producing memory T-cells in peripheral blood and gingival tissues in periodontitis patients with high serum antibody titers to Porphyromonas gingivalis. Oral Microbiol Immunol 1995: 10: 304–310. 10.1111/j.1399-302X.1995.tb00159.x CASPubMedWeb of Science®Google Scholar 5 Aoyagi T, Yamazaki K, Kabasawa-Katoh Y, Nakajima T, Yamashita N, Yoshie H, Hara K. Elevated CTLA-4 expression on CD4 T cells from periodontitis patients stimulated with Porphyromonas gingivalis outer membrane antigen. Clin Exp Immunol 2000: 119: 280–286. 10.1046/j.1365-2249.2000.01126.x CASPubMedWeb of Science®Google Scholar 6 Ashkenazi M, White RR, Dennison DK. Neutrophil modulation by Actinobacillus actinomycetemcomitans. I. Chemotaxis, surface receptor expression and F-actin polymerization. J Periodontal Res 1992: 27: 264–273. 10.1111/j.1600-0765.1992.tb01677.x PubMedWeb of Science®Google Scholar 7 Ashkenazi M, White RR, Dennison DK. Neutrophil modulation by Actinobacillus actinomycetemcomitans. II. Phagocytosis and development of respiratory burst. J Periodontal Res 1992: 27: 457–465. 10.1111/j.1600-0765.1992.tb01818.x PubMedWeb of Science®Google Scholar 8 Attstrom R, Schroeder HE. Effect of experimental neutropenia on initial gingivitis in dogs. Scand J Dent Res 1979: 87: 7–23. CASPubMedWeb of Science®Google Scholar 9 Baggiolini M, Dewald B, Moser B. Human chemokines: an update. Annu Rev Immunol 1997: 15: 675–705. 10.1146/annurev.immunol.15.1.675 CASPubMedWeb of Science®Google Scholar 10 Baker PJ, Wilson ME. Opsonic IgG antibody against Actinobacillus actinomycetemcomitans in localized juvenile periodontitis. Oral Microbiol Immunol 1989: 4: 98–105. 10.1111/j.1399-302X.1989.tb00106.x CASPubMedWeb of Science®Google Scholar 11 Baker PJ, Evans RT, Roopenian DC. Oral infection with Porphyromonas gingivalis and induced alveolar bone loss in immunocompetent and severe combined immunodeficient mice. Arch Oral Biol 1994: 39: 1035–1040. 10.1016/0003-9969(94)90055-8 CASPubMedWeb of Science®Google Scholar 12 Baker PJ, Dixon M, Evans RT, Dufour L, Johnson E, Roopenian DC. CD4+ T cells and the proinflammatory cytokines γ interferon and interleukin-6 contribute to alveolar bone loss in mice. Infect Immun 1999: 67: 2804–2809. 10.1128/IAI.67.6.2804-2809.1999 CASPubMedWeb of Science®Google Scholar 13 Baker PJ, Dixon M, Roopenian DC. Genetic control of susceptibility to Porphyromonas gingivalis-induced alveolar bone loss in mice. Infect Immun 2000: 68: 5864–5868. 10.1128/IAI.68.10.5864-5868.2000 CASPubMedWeb of Science®Google Scholar 14 Bartova J, Kratka Opatrna Z, Prochazkova J, Krejsa O, Duskova J, Mrklas L, Tlaskalova H, Cukrowska B. Th1 and Th2 cytokine profile in patients with early onset periodontitis and their healthy siblings. Mediators Inflamm 2000: 9: 115–120. 10.1080/096293500411587 CASPubMedWeb of Science®Google Scholar 15 Belov L, De La Vega O, Dos Remedios CG, Mulligan SP, Christopherson RI. Immunophenotyping of leukemias using a cluster of differentiation antibody microarray. Cancer Res 2001: 61: 4483–4489. CASPubMedWeb of Science®Google Scholar 16 Bird PS, Gemmell E, Polak B, Paton RG, Sosroseno W, Seymour GJ. Protective immunity to Porphyromonas gingivalis infection in a murine model. J Periodontol 1995: 66: 351–362. 10.1902/jop.1995.66.5.351 PubMedWeb of Science®Google Scholar 17 Bloom BR, Salgame P. Diamond B. Revisiting and revising suppressor T cells. Immunol Today 1992: 13: 131–136. 