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Polyclonal B‐cell activation in periodontitis*

1989; Wiley; Volume: 24; Issue: 4 Linguagem: Inglês

10.1111/j.1600-0765.1989.tb01787.x

1600-0765

John G. Tew, David Engel, D F Mangan,

Immune Response and Inflammation

Journal of Periodontal ResearchVolume 24, Issue 4 p. 225-241 Polyclonal B-cell activation in periodontitis* John Tew, Corresponding Author John Tew Virginia Commonwealth University, Richmond, VA, U.S.A.Address: Dr. John Tew, Department of Microbiology and Immunology, Medical College of Virginia, Virginia Commonwealth University, Richmond, VA 23298, U.S.A.Search for more papers by this authorDavid Engel, David Engel The University of Washington, Seattle, WA, U.S.A.Search for more papers by this authorDennis Mangan, Dennis Mangan The University of Rochester, Rochester, NY, U.S.A.Search for more papers by this author John Tew, Corresponding Author John Tew Virginia Commonwealth University, Richmond, VA, U.S.A.Address: Dr. John Tew, Department of Microbiology and Immunology, Medical College of Virginia, Virginia Commonwealth University, Richmond, VA 23298, U.S.A.Search for more papers by this authorDavid Engel, David Engel The University of Washington, Seattle, WA, U.S.A.Search for more papers by this authorDennis Mangan, Dennis Mangan The University of Rochester, Rochester, NY, U.S.A.Search for more papers by this author First published: July 1989 https://doi.org/10.1111/j.1600-0765.1989.tb01787.xCitations: 88 * Supported in part by USPHS grants DE08229, DE05I39, and DE06976, from the National Institutes of Health. 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J Periodont Res 1968; 3: 313–327. 10.1111/j.1600-0765.1968.tb01937.x CASPubMedGoogle Scholar 4 Schroeder HE, Page RC. Lymphocyte-fibroblast interaction in the pathogenesis of inflammatory gingival disease. Experientia 1972; 28: 1228–1230. 10.1007/BF01946188 PubMedWeb of Science®Google Scholar 5 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 6 Horton JE, Leikin S, Oppenheim JJ. Human lymphoproliferalive reaction to saliva and dental plaque deposits. An in vitro correlation with periodontal disease. J Periodontol 1972; 43: 522–527. 10.1902/jop.1972.43.9.522 PubMedWeb of Science®Google Scholar 7 Kiger RD, Wright WH, Creamer HR. The significance of lymphocyte transformation responses to various microbial stimulants. J Periodontol 1977; 45: 780–785. 10.1902/jop.1974.45.11.780 PubMedWeb of Science®Google Scholar 8 Osterberg SK, Page RC, Sims T, Wilde G. Blastogenic responsiveness of peripheral blood mononuclear cells from individuals with various forms of periodontitis and effects of treatment. J Clin Periodontol 1983; 10: 72–88. 10.1111/j.1600-051X.1983.tb01269.x PubMedWeb of Science®Google Scholar 9 Lopatin DE, Smith FN, Syed SA, Morrison EC. The effect of periodontal therapy on lymphocyte blastogenesis to plaque associated microorganisms. J Periodont Res 1983; 18: 93–102. 10.1111/j.1600-0765.1983.tb00340.x PubMedWeb of Science®Google Scholar 10 Donaldson SL, Ranney RR, Burmeister JA, Tew JG. Blastogenic responses by lymphocytes from periodontally healthy populations induced by periodontitis-associated bacteria. J Periodontol 1982; 53: 743–751. 