Mechanisms of alveolar bone destruction in periodontitis

Periodontology 2000

Volumn 14, Issue 1, 1997, Pages 158-172

  Schwartz, Zvi ^a   Goultschin, Josef ^a   Dean, David D ^a   Boyan, Barbara D ^a  

^a NONE

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; GROWTH PROMOTOR; PROSTAGLANDIN;

BONE REMODELING; HUMAN; JAW; METABOLISM; OSTEOBLAST; OSTEOCLAST; OSTEOLYSIS; PATHOPHYSIOLOGY; PERIODONTITIS; PHYSIOLOGY; REVIEW;

ALVEOLAR BONE LOSS; ALVEOLAR PROCESS; BONE REMODELING; CYTOKINES; GROWTH SUBSTANCES; HUMANS; OSTEOBLASTS; OSTEOCLASTS; PERIODONTITIS; PROSTAGLANDINS;

EID: 0031152178     PISSN: 09066713     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1600-0757.1997.tb00196.x     Document Type: Article

References (149)

1. Akatsu T, Takahashi N, Udagawa N, Imamura K, Yamaguchi A, Sato K, Nagata N, Suda T. Role of prostaglandins in interleukin-1-induced bone resorption in mice in vitro. J Bone Miner Res 1991: 6: 183-190.
2. Albers HK, Loning T, Lisboa BP. Biochemische und morphologische Untersuchungen über die Prostaglandine E und F der normalen und entzündlich veranderten Gingiva. Dtsch Zahn Z 1979: 34: 440-443.
3. Alexander P, Evans R. Endotoxin and double stranded RNA render macrophages cytotoxic. Nature New Biol 1971: 232: 76-78.
4. Bellido T, Jilka RL, Boyce BF, Girasole G, Broxmeyer H, Dalrymple SA, Murray R, Manolagas SC. Regulation of interleukin-6, osteoclastogenesis, and bone mass by androgens. The role of the androgen receptor. J Clin Invest 1995: 95: 2886-2895.
5. Bertolini DR, Nedwin GE, Bringman TS, Smith DD, Mundy GR. Stimulation of bone resorption and inhibition of bone formation in vitro by human tumour necrosis factors. Nature 1986: 319: 516-518.
6. 2 release and does not correlate with the extent of bone resorption. Cytokine 1994: 6: 368-375.
7. Bonewald LF. Transforming growth factor-beta. In: Bilezikian JP, Raisz LG, Rodan GA, ed. Principles of bone biology. San Diego: Academic Press, 1996: 647-659.
8. 3 on differentiation of a human osteosarcoma (MG-63). J Biol Chem 1992: 267: 8943-8949.
9. Bonewald LF, Schwartz Z, Swain LD, Ramirez V, Poser J, Boyan BD. Stimulation of plasma membrane and matrix vesicle enzyme activity by transforming growth factor-β in osteosarcoma cell cultures. J Cell Physiol 1990: 145: 200-206.
10. Broulik P, Kragstrup J, Mosekilde L, Melsen F. Osteon cross-sectional size in the iliac crest: variation in normals and patients with osteoporosis, hyperparathyroidism, acromegaly, hypothyroidism and treated epilepsia. APMIS 1982: 90: 339-344.
11. Burgess WH, Maciag TL. The heparin-binding (fibroblast) growth factor family of proteins. Annu Rev Biochem 1989: 58: 575-606.
12. Canalis E. Interleukin-1 has independent effects on deoxyribonucleic acid and collagen synthesis in cultures of rat calvariae. Endocrinology 1986: 118: 74-81.
13. Canalis E, McCarthy TL, Centrella M. Isolation and characterization of insulin-like growth factor I (somatomedin C) from cultures of fetal rat calvariae. Endocrinology 1988: 122: 22-27.
14. Canalis E, McCarthy TL, Centrella M. Effects of plateletderived growth factor on bone formation in vitro. J Cell Physiol 1989: 140: 530-537.
15. Canalis E, Rydziel S. Platelet-derived growth factor and the skeleton. In: Bilezikian JP, Raisz LG, Rodan GA, ed. Principles of bone biology. San Diego: Academic Press, 1996: 619-626.
16. Canalis E, Varghese S, McCarthy TL, Centrella M. Role of platelet derived growth factor in bone cell function. Growth Regul 1992: 2: 151-155.
17. Carranza FA Jr, Saglie R, Newman MG, Valentin PL. Scanning and transmission electron microscopic study of tissue-invading microorganisms in localized juvenile periodontitis. J Periodontol 1983: 54: 598-617.
18. Centrella M, McCarthy TL, Canalis E. Receptors for insulin-like growth factors I and II in osteoblast-enriched cultures from fetal rat bone. Endocrinology 1990: 126: 39-44.
19. Centrella M, McCarthy TL, Canalis E. Relative effects of hetero- and homodimeric isoforms of platelet-derived growth factor in fetal rat bone cells. In: Cohn DV, Glorieux FH, Martin TJ, ed. Calcium regulation and bone metabolism. 10. Basic and clinical aspects. Amsterdam: Elsevier, 1990: 324-329.