10.1016/0167-5699(92)90110-S CASPubMedWeb of Science®Google Scholar 18 Boyatzis S, Seymour GJ. Effect of age and periodontal disease status in man on the spontaneous proliferation of peripheral blood lymphocytes. Arch Oral Biol 1986: 31: 749–755. 10.1016/0003-9969(86)90007-5 CASPubMedWeb of Science®Google Scholar 19 Boyton RJ, Altmann DM. Is selection for T-cell receptor affinity a factor in cytokine polarization? Trends Immunol 2002: 23: 526–529. 10.1016/S1471-4906(02)02319-0 CASPubMedWeb of Science®Google Scholar 20 Boyton RJ, Zaccai N, Jones EY, Altmann DM. CD4 T cells selected by antigen under Th2 polarizing conditions favor an elongated T-cell receptor α chain complementarity-determining region 3. J Immunol 2002: 168: 1018–1027. 10.4049/jimmunol.168.3.1018 CASPubMedWeb of Science®Google Scholar 21 Bredius RG, Derkx BH, Fijen CA, De-Wit TP, De Haas M, Weening RS, Vande Winkel JG, Out TA. Fc γ receptor IIa (CD32) polymorphism in fulminant meningococcal septic shock in children. J Infect Dis 1994: 170: 848–853. 10.1093/infdis/170.4.848 CASPubMedWeb of Science®Google Scholar 22 Breivik T, Thrane PS, Gjermo P, Opstad PK. Glucocorticoid receptor antagonist RU 486 treatment reduces periodontitis in Fischer 344 rats. J Periodontal Res 2000: 35: 285–290. 10.1034/j.1600-0765.2000.035005285.x CASPubMedWeb of Science®Google Scholar 23 Busch DH, Pamer EG. T cell affinity maturation by selective expansion during infection. J Exp Med 1999: 189: 701–710. 10.1084/jem.189.4.701 CASPubMedWeb of Science®Google Scholar 24 Chambers CA, Allison JP. Co-stimulation in T cell responses. Curr Opin Immunol 1997: 9: 396–404. 10.1016/S0952-7915(97)80087-8 CASPubMedWeb of Science®Google Scholar 25 Champaiboon C, Yongvanitchit K, Pichyangkul S, Mahanonda R. The immune modulation of B-cell responses by Porphyromonas gingivalis and interleukin-10. J Periodontol 2000: 71: 468–475. 10.1902/jop.2000.71.3.468 CASPubMedWeb of Science®Google Scholar 26 Chapple CC, Srivastava M, Hunter N. Failure of macrophage activation in destructive periodontal disease. J Pathol 1998: 186: 281–286. 10.1002/(SICI)1096-9896(1998110)186:3 3.0.CO;2-7 CASPubMedWeb of Science®Google Scholar 27 Chen PB, Davern LB, Schifferle R, Zambon JJ. Protective immunization against experimental Bacteroides (Porphyromonas) gingivalis infection. Infect Immun 1990: 58: 3394–3400. 10.1128/iai.58.10.3394-3400.1990 PubMedWeb of Science®Google Scholar 28 Chen PB, Davern LB, Katz J, Eldridge JH, Michalek SM. Host responses induced by co-infection with Porphyromonas gingivalis and Actinobacillus actinomycetemcomitans in a murine model. Oral Microbiol Immunol 1996: 11: 274–281. 10.1111/j.1399-302X.1996.tb00181.x PubMedWeb of Science®Google Scholar 29 Chensue SW, Warmington KS, Ruth JH, Sanghi PS, Lincoln P, Kunkel SL. Role of monocyte chemoattractant protein-1 (MCP-1) in Th1 (mycobacterial) and Th2 (schistosomal) antigen-induced granuloma formation: relationship to local inflammation, Th cell expression, and IL-12 production. J Immunol 1996: 157: 4602–4608. CASPubMedWeb of Science®Google Scholar 30 Chiu B. Multiple infections in carotid atherosclerotic plaques. Am Heart J 1999: 138: S534–536. 10.1016/S0002-8703(99)70294-2 CASPubMedWeb of Science®Google Scholar 31 Choi JI, Borrello MA, Smith ES, Zauderer M. Polarization of Porphyromonas gingivalis-specific helper T-cell subsets by prior immunization with Fusobacterium nucleatum. Oral Microbiol Immunol 2000: 15: 181–187. 