10.1902/jop.1982.53.12.743 PubMedWeb of Science®Google Scholar 11 Engel D, Clagett J, Page RC, Williams B. Mitogenic activity of Actinomyces viscosus. I. Effects on murine B and T lymphocytes and partial characterization. J Immunol 1977; 118: 1466–1471. PubMedWeb of Science®Google Scholar 12 Burckhardt JJ, Guggenheim B, Hefti A. Are Actinomyces viscosus antigens B cell mitogens J Immunol 1977; 118: 1460–1465. CASPubMedWeb of Science®Google Scholar 13 Smith S, Bick PH, Miller GA, et al. Polyclonal B cell activation: Severe periodontal disease in young adults. Clin Immunol Immunopathol 1980; 16: 354–366. 10.1016/0090-1229(80)90141-5 CASPubMedWeb of Science®Google Scholar 14 Bick PH, Carpenter AB, Holdeman LV, et al. Polyclonal B-cell activation induced by extracts of gram-negative bacteria isolated from periodontally diseased sites. Infect Immun 1981; 34: 43–49. PubMedWeb of Science®Google Scholar 15 Donaldson SL, Bick PH, Moore WEC, Ranney RR, Burmeister JA, Tew JG. Polyclonal B-cell activating capacities of gram-positive bacteria frequently isolated from periodontally diseased sites. J Periodont Res 1982; 17: 569–575. 10.1111/j.1600-0765.1982.tb01178.x PubMedWeb of Science®Google Scholar 16 Bretscher P, Cohn M. A theory of self-nonself discrimination. Science 1970; 169: 1042–1049. 10.1126/science.169.3950.1042 CASPubMedWeb of Science®Google Scholar 17 Moller G. B lymphocyte activation. Immunol Today 1981; 2: 181–184. 10.1016/0167-5699(81)90060-8 PubMedWeb of Science®Google Scholar 18 Rasmussen R, Takatsu K, Harada N, et al. T cell-dependent hapten specific and polyclonal B cell responses require release of interleukin 5. J Immunol 1988; 140: 705–712. CASPubMedWeb of Science®Google Scholar 19 Golay JT. Functional B lymphocyte surface antigens. Immunology 1986; 59: 1–5. PubMedWeb of Science®Google Scholar 20 Klaus GGB, Humphrey JH. A re-evaluation of the role of C3 in B-cell activation. Immunol Today 1986; 7: 163–165. 10.1016/0167-5699(86)90165-9 CASPubMedWeb of Science®Google Scholar 21 Muraguchi A, Kehrl JH, Butler JL, Fauci AS. Regulation of human B-cell activation, proliferation, and differentiation by soluble factors. J Clin Immunol 1984; 4: 337–347. 10.1007/BF00917136 CASPubMedWeb of Science®Google Scholar 22 Clark EA, Ledbetter JA. Amplification of the immuneresponse by agonistic antibodies. Immunol Today 1987; 7: 267–270. 10.1016/0167-5699(86)90008-3 Web of Science®Google Scholar 23 Klaus GGB, Hawrylowicz CM. Cell-cycle control in lymphocyte stimulation. Immunol Today 1984; 5: 15–19. 10.1016/0167-5699(84)90060-4 CASPubMedWeb of Science®Google Scholar 24 Guy GR, Gordon J. Coordinated action of IgE and a Bcell-stimulatory factor on the CD23 receptor molecule upregulates B-lymphocyte growth. Proc Nat Acad Sci USA 1987; 84: 86239–6243. 10.1073/pnas.84.17.6239 Web of Science®Google Scholar 25 Namen AE, Schmierer AE, March CJ, et al. B cell precursor growth-promoting activity. Purification and characterization of a growth factor active on lymphocyte precursors. J Exp Med 1988; 167: 988–1002. 10.1084/jem.167.3.988 CASPubMedWeb of Science®Google Scholar 26 Namen AE, Lupton S, Hjerrild K, et al. Stimulation of B-cell progenitors by cloned murine interleukin-7. Nature 1988; 333: 571–573. 10.1038/333571a0 CASPubMedWeb of Science®Google Scholar 27 Goodwin RG, Lupton S, Schmierer A, et al. Human interleukin 7: Molecular cloning and growth factor activity on human and murine B-lineage cells. Proc Natl Acad Sci USA 1989; 86: 302–306. 