20. Centrella M, McCarthy TL, Canalis E. Glucocorticoid control of transforming growth factor β(TGFβ) binding and effects in osteoblast-enriched cultures from fetal rat bone. J Bone Miner Res 1990: 5(suppl 2): S211 (abstr).
21. Centrella M, McCarthy TL, Canalis E. Glucocorticoid regulation of transforming growth factor beta 1 activity and binding in osteoblast-enriched cultures from fetal rat bone. Mol Cell Biol 1991: 11: 4490-4496.
22. Centrella M, McCarthy TL, Kusmik WF, Canalis E. Isoform-specific regulation of platelet-derived growth factor activity and binding in osteoblast-enriched cultures from fetal rat bone. J Clin Invest 1992: 89: 1076-1084.
23. Centrella M, McCarthy TL, Ladd C, Canalis E. Expression of platelet-derived growth factor (PDGF) and regulation of PDGF binding are both isoform specific in osteoblast-enriched cultures from fetal rat bone. J Bone Miner Res 1990: 5(suppl 2): S86 (abstr).
24. 47calcium kinetic study and dynamic histomophometry. Metab Clin Exp 1987: 36: 1118-1124.
25. Charon JA, Luger TA, Mergenhagen SE, Oppenheim JJ. Increased thymocyte-activating factor in human gingival fluid during gingival inflammation. Infect Immun 1982: 38: 1190-1195.
26. Chen R-H, Derynck R. Homomeric interactions between type II transforming growth factor-β receptors. J Biol Chem 1994: 269: 22868-22874.
27. Chen R-H, Moses HL, Maruoka EM, Derynck R, Kawabata M. Phosphorylation-dependent interaction of the cytoplasmic domains of the type I and type II transforming growth factor-β receptors. J Biol Chem 1995: 270: 12235-12241.
28. Chole RA, Faddis BT, Tinling SP. In vivo inhibition of localized bone resorption by human recombinant interleukin-1 receptor antagonist. J Bone Miner Res 1995: 10: 281-284.
29. Christersson LA, Albini B, Zambon JJ, Wikesjö UM, Genco RJ. Tissue localization of Actinobacillus actinomycetemcomitans in human periodontitis. I. Light, immunofluorescence and electron microscopic studies. J Periodontol 1987: 58: 529-539.
30. 2. Prostaglandins 1984: 27: 97-103.
31. Coupron P, Meunier P, Bressot C, Giroux JM. Amount of bone iliac crest biopsy. Significance of the trabecular bone volume. Its value in normal and in pathological conditions. In: Meuiner PJ, ed. Bone histomorphometry. Paris: Armour Montagu, 1977: 39-47.
32. 2 potentiates interleukin-1β induced interleukin-6 production by human gingival fibroblasts. J Clin Periodontol 1996: 23: 635-640.
33. Dean DD, Arsenis CH, Muniz OE, Howell DS. Vitamin D metabolites regulate interleukin-1α and β levels in rat growth plate cartilage. J Bone Miner Res 1994: 9: S375 (abstr).
34. Deporter DA, Brown DY. Fine structural observations on the mechanism of loss of attachment during experimental periodontal disease in the rat. J Periodont Res 1980: 15: 304-313.
35. Dewhirst FE, Ago JM, Peros WJ, Stashenko P. Synergism between parathyroid hormone and interleukin-1 in stimulating bone resorption in organ culture. J Bone Miner Res 1987: 2: 127-134.
36. 2, thromboxane, and prostacyclin in periodontal tissue. J Periodont Res 1983: 18: 156-163.
37. El Attar TMA, Lin HS. Prostaglandins in gingiva of patients with periodontal disease. J Periodontol 1981: 52: 16-19.
38. Ellison SA. Oral bacteria and periodontal disease. J Dent Res 1970: 49: 198-202.
39. Ericksen EF, Mosekilde L, Melsen F. Trabecular bone remodeling and balance in primary hyperparathyroidism. Bone 1986: 7: 213-221.
40. Feldman RS, Szeto B, Chauncey HH, Goldhaber P. Nonsteroidal anti-inflammatory drugs in the reduction of alveolar bone loss. J Clin Periodontol 1983: 10: 131-136.
41. Felix R, Cecchini MG, Fleisch H. Macrophage colony stimulating factor restores in vivo bone resorption in the op/op osteopetrotic mouse. Endocrinology 1990: 127: 2592-2594.
42. Finkelstein JS, Mibanski A, Neer RM, Doppelt SH, Rosenthal DI, Segre GV, Growley WF Jr. Increases in bone density during treatment of men with idiopathic hypogonadotropic hypogonadism. J Clin Endocrinol Metab 1989: 69: 776-783.
43. Foresta C, Ruzza G, Mioni R, Guarneri G, Gribaldo R, Meneghello A, Matrogiacomo I. Osteoporosis and decline of gonadal function in the elderly male. Hormone Res 1984: 19: 18-22.
44. Franzen P, Heldin CH, Miyazono K. The GS domain of the transforming growth factor-β type I receptor is important in signal transduction. Biochem Biophys Res Commun 1995: 207: 682-689.