10.1034/j.1399-302x.2000.150306.x CASPubMedWeb of Science®Google Scholar 32 Cohen DW. Periodontal medicine in the next millennium. Refuat Hapeh Vehashinayim 2001: 18: 6–8, 60. CASPubMedGoogle Scholar 33 Colombo AP, Eftimiadi C, Haffajee AD, Cugini MA, Socransky SS. Serum IgG2 level, Gm (23) allotype and FcγRIIa and FcγRIIIb receptors in refractory periodontal disease. J Clin Periodontol 1998: 25: 465–474. 10.1111/j.1600-051X.1998.tb02475.x CASPubMedWeb of Science®Google Scholar 34 Cottrez F, Hurst SD, Coffman RL, Groux H. T regulatory cells 1 inhibit a Th2-specific response in vivo. J Immunol 2000: 165: 4848–4853. 10.4049/jimmunol.165.9.4848 CASPubMedWeb of Science®Google Scholar 35 Cutler CW, Arnold RR, Schenkein HA. Inhibition of C3 and IgG proteolysis enhances phagocytosis of Porphyromonas gingivalis. J Immunol 1993: 151: 7016–7029. CASPubMedWeb of Science®Google Scholar 36 Cutler CW, Jotwani R, Palucka KA, Davoust J, Bell D, Banchereau J. Evidence and a novel hypothesis for the role of dendritic cells and Porphyromonas gingivalis in adult periodontitis. J Periodontal Res 1999: 34: 406–412. 10.1111/j.1600-0765.1999.tb02274.x CASPubMedWeb of Science®Google Scholar 37 Darveau RP, Cunningham MD, Bailey T, Seachord C, Ratcliffe K, Bainbridge B, Dietsch M, Paige RC, Aruffo A. Ability of bacteria associated with chronic inflammatory disease to stimulate E-selectin expression and promote neutrophil adhesion. Infect Immun 1995: 63: 1311–1317. 10.1128/IAI.63.4.1311-1317.1995 CASPubMedWeb of Science®Google Scholar 38 Darveau RP, Tanner A, Page RC. The microbial challenge in periodontitis. Periodontol 2000 1997: 14: 12–32. 10.1111/j.1600-0757.1997.tb00190.x CASPubMedWeb of Science®Google Scholar 39 Dasanayake AP. Poor periodontal health of the pregnant woman as a risk factor for low birth weight. Ann Periodontol 1998: 3: 206–212. 10.1902/annals.1998.3.1.206 CASPubMedGoogle Scholar 40 DeStefano F, Anda RF, Kahn HS, Williamson DF, Russell CM. Dental disease and risk of coronary heart disease and mortality. BMJ 1993: 306: 688–691. 10.1136/bmj.306.6879.688 CASPubMedWeb of Science®Google Scholar 41 Dhanasekaran SM, Barrette TR, Ghosh D, Shah R, Varambally S, Kurachi K, Pienta KJ, Rubin MA, Chinnaiyan AM. Delineation of prognostic biomarkers in prostate cancer. Nature 2001: 412: 822–826. 10.1038/35090585 CASPubMedWeb of Science®Google Scholar 42 Diab A, Abdalla H, Li HL, Shi FD, Zhu J, Hojberg B, Lindquist L, Wretlind B, Bakhiet M, Link H. Neutralization of macrophage inflammatory protein 2 (MIP-2) and MIP-1α attenuates neutrophil recruitment in the central nervous system during experimental bacterial meningitis. Infect Immun 1999: 67: 2590–2601. 10.1128/IAI.67.5.2590-2601.1999 CASPubMedWeb of Science®Google Scholar 43 Ebersole JL, Taubman MA. The protective nature of host responses in periodontal diseases. Periodontol 2000 1994: 5: 112–141. 10.1111/j.1600-0757.1994.tb00021.x CASPubMedGoogle Scholar 44 Ebersole JL, Feuille F, Kesavalu L, Holt SC. Host modulation of tissue destruction caused by periodontopathogens: effects on a mixed microbial infection composed of Porphyromonas gingivalis and Fusobacterium nucleatum. Microb Pathog 1997: 23: 23–32. 10.1006/mpat.1996.0129 CASPubMedWeb of Science®Google Scholar 45 Farber JM. Mig and IP-10: CXC chemokines that target lymphocytes. J Leukoc Biol 1997: 61: 246–257. 