10.1073/pnas.86.1.302 CASPubMedWeb of Science®Google Scholar 28 Rabin EM, Ohara J, Paul WE. B-cell stimulatory factor I activates resting B cells. Proc Nat Acad Sci USA 1985; 82: 2935–2939. 10.1073/pnas.82.9.2935 CASPubMedWeb of Science®Google Scholar 29 Melchers F, Lemhardt W. Three restriction points in the cell cycle of activated murine B lymphocytes. Proc Nat Acad Sci USA 1985; 82: 7681–7685. 10.1073/pnas.82.22.7681 CASPubMedWeb of Science®Google Scholar 30 March CJ, Mosley B, Larsen A, et al. Cloning, sequence and expression of two distinct human interleukin-1 complementary DNAs. Nature 1985; 315: 0641–647. 10.1038/315641a0 CASPubMedWeb of Science®Google Scholar 31 Howard M, Mizel SB, Lachman L, Ansel J, Johnson B, Paul WE. Role of interleukin 1 in anti-immunoglobulininduced B cell proliferation. J Exp Med 1983; 157: 1529–1543. 10.1084/jem.157.5.1529 CASPubMedWeb of Science®Google Scholar 32 O'Garra A, Umland S, DeFrance T, Christiansen J. "B-cell factors" are pleiotropic. Immunol Today 1988; 9: 45–54. 10.1016/0167-5699(88)91259-5 CASPubMedWeb of Science®Google Scholar 33 Coffman RL, Schrader B, Carty J, et al. A mouse T cell product that preferentially enhances IgA production I. Biologic characterization. J Immunol 1987; 139: 3685–3690. CASPubMedWeb of Science®Google Scholar 34 Snapper CM, Paul WE. B cell stimulatory factor-1 (interleukin 4) prepares resting murine B cells to secrete IgG1 upon subsequent stimulation with bacterial lipopolysaccharide. J Immunol 1987; 139: 10–17. CASPubMedWeb of Science®Google Scholar 35 Snapper CM, Paul WE. Interferon-γ and B cell stimulatory factor-1 reciprocally regulate Ig isotype production. Science 1987; 236: 944–947. 10.1126/science.3107127 CASPubMedWeb of Science®Google Scholar 36 Finkelman FD, Katona IM, Mosmann TR, Coffman RL. IFN-γ regulates the isotypes of Ig secreted during in vivo humoral immune responses. J Immunol 1988; 140: 1022–1027. CASPubMedWeb of Science®Google Scholar 37 Hirano T, Yasukawa K, Harada H, et al. Complementary DNA for a novel human inlerleukin (BSF-2) thai induces B lymphocytes to produce immunoglobulin. Nature 1986; 324: 073–76. 10.1038/324073a0 CASPubMedGoogle Scholar 38 Poupart P, Vandenabeele P, Cayphas S, et al. B cell growth modulating and differentiating activity of recombinant human 26-Kd protein (BSF-2, HuIFN-β2, HPGF). EMBO J 1987; 6: 1219–1224. 10.1002/j.1460-2075.1987.tb02357.x CASPubMedWeb of Science®Google Scholar 39 Jeske DJ, Capra JD. Immunoglobulins: Structure and function. In: Paul WE, ed. Fundamental immunology. New York : Raven Press. 1984; 131–165. Google Scholar 40 Wakasugi H, Bensimon C, Mahe Y, et al. B-cell-derived interleukin-1. Ann lnst Pasteur/Immunol 1987; 138: 599–603. 10.1016/S0769-2625(87)80129-0 CASWeb of Science®Google Scholar 41 Wakasugi H, Rimsky L, Mahe Y, et al. Epstein-Barr viruscontaining B-cell line produces an interleukin 1 that it uses as a growth factor. Proc Nat Acad Sci USA 1987; 84: 804–808. 10.1073/pnas.84.3.804 CASPubMedWeb of Science®Google Scholar 42 Kurt-Jones EA, Kiely JM, Unanue ER. Conditions required for expression of membrane IL 1 on B cells. J Immunol 1985; 135: 1548–1550. CASPubMedWeb of Science®Google Scholar 43 Mundy GR, Luben RA, Raisz LG, Oppenheim JJ, Buell DN. Bone-resorbing activity in supernatants from lymphoid cell lines. New Eng J Med 1974; 290: 867–871. 