45. Fried RM, Voelkel EF, Rice RH, Levine L, Gaffney EV, Tashjian AH. Two squamous cell carcinomas not associated with humoral hypercalcemia produce a potent bone resorption-stimulating factor which is interleukin-1 alpha. Endocrinology 1989: 125: 742-751.
46. Frost HM. Dynamics of bone remodeling. In: Frost HM, ed. Bone biodynamics. Boston: Little Brown, 1964: 315-333.
47. Fujihashi K, Beagley KW, Kono Y, Aicher WK, Yamamoto M, DiFabio S, Xu-Amano J, McGhee JR, Kiyono H. Gingival mononuclear cells from chronic inflammatory periodontal tissues produce interleukin (IL)-5 and IL-6 but not IL-2 and IL-4. Am J Pathol 1993: 142: 1239-1250.
48. Gallwitz WE, Mundy GR, Lee CH, Qiao M, Roodman GD, Raftery M, Gaskell SJ, Bonewald LF. 5-Lipoxygenase metabolites of arachidonic acid stimulate isolated osteoclasts to resorb calcified matrices. J Biol Chem 1993: 268: 10087-10094.
49. Gemmell E, Seymour GJ. Interleukin 1, interleukin 6 and transforming growth factor-beta production by human gingival mononuclear cells following stimulation with Porphyromonas gingivalis and Fusobacterium nucleatum. J Periodont Res 1993: 28: 122-129.
50. Genco RJ, Evans RT, Ellison SA. Dental research in microbiology with emphasis on periodontal disease. J Am Dent Assoc 1969: 78: 1016-1036.
51. Gillett R, Johnson NW. Bacterial invasion of the periodontium in a case of juvenile periodontitis. J Clin Periodontol 1982: 9: 93-100.
52. Globus RK, Plouet J, Gospodarowicz D. Cultured bovine bone cells synthesize basic fibrpblast growth factor and store it in their extracellular matrix. Endocrinology 1989: 124: 1539-1547.
53. 2 levels and human periodontal disease. Prostaglandins 1974: 6: 81-85.
54. Gowen M, Chapman K, Littlewood A, Hughes D, Evans D, Russell G. Production of tumor necrosis factor by human osteoblasts is modulated by other cytokines, but not by osteotropic hormones. Endocrinology 1990: 126: 1250-1255.
55. Gowen M, Meikle MC, Reynolds JJ. Stimulation of bone resorption in vitro by a nonprostanoid factor released by human monocytes in culture. Biochim Biophys Acta 1983: 762: 471-474.
56. Graves DT, Valetin-Opran A, Delgado R, Valente AJ, Mundy GR, Piche J. The potential role of platelet-derived growth factor as an autocrine or paracine factor for human bone cells. Connect Tissue Res 1989: 23: 209-218.
57. 3H/HeJ mice. Infect Immun 1985: 50: 262-270.
58. Heldin CH, Westermark B. PDGF-like growth factors in autocrine stimulation of growth. J Cell Physiol 1987: 5(suppl): 31-34.
59. Heldin CH, Westermark B. Platelet-derived growth factors: a family of isoforms that bind to two distinct receptors. Br Med Bull 1989: 45: 453-164.
60. Hock JM, Canalis E. Platelet-derived growth factor enhances bone cell replication, but not differentiated function of osteoblasts. Endocrinology 1994: 134: 1423-1428.
61. Hock JM, Canalis E, Centrella M. Transforming growth factor beta (TGF-beta 1) stimulates bone matrix apposition and bone cell replication in cultured fetal rat calvariae. Endocrinology 1990: 126: 421-426.
62. Hock JM, Centrella M, Canalis E. Insulin-like growth factor I has independent effects on bone matrix formation and cell replication. Endocrinology 1988: 122: 254-260.
63. 2 levels. J Periodont Res 1977: 12: 500-509.
64. Howell TH, Fiorellini JP, Weber HP, Williams RC. Effect of the NSAID piroxicam, topically administered, on the development of gingivitis in beagle dogs. J Periodont Res 1991: 26: 180-183.
65. Hurley MM, Florkiewicz RZ. Fibroblast growth factor and vascular endothelial cell growth factor families. In: Bilezikian JP, Raisz LG, Rodan GA, ed. Principles of bone biology. San Diego: Academic Press, 1996: 627-645.
66. Jandinski JJ, Stashenko P, Feder LS, Leung CC, Peros WJ, Rynar JE, Deasy MJ. Localization of interleukin-1β in human periodontal tissue. J Periodontol 1991: 62: 36-43.
67. 2. Bone 1987: 8: 171-178.
68. Jeffcoat MK, Page R, Reddy M, Wannawisute A, Waite P, Palcanis K, Cogen R, Williams RC, Basch C. Use of digital radiography to demonstrate the potential of naproxen as an adjunct in the treatment of rapidly progressive periodontitis. J Periodont Res 1991: 26: 415-121.
69. Jeffcoat MK, Reddy MS, Haigh S, Buchanan W, Doyle