10.1002/jlb.61.3.246 CASPubMedWeb of Science®Google Scholar 46 Feuille F, Ebersole JL, Kesavalu L, Stepfen MJ, Holt SC. Mixed infection with Porphyromonas gingivalis and Fusobacterium nucleatum in a murine lesion model: potential synergistic effects on virulence. Infect Immun 1996: 64: 2094–2100. 10.1128/IAI.64.6.2094-2100.1996 CASPubMedWeb of Science®Google Scholar 47 Fives-Taylor P, Meyer D, Mintz K. Characteristics of Actinobacillus actinomycetemcomitans invasion of and adhesion to cultured epithelial cells. Adv Dent Res 1995: 9: 55–62. 10.1177/08959374950090011001 CASPubMedGoogle Scholar 48 Freeman GJ, Lombard DB, Gimmi CD, Brod SA, Lee K, Laning JC, Hafler DA, Dorf ME, Gray GS, Reiser H et al. CTLA-4 and CD28 mRNA are coexpressed in most T cells after activation. Expression of CTLA-4 and CD28 mRNA does not correlate with the pattern of lymphokine production. J Immunol 1992: 149: 3795–3801. 10.4049/jimmunol.149.12.3795 CASPubMedWeb of Science®Google Scholar 49 Fujihashi K, Kono Y, Yamamoto M, McGhee JR, Beagley K, Aicher WK, Kiyono H. Interleukin production by gingival mononuclear cells isolated from adult periodontitis patients. Dent Res 1991: 70: 550 (Abstract 2269). Google Scholar 50 Fujihashi K, Yamamoto M, McGhee JR, Kiyono H. Type 1/Type 2 cytokine production by CD4+ T cells in adult periodontitis. J Dent Res 1994: 73: 204 (Abstract 818). Web of Science®Google Scholar 51 Fukaura H, Kent SC, Pietrusewicz MJ, Khoury SJ, Weiner HL, Hafler DA. Induction of circulating myelin basic protein and proteolipid protein-specific transforming growth factor-β1-secreting Th3 T cells by oral administration of myelin in multiple sclerosis patients. J Clin Invest 1996: 98: 70–77. 10.1172/JCI118779 CASPubMedWeb of Science®Google Scholar 52 Galbraith GM, Steed RB, Sanders JJ, Pandey JP. Tumor necrosis factor α production by oral leukocytes: influence of tumor necrosis factor genotype. J Periodontol 1998: 69: 428–433. 10.1902/jop.1998.69.4.428 CASPubMedGoogle Scholar 53 Gamonal J, Bascones A, Jorge O, Silva A. Chemokine RANTES in gingival crevicular fluid of adult patients with periodontitis. J Clin Periodontol 2000: 27: 675–681. 10.1034/j.1600-051x.2000.027009675.x CASPubMedWeb of Science®Google Scholar 54 Gamonal J, Acevedo A, Bascones A, Jorge O, Silva A. Characterization of cellular infiltrate, detection of chemokine receptor CCR5 and interleukin-8 and RANTES chemokines in adult periodontitis. J Periodontal Res 2001: 36: 194–203. 10.1034/j.1600-0765.2001.360309.x CASPubMedWeb of Science®Google Scholar 55 Gangur V, Simons FE, Hayglass KT. Human IP-10 selectively promotes dominance of polyclonally activated and environmental antigen-driven IFN-γ over IL-4 responses. FASEB J 1998: 12: 705–713. 10.1096/fasebj.12.9.705 CASPubMedWeb of Science®Google Scholar 56 Gause WC, Halvorson MJ, Lu P, Greenwald R, Linsley P, Urban JF, Finkelman FD. The function of costimulatory molecules and the development of IL-4-producing T cells. Immunol Today 1997: 18: 115–120. 10.1016/S0167-5699(97)01005-0 CASPubMedWeb of Science®Google Scholar 57 Gemmell E, Seymour GJ. Different responses in B cells induced by Porphyromonas gingivalis and Fusobacterium nucleatum. Arch Oral Biol 1992: 37: 565–573. 10.1016/0003-9969(92)90139-Y PubMedWeb of Science®Google Scholar 58 Gemmell E, Seymour GJ. Interleukin 1, interleukin 6 and transforming growth factor-β production by human gingival mononuclear cells following stimulation with Porphyromonas gingivalis and Fusobacterium nucleatum. J Periodontal Res 1993: 28: 122–129. 