10.1056/NEJM197404182901601 CASPubMedWeb of Science®Google Scholar 44 Matsushima K, Kuang YD, Tosato G, Hopkins SJ, Oppenheim JJ. B-cell-derived inlerleukin 1 (IL-1)-like factor; I. Relationship of production of IL-1-like factor to accessory cell function of Epstein-Barr virus-transformed human Blymphoblast lines. Cell Immunol 1984; 94: 406–417. 10.1016/0008-8749(85)90264-3 Web of Science®Google Scholar 45 Matsushima K, Procopio A, Abe H, Scalachre G, Ortaldo JR, Oppenheim JJ. Production of inlerleukin 1 activity by normal human peripheral blood B lymphocytes. J Immunol 1985; 135: 1132–1136. CASPubMedWeb of Science®Google Scholar 46 Matsushima K, Tosato G, Benjamin D, Oppenheim JJ. B-cell-derived interleukin-1 (IL-1)-like factor; II. Sources, effects, and biochemical properties. Cell Immunol 1985; 94: 418–426. 10.1016/0008-8749(85)90265-5 CASPubMedWeb of Science®Google Scholar 47 Mackler BF, Altman LC, Wahl S, Rosenstreich DL, Oppenheim JJ, Mcrgenhagen SE. Blastogenesis and lymphokine synthesis by T and B lymphocytes from patients with periodontat disease. Infect Immun 1974; 10: 844–850. CASPubMedWeb of Science®Google Scholar 48 Dinarello CA, Cannon JG. Interleukin-1. Prog Immunol 1986; VI: 449–457. 10.1016/B978-0-12-174685-8.50047-0 Google Scholar 49 Pistoia V, Cozzolino F, Rubartelli A, Torcia M, Roncella S, Ferrarini M. In vitro production of interleukin 1 by normal and malignant human B lymphocytes. J Immunol 1986; 136: 1688–1692. CASPubMedWeb of Science®Google Scholar 50 Scala G, Kuang YD, Hall RE, et al. Accessory cell function of human B cells. I. Production of both interleukin-1-like activity and an interleukin 1 inhibitory factor by an EBV-transformed human B cell line. J Exp Med 1984; 159: 1637–1652. 10.1084/jem.159.6.1637 CASPubMedWeb of Science®Google Scholar 51 Scala G, Morrone G, Tamburrini M, Alfinito F, Pastore CI, ĎAllesio G, Venuta S. Autocrine growth function of human interleukin 1 molecules on ROHA-9, an EBV-transformed human B cell line. J Immunol 1987; 138: 2527–2534. CASPubMedWeb of Science®Google Scholar 52 Acres RB, Larsen A, Gillis S, Conlon PJ. Production of IL-1α and IL-1β by clones of EBV transformed, human B cells. Mol Immunol 1987; 24: 479–485. 10.1016/0161-5890(87)90022-8 CASPubMedWeb of Science®Google Scholar 53 Taira S, Matsui M, Hayakawa K, Yokoyama T, Nariuchi H. Interleukin secretion by B cell lines and splenic B cells stimulated with calcium ionophore and phorbol ester. J. Immunol 1987; 139: 2957–2964. CASPubMedWeb of Science®Google Scholar 54 Benjamin D, Hartmann DP, Bazar LS, Jacobson RJ. Burkitt's cells can be triggered by teleocidin to secrete interferon-γ. Am J Hematol 1986; 22: 169–177. 10.1002/ajh.2830220207 CASPubMedWeb of Science®Google Scholar 55 Benjamin D, Bazar LS, Wallace B, Jacobson RJ. Heterogeneity of B-cell growth factor receptor reactivity in healthy donors and in patients with chronic lymphatic leukemia: Relationship to B-cell-derived lymphokines. Cellular Immunol 1986; 103: 394–408. 10.1016/0008-8749(86)90099-7 CASPubMedWeb of Science®Google Scholar 56 Clark-Lewis I, Schrader JW, Wu Y, Harris AW. A B lymphoma cell line produces growth factors for hemopoietic, lymphoid, and mast cells. Cellular Immunol 1982; 69: 196–200. 10.1016/0008-8749(82)90064-8 CASPubMedWeb of Science®Google Scholar 57 Jurgensen CH, Ambrus JL Jr, Fauci AS. Production of B-cell growth factor by normal human B cells. J Immunol 1986; 136: 4542–4547. CASPubMedWeb of Science®Google Scholar 58 Swendeman S, Thorley-Lawson DA. The activation antigen BLAST-2, when shed, is an autocrine BCGF for normal and transformed B cells. EMBO J 1987; 6: 1637–1642. 10.1002/j.1460-2075.1987.tb02412.x CASPubMedWeb of Science®Google Scholar 59 Kang H, Koyasu S, Takei M, et al. Characterization of a B cell-derived growth-enhancing factor produced by a human B cell line established from a patient with rheumatoid arthritis. J Immunol 1987; 139: 1154–1160. CASPubMedWeb of Science®Google Scholar 60 Sherr DH, Dorf ME. Gibson M, Sidman CL. Ly-1 Bhelper cells in autoimmune "variable motheaten" mice. J Immunol 1987; 139: 1811–1817. CASPubMedWeb of Science®Google Scholar 61 Pelton BK, Denman AM. Spontaneous production of B-cell growth factors by SLE lymphocytes. Clin Exp Immunol 1987; 67: 159–166. CASPubMedWeb of Science®Google Scholar 62 Ambrus JL Jr, Fauci AS. Human B lymphoma cell line producing B cell growth factor. J Clin Invest 1985; 75: 732–739. 10.1172/JCI111754 CASPubMedWeb of Science®Google Scholar 63 Nakajima K, Hirano T, Takalsuki F, Sakaguchi N, Yoshida N, Kishimoto T. Physiochemical and functional properties of murine B cell-derived B cell growth factor II (WEHI-231-BCGF-II). J Immunol 1985; 135: 1207–1212. CASPubMedWeb of Science®Google Scholar 64 Gordon J, Guy GR. The molecules controlling B lymphocytes. Immunol Today 1987; 8: 339–344. 10.1016/0167-5699(87)90009-0 CASPubMedWeb of Science®Google Scholar 65 Gordon J, Ley SC, Melamed MD, English LS, Hughes-Jones NC. Immortalized B lymphocytes produce B-cell growth factor. Nature 1984; 310: 145–147. 10.1038/310145a0 CASPubMedWeb of Science®Google Scholar 66 Pisko EJ, Foster SL, White RE, Panetti M, Turner RA. Suppression of a pokeweed mitogen-stimulated plaqueforming cell response by a human B lymphocyte-derived aggregated IgG-stimulated suppressor factor: suppressive B cell factor (SBF). J Immunol 1986; 136: 2141–2150. CASPubMedWeb of Science®Google Scholar 67 Ohno T, Miyama-Inaba M, Masuda T, et al. Inhibitory mechanism of the proliferative responses of resting B cells: Feedback regulation by a lymphokine (suppressive B-cell factor) produced by Fc receptor-stimulated B cells. Immunology 1987; 61: 35–41. CASPubMedWeb of Science®Google Scholar 68 Kuribayasbi K, Katayama H, Nishihara T, Saito K. Regulatory action of immune B cells on deiayed-type hypersensitivity in mice. Cell Immunol 1987; 108: 366–377. 10.1016/0008-8749(87)90220-6 PubMedWeb of Science®Google Scholar 69 White RE, Pisko EJ, Foster SL, Panetti M, Turner RA. Decreased suppressive B cell factor (SBF) in rheumatoid arthritis: Evidence for a defect in B cell autoregulalion. J Immunol 1986; 136: 2151–2157. CASPubMedWeb of Science®Google Scholar 70 Garrett IR, Durie GM, Nedwin GE et al. Production of lymphotoxin, a bone-resorbing cytokine, by cultured human myeloma cells. Nes Engl J Med 1987; 317: 526–532. 