10.1111/j.1600-0765.1993.tb01059.x PubMedWeb of Science®Google Scholar 59 Gemmell E, Seymour GJ. Modulation of immune responses to periodontal bacteria. Curr Opin Periodontol 1994: 94: 28–38. Google Scholar 60 Gemmell E, Seymour GJ. Cytokine profiles of cells extracted from humans with periodontal diseases. J Dent Res 1998: 77: 16–26. 10.1177/00220345980770010101 CASPubMedWeb of Science®Google Scholar 61 Gemmell E, Feldner B, Seymour GJ. CD45RA and CD45RO positive CD4 cells in human peripheral blood and periodontal disease tissue before and after stimulation with periodontopathic bacteria. Oral Microbiol Immunol 1992: 7: 84–88. 10.1111/j.1399-302X.1992.tb00514.x CASPubMedWeb of Science®Google Scholar 62 Gemmell E, Kjeldsen M, Yamazaki K, Nakajima T, Aldred MJ, Seymour GJ. Cytokine profiles of Porphyromonas gingivalis-reactive T lymphocyte line and clones derived from P. gingivalis-infected subjects. Oral Dis 1995: 1: 139–146. 10.1111/j.1601-0825.1995.tb00176.x CASPubMedGoogle Scholar 63 Gemmell E, Marshall RI, Seymour GJ. Cytokines and prostaglandins in immune homeostasis and tissue destruction in periodontal disease. Periodontol 2000 1997: 14: 112–143. 10.1111/j.1600-0757.1997.tb00194.x CASPubMedWeb of Science®Google Scholar 64 Gemmell E, Grieco DA, Cullinan MP, Westerman B, Seymour GJ. The proportion of interleukin-4, interferon-10-positive cells in Porphyromonas gingivalis-specific T-cell lines established from P. gingivalis-positive subjects. Oral Microbiol Immunol 1999: 14: 267–274. 10.1034/j.1399-302X.1999.140501.x CASPubMedWeb of Science®Google Scholar 65 Gemmell E, Grieco DA, Seymour GJ. Chemokine expression in Porphyromonas gingivalis-specific T-cell lines. Oral Microbiol Immunol 2000: 15: 166–171. 10.1034/j.1399-302x.2000.150304.x CASPubMedWeb of Science®Google Scholar 66 Gemmell E, Winning TA, Grieco DA, Bird PS, Seymour GJ. The influence of genetic variation on the splenic T cell cytokine and specific serum antibody responses in Porphyromonas gingivalis in mice. J Periodontol 2000: 71: 1130–1138. 10.1902/jop.2000.71.7.1130 CASPubMedWeb of Science®Google Scholar 67 Gemmell E, Carter CL, Seymour GJ. Chemokines in human periodontal disease tissues. Clin Exp Immunol 2001: 125: 134–141. 10.1046/j.1365-2249.2001.01511.x CASPubMedWeb of Science®Google Scholar 68 Gemmell E, McHugh GB, Grieco DA, Seymour GJ. Costimulatory molecules in human periodontal disease tissues. J Periodontal Res 2001: 36: 92–100. 10.1034/j.1600-0765.2001.360205.x CASPubMedWeb of Science®Google Scholar 69 Gemmell E, Bird PS, Carter CL, Drysdale KE, Seymour GJ. Effect of Fusobacterium nucleatum on the T and B cell responses to Porphyromonas gingivalis in a mouse model. Clin Exp Immunol 2002: 128: 238–244. 10.1046/j.1365-2249.2002.01852.x CASPubMedWeb of Science®Google Scholar 70 Gemmell E, Carter CL, Grieco DA, Sugerman PB, Seymour GJ. P. gingivalis-specific T cell lines produce Th1 and Th2 cytokine. J Dent Res 2002: 81: 303–307. 10.1177/154405910208100503 CASPubMedWeb of Science®Google Scholar 71 Gemmell E, Carter CL, Hart DNJ, Drysdale KE, Seymour GJ. Antigen presenting cells in human periodontal disease tissues. Oral Microbiol Immunol 2003: 18: 388–393. Google Scholar 72 Genco CA, Kapczynski DR, Cutler CW, Arko RJ, Arnold RR. Influence of immunisation on Porphyromonas gingivalis colonisation and invasion in the mouse chamber model. Infect Immun 1992: 60: 1447–1454. PubMedWeb of Science®Google Scholar 73 Gilbert P, Das J, Foley I. Biofilm susceptibility to antimicrobials. Adv Dent Res 1997: 11: 160–167. 