10.1056/NEJM198708273170902 CASPubMedWeb of Science®Google Scholar 71 Rasanen L, Karhumaki E, Arvilommi H. Bacleria induce lymphokine synthesis polyclonally in human B lympocytes. J Immunol 1978; 121: 418–420. CASPubMedWeb of Science®Google Scholar 72 Sung S-SJ, Jung LK-L, Walters JA, Chen W, Wang CY, Fu SM. Production of tumor necrosis factor acachectin by human B lymphocytes. FASEB J 1988; 2: A900 (abstract). Web of Science®Google Scholar 73 Rabinovitch PS, Torres RM, Engel D. Simultaneous cell cycle analysis and two-color surface immunofluorescence using 7-amino-actinomycin D and single laser excitation: Applications to study cell activation and the cell cycle of murine Ly-1 B cells. J Immunol 1986; 136: 2769–2775. CASPubMedWeb of Science®Google Scholar 74 Dewhirst FE, Stashenko PP, Mole JE, Tsurumachi T. Purification and partial sequence of human osteoclast-activaling factor: identity with interleukin 1 beta. J Immunol 1985; 135: 2562–2568. CASPubMedWeb of Science®Google Scholar 75 Horton JE, Oppenheim JJ, Mergenhagen SE, Raisz LG. Macrophage-lymphocyle synergy in the production of osteoclast activating factor. J Immunol 1974; 113: 1278–1287. CASPubMedWeb of Science®Google Scholar 76 Chen P, Trummel C, Horton J, Baker JJ, Oppenheim JJ. Production of osteoclast-activating factor by normal peripheral blood rosetting and nonrosetting lymphocytes. Eur J Immunol 1976; 6: 732–736. 10.1002/eji.1830061014 CASPubMedWeb of Science®Google Scholar 77 Yoneda T, Mundy GR. Monocytes regulate osteoclastactivating factor production by releasing prostaglandins. J Exp Med 1979; 150: 338–350. 10.1084/jem.150.2.338 CASPubMedWeb of Science®Google Scholar 78 Hanazawa S, Nakada K, Ohmori Y, Miyoshi T, Amano A, Kitano S. Functional role of interleukin 1 in periodontal disease: Induction of interleukin 1 production by Bacteroides gingivalis lipopolysaccharide in peritoneal macrophages from C3H/HeN and C3H/HeJ mice. Infect Immun 1985; 50: 262–270. 10.1128/iai.50.1.262-270.1985 CASPubMedWeb of Science®Google Scholar 79 Lindemann RA, Economou JS. Rothermel H. Production of interleukin-1 and tumor necrosis factor by human peripheral monocytes activated by periodontal bacteria and extracted lipopolysaccharides. J Dent Res 1988; 67: 1131–1135. 10.1177/00220345880670081401 CASPubMedWeb of Science®Google Scholar 80 Chesnut R, Grey HM. Antigen presentation by B cells and its significance in T-B reactions. Adv Immunol 1986; 39: 51–94. 10.1016/S0065-2776(08)60348-X PubMedWeb of Science®Google Scholar 81 Moticka EJ. Polyclonal hyperimmunoglobulinemia (pHIg): A vestige of primeval immunity Dev Comp Immunol 1978; 2: 109–120. 10.1016/S0145-305X(78)80030-5 CASPubMedWeb of Science®Google Scholar 82 Moticka EJ, Streilein JW. Hypothesis: Nonspecific polyclonal activation of memory B cells by antigen as a mechanism for the preservation of long term immunologic anamnesis. Cell Immunol 1978; 41: 406–413. 10.1016/0008-8749(78)90237-X CASPubMedWeb of Science®Google Scholar 83 Clagett JA, Engel D. Polyclonal activation: A form of primitive immunity and its possible role in pathogenesis of inflammatory diseases. Dev Comp Immunol 1978; 2: 235–242. 10.1016/S0145-305X(78)80066-4 CASPubMedWeb of Science®Google Scholar 84 Finger H, Wirsing von Konig CH. Enhancement and suppression of immune responsiveness by bacteria, bacterial products and extracts. In: W Zschiesche, ed. Immune Modulation by Infectious Agents. Jena : Verlag, 1987; pp. 16–113. Google Scholar 85 Lopatin DE, Mangan DF, Horner IS, Peebles FL. Mitogen-induced amplification of blastogenesis in lipopolysaccharide-precultured lymphocytes. Infect Immun 1980; 29: 512–519. PubMedWeb of Science®Google Scholar 86 Lopatin DE, Mangan DF, Homer IS. Cells involved in the mitogen-induced helper function which facilitates the blastogenic response to Actinomyces viscosus. Clin Immunol Immunopathol 1981; 19: 394–405. 10.1016/0090-1229(81)90082-9 CASPubMedWeb of Science®Google Scholar 87 Tew JG, Thomas SS, Ranney RR. Fusobacterium nucleatwn-mediated immunomodulation of the in vitro secondary antigen response to tetanus toxoid and Actinobacillus actinomycetemcomitans. J Periodont Res 1987; 22: 506–512. 10.1111/j.1600-0765.1987.tb02062.x CASPubMedWeb of Science®Google Scholar 88 Page RC, Schroeder HE. Pathogenesis of inflammatory periodontal disease. Lab Invest 1976; 34: 235–249. CASPubMedWeb of Science®Google Scholar 89 Seymour GJ, Powell RN, Davies WIR. Conversion of a stable T cell lesion to a progressive B cell lesion in the pathogenesis of chronic inflammatory periodontal disease: an hypothesis. J Clin Periodontol 1979; 6: 267–277. 10.1111/j.1600-051X.1979.tb01930.x PubMedWeb of Science®Google Scholar 90 Passo SM, Reinhardt RA, DuBois LM, Cohen DM. Histological characteristics associated with suppurating periodontal pockets. J Periodontol 1988; 59: 731–740. 10.1902/jop.1988.59.11.731 PubMedWeb of Science®Google Scholar 91 Ivanyi L, Lehner T. Stimulation of human lymphocytes by B cell mitogens. Clin Exp Immunol 1974; 18: 347–356. CASPubMedWeb of Science®Google Scholar 92 Ivanyi L. The mitogenicity of dcxtrans for B lymphocytes in man. Clin Immunol Immunopathol 1977; 7: 123–129. 10.1016/0090-1229(77)90036-8 CASPubMedWeb of Science®Google Scholar 93 Ranney RR, Ruddy S, Tew JG, Welshimer H, Paicanis KG, Segreti A. Immunologic studies of young adults with severe periodontitis I. Medical evaluation and humoral factors. J Peridont Res 1981; 16: 390–402. 10.1111/j.1600-0765.1981.tb00990.x PubMedWeb of Science®Google Scholar 94 Tew JG, Miller GA, Greene EJ, et al. Immunological studies of young adults with severe periodontitis. II. Cellular factors. J Periodont Res 1981; 16: 403–516. 10.1111/j.1600-0765.1981.tb00991.x CASPubMedWeb of Science®Google Scholar 95 Engel D, Monzingo S, Rabinovitch P, Clagett J, Stone R. Mitogen-induced hyperproliferation response of peripheral blood mononuclear cells from patients with severe generalized periodontitis: Lack of correlation with proportions of T cells and T cell subsets. Clin Immunol Immunopathol 1984; 30: 374–386. 10.1016/0090-1229(84)90023-0 PubMedWeb of Science®Google Scholar 96 Suzuki JB, Falkler WA. Immunologic profile of juvenile periodontitis I. Lymphocyte blastogenesis and the autologous mixed lymphocyte response. J Periodontol 1984; 55: 453–460. 10.1902/jop.1984.55.8.453 PubMedWeb of Science®Google Scholar 97 Tew JG, Burmeister JA, Paicanis KG, Ranney RR. Spontaneous lymphocyte proliferation and periodontal status of young adults. J Periodont Res 1983; 18: 534–540. 10.1111/j.1600-0765.1983.tb00390.x CASPubMedWeb of Science®Google Scholar 98 McAnulty K, Stone R, Hastings G, Clagett J, Engel D. Immunoregulation in severe generalized periodontitis. Clin Immunol Immunopathol 1985; 34: 84–93. 