10.1177/08959374970110010701 CASPubMedGoogle Scholar 74 Greenberg SA. DNA microarray gene expression analysis technology and its application to neurological disorders. Neurology 2001: 57: 755–761. 10.1212/WNL.57.5.755 CASPubMedWeb of Science®Google Scholar 75 Groux H, O'Garra A, Bigler M, Rouleau M, Antonenko S, De Vries JE, Roncarolo MG. A CD4+ T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature 1997: 389: 737–742. 10.1038/39614 CASPubMedWeb of Science®Google Scholar 76 Gu L, Tseng S, Horner RM, Tam C, Loda M, Rollins BJ. Control of TH2 polarization by the chemokine monocyte chemoattractant protein-1. Nature 2000: 404: 407–411. 10.1038/35006097 CASPubMedWeb of Science®Google Scholar 77 Hemmerle J, Frank RM. Bacterial invasion of periodontal tissues after experimental immunosuppression in rats. J Biol Buccale 1991: 19: 271–282. CASPubMedGoogle Scholar 78 Hennig BJ, Parkhill JM, Chapple IL, Heasman PA, Taylor JJ. Dinucleotide repeat polymorphism in the interleukin-10 gene promoter (IL-10.G) and genetic susceptibility to early-onset periodontal disease. Genes Immun 2000: 1: 402–404. 10.1038/sj.gene.6363687 CASPubMedWeb of Science®Google Scholar 79 Hirschfeld M, Weis JJ, Toshchakov V, Salkowski CA, Cody MJ, Ward DC, Qureshi N, Michalek SM, Vogel SN. Signaling by toll-like receptor 2 and 4 agonists results in differential gene expression in murine macrophages. Infect Immun 2001: 69: 1477–1482. 10.1128/IAI.69.3.1477-1482.2001 CASPubMedWeb of Science®Google Scholar 80 Holt SC, Brunsvold M, Jones A, Wood R, Ebersole JL. Cell envelope and cell wall immunization of Macaca fascicularis: effect on the progression of ligature-induced periodontitis. Oral Microbiol Immunol 1995: 10: 321–333. 10.1111/j.1399-302X.1995.tb00162.x PubMedWeb of Science®Google Scholar 81 Hotokezaka H, Hayashida H, Ohara N, Nomaguchi H, Kobayashi K, Yamada T. Cloning and sequencing of the groEL homologue from Porphyromonas gingivalis. Biochim Biophys Acta 1994: 1219: 175–178. 10.1016/0167-4781(94)90265-8 CASPubMedWeb of Science®Google Scholar 82 Huang Q, Liu D, Majewski P, Schulte LC, Korn JM, Young RA, Lander ES, Hacohen N. The plasticity of dendritic cell responses to pathogens and their components. Science 2001: 294: 870–875. 10.1126/science.294.5543.870 CASPubMedWeb of Science®Google Scholar 83 Iacopino AM. Diabetic periodontitis: possible lipid-induced defect in tissue repair through alteration of macrophage phenotype and function. Oral Dis 1995: 1: 214–229. 10.1111/j.1601-0825.1995.tb00187.x CASPubMedGoogle Scholar 84 Iezzi G, Scotet E, Scheidegger D, Lanzavecchia A. The interplay between the duration of T-cell receptor and cytokine signaling determines T cell polarization. Eur J Immunol 1999: 29: 4092–4101. 10.1002/(SICI)1521-4141(199912)29:12 3.0.CO;2-A CASPubMedWeb of Science®Google Scholar 85 Ishikawa I, Nakashima K, Koseki T, Nagasawa T, Watanabe H, Arakawa S, Nitta H, Nishihara T. Induction of the immune response to periodontopathic bacteria and its role in the pathogenesis of periodontitis. Periodontol 2000 1997: 14: 79–111. 10.1111/j.1600-0757.1997.tb00193.x CASPubMedWeb of Science®Google Scholar 86 Ivanyi L, Lehner T. Stimulation of lymphocyte transformation by bacterial antigens in patients with periodontal disease. Arch Oral Biol 1970: 15: 1089–1096. 10.1016/0003-9969(70)90121-4 CASPubMedWeb of Science®Google Scholar 87 Jenkins MK, Johnson JG. Molecules involved in T-cell costimulation. Curr Opin Immunol 1993: 5: 361–367. 10.1016/0952-7915(93)90054-V CASPubMedWeb of Science®Google Scholar 88 Johnston B, Burns AR, Suematsu M, Issekutz TB, Woodman RC, Kubes P. Chronic inflammation upregulates chemokine receptors and induces neutrophil migration to monocyte chemoattractant protein-1. J Clin Invest 1999: 103: 1269–1276. 10.1172/JCI5208 CASPubMedWeb of Science®Google Scholar 89 Joos TO, Schrenk M, Hopfl P, Kroger K, Chowdhury U, Stoll D, Schorner D, Durr M, Herick K, Rupp S, Sohn K, Hammerle H. A microarray enzyme-linked immunosorbent assay for autoimmune diagnostics. Electrophoresis 2000: 21: 2641–2650. 10.1002/1522-2683(20000701)21:13 3.0.CO;2-5 CASPubMedWeb of Science®Google Scholar 90 Jotwani R, Palucka AK, Al-Quotub M, Nouri-Shirazi M, Kim J, Bell D, Banchereau J, Cutler CC. Mature dendritic cells infiltrate the T cell-rich region of oral mucosa in chronic periodontitis: in situ, in vivo, and in vitro studies. J Immunol 2001: 167: 4693–4700. 10.4049/jimmunol.167.8.4693 CASPubMedWeb of Science®Google Scholar 91 Karatzas S, Novak MJ, Blieden TM. Cytokine production by Porphyromonas gingivalis-specific human T cells. J Dent Res 1996: 75: 322 (Abstract No. 2435). Google Scholar 92 Katz J, Michalek SM. Effect of immune T cells derived from mucosal or systemic tissue on host responses to Porphyromonas gingivalis. Oral Microbiol Immunol 1998: 13: 73–80. 10.1111/j.1399-302X.1998.tb00716.x CASPubMedWeb of Science®Google Scholar 93 Katz J, Ward DC, Michalek SM. Effect of host responses on the pathogenicity of strains of Porphyromonas gingivalis. Oral Microbiol Immunol 1996: 5: 309–318. 10.1111/j.1399-302X.1996.tb00187.x Web of Science®Google Scholar 94 Kaufmann SH. Heat shock proteins and the immune response. Immunol Today 1990: 11: 129–136. 10.1016/0167-5699(90)90050-J CASPubMedWeb of Science®Google Scholar 95 Kawai T, Eisen Lev R, Seki M, Eastcott JW, Wilson ME, Taubman MA. Requirement of B7 costimulation for Th1-mediated inflammatory bone resorption in experimental periodontal disease. J Immunol 2000: 164: 2102–2109. 10.4049/jimmunol.164.4.2102 CASPubMedWeb of Science®Google Scholar 96 Kesavalu L, Ebersole JL, Machen RL, Holt SC. Porphyromonas gingivalis virulence in mice: Induction of immunity to bacterial components. Infect Immun 1992: 60: 1455–1464. 10.1128/iai.60.4.1455-1464.1992 CASPubMedWeb of Science®Google Scholar 97 Kim JJ, Nottingham LK, Sin JI, Tsai A, Morrison L, Oh J, Dang K, Hu Y, Kazahaya K, Bennett M, Dentchev T, Wilson DM, Chalian AA, Boyer JD, Agadjanyan MG, Weiner DB. CD8 positive T cells influence antigen-specific immune responses through the expression of chemokines. J Clin Invest 1998: 102: 1112–1124. 10.1172/JCI3986 CASPubMedWeb of Science®Google Scholar 98 Klein J, Hoøejší V. Immunology, Chapter 19. Oxford: Blackwell Science, 1997: 515–521. Web of Science®Google Scholar 99 Knight SC, Stagg AJ. Antigen-presenting cell types. Curr Opin Immunol 1993: 5: 374–382. 10.1016/0952-7915(93)90056-X CASPubMedWeb of Science®Google Scholar 100 Kohler JJ, Pathangey LB, Brown TA. Oral immunization with recombinant Salmonella typhimurium expressing a cloned Porphyromonas gingivalis hemagglutinin: effect of boosting on mucosal, systemic and immunoglobulin G subclass response. Oral Microbiol Immunol 1998: 13: 81–88. 10.1111/j.1399-302X.1998.tb00717.x CASPubMedWeb of Science®Google Scholar 101 Kornman KS, Crane A, Wang HY, Di Giovine FS, Newman MG, Pirk FW, Wilson TG, Jr, Higginbottom FL, Duff GW. The interleukin-1 genotype as a severity factor in adult periodontal disease. J Clin Periodontol 1997: 24: 72–77. 10.1111/j.1600-051X.1997.tb01187.x CASPubMedWeb of Science®Google Scholar 102 Kornman KS, Page RC, Tonetti MS. The host response to the microbial challenge in periodontitis: assembling the players. Periodontol 2000 1997: 14: 33–53. 10.1111/j.1600-0757.1997.tb00191.x CASPubMedWeb of Science®Google Scholar 103 Kornman KS, Pankow J, Offenbacher S, Beck J, Di Giovine F, Duff GW. Interleukin-1 genotypes and the association between periodontitis and cardiovascular disease. J Periodontal Res 1999: 34: 353–357. 10.1111/j.1600-0765.1999.tb02265.x CASPubMedWeb of Science®Google Scholar 104 Lamont RJ, Jenkinson HF. Life below the gum line: pathogenic mechanisms of Porphyromonas gingivalis. Microbiol Mol Biol Rev 1998: 62: 1244–1263. 10.1128/MMBR.62.4.1244-1263.1998 CASPubMedWeb of Science®Google Scholar 105 Lappin DF, MacLeod CP, Kerr A, Mitchell T, Kinane DF. Anti-inflammatory cytokine IL-10 and T cell cytokine profile in periodontitis granulation tissue. Clin Exp Immunol 2001: 123: 294–300. 10.1046/j.1365-2249.2001.01448.x CASPubMedWeb of Science®Google Scholar 106 Lee SC, Brummet ME, Shahabuddin S, Woodworth TG, Georas SN, Leiferman KM, Gilman SC, Stellato C, Gladue RP, Schleimer RP, Beck LA. Cutaneous injection of human subjects with macrophage inflammatory protein-1 α induces significant recruitment of neutrophils and monocytes. J Immunol 2000: 164: 3392–3401. 10.4049/jimmunol.164.6.3392 CASPubMedWeb of Science®Google Scholar 107 Lindhe J, Liljenberg B, Listgarten M. Some microbiological and histopathological features of periodontal disease in man. J Periodontol 1980: 51: 264–269. 10.1902/jop.1980.51.5.264 CASPubMedWeb of Science®Google Scholar 108 Linsley PS, Greene JL, Tan P, Bradshaw J, Ledbetter JA, Anasetti C, Damle NK. Coexpression and functional cooperation of CTLA-4 and CD28 on activated T lymphocytes. J Exp Med 1992: 176: 1595–1604. 10.1084/jem.176.6.1595 CASPubMedWeb of Science®Google Scholar 109 Lloyd AR, Oppenheim JJ. Poly's lament: the neglected role of the polymorphonuclear neutrophil in the afferent limb of the immune response. Immunol Today 1992: 13: 169–172. 10.1016/0167-5699(92)90121-M CASPubMedWeb of Science®Google Scholar 110 Lopatin DE, Blackburn E. Avidity and titer of immunoglobulin G subclasses to Porphyromonas gingivalis in adult periodontitis patients. Oral Microbiol Immunol 1992: 7: 332–337. 10.1111/j.1399-302X.1992.tb00632.x CASPubMedWeb of Science®Google Scholar 111 Lopatin DE, Shelburne CE, Van Poperin N, Kowalski CJ, Bagramian RA. Humoral immunity to stress proteins and periodontal disease. J Periodontol 1999: 70: 1185–1193. 10.1902/jop.1999.70.10.1185 CASPubMedWeb of Science®Google Scholar 112 Lourbakos A, Chinni C, Thompson P, Potempa J, Travis J, Mackie EJ, Pike RN. Cleavage and activation of proteinase-activated receptor-2 on human neutrophils by gingipain-R from Porphyromonas gingivalis. FEBS Lett 1998: 435: 45–48. 10.1016/S0014-5793(98)01036-9 CASPubMedWeb of Science®Google Scholar 113 Lu B, McBri
Referência(s)