10.1016/0090-1229(85)90010-8 PubMedWeb of Science®Google Scholar 99 Long JC, Nance WE, Waring P, Burmeister JA, Ranney RR. Early onset periodontitis: A comparison and evaluation of two proposed modes of inheritance. Genet Epi 1987; 4: 13–24. 10.1002/gepi.1370040103 PubMedGoogle Scholar 100 Boughman JA, Beaty TH, Yang P, Goodman SB, Wooten RK, Suzuki JB. Problems of genetic model testing in early onset periodontitis. J Periodontol 1988; 59: 332–337. 10.1902/jop.1988.59.5.332 PubMedWeb of Science®Google Scholar 101 Engel D, Clark EA, Held L, Kimball H, Clagett J. Immune responsiveness of SM/J mice. Cellular characteristics and genetic analysis of hyperresponsiveness to B cell mitogens. J Exp Med 1981; 154: 726–736. 10.1084/jem.154.3.726 CASPubMedWeb of Science®Google Scholar 102 Stone R, Engel D. Genetic control of mitogen-induced B cell hyperproliferation in SM/J mice. Immunogenetics 1985; 22: 69–75. 10.1007/BF00430595 CASPubMedWeb of Science®Google Scholar 103 Yoshie H, Taubman MA, Ebersole JL, Smith DJ, Olson CL. Periodontal bone loss and immune characteristics of congenitally athymic and thymus cell-reconstituted athymic rats. Infect Immun 1985; 50: 403–408. 10.1128/IAI.50.2.403-408.1985 CASPubMedWeb of Science®Google Scholar 104 Mallison SM, Szakal AK, Ranney RR, Tew JG. Antibody synthesis specific for nonoral antigens in inflamed gingiva. Infect Immuno 1988; 55: 823–830. Google Scholar 105 Brandtzaeg P, Tolo K. Immunoglobulin systems of the gingivae. In: T Lehner, ed. The borderland between caries and periodontal disease. London : Academic Press, 1977; 145–183. Google Scholar 106 Bergland SE. Immunoglobulins in human gingiva with specificity for oral bacteria. J Periodontol 1971; 42: 546–551. 10.1902/jop.1971.42.9.546 PubMedWeb of Science®Google Scholar 107 Ebersole JL, Taubman MA, Smith DJ, Goodson JM. Gingival crevicular fluid antibody to oral microorganism I. Method of collection and analysis of antibody. J Periodont Res 1984; 19: 124–132. 10.1111/j.1600-0765.1984.tb00801.x PubMedWeb of Science®Google Scholar 108 Tew JG, Marshall DR, Burmeister JA, Ranney RR. Relationship between gingival crevicular fluid and serum antibody titers in young adults with generalized and localized periodontitis. Infect Immun 1985; 49: 487–493. PubMedWeb of Science®Google Scholar 109 Ebersole JL, Holt SC. Serum antibodies to periodontopathic microorganisms: Specific induction. In: B Guggenheim, ed. Periodontology Today, International Congress, Zurich 1988; pp. 169–177. Basel : S. Karger, 1988. Google Scholar 110 Mallison SM, Kaugars C, Szakal AK, Schenkein HA, Tew JG. Synthesis of antibody specific for nonoral antigen in the gingiva of periodontitis patients. J Periodont Res 1989 (in press). Google Scholar 111 Peters M, Fauci AS. Selective activation of antigen-specific human B cells in recently immunized individuals by nonspecific factors in the absence of antigen. J Immunol 1983; 130: 678–680. CASPubMedWeb of Science®Google Scholar 112 Donaldson SL, Ranney RR, Tew JG. Evidence of mitogenic activity in periodontitis-associated bacteria. Infect Immun 1983; 42: 487–495. 10.1128/IAI.42.2.487-495.1983 CASPubMedWeb of Science®Google Scholar 113 Carpenter AB, Sully EC, Ranney RR, Bick PH. T cell regulation of polyclonal B cell activation induced by extracts of oral bacteria associated with periodontal diseases. Infect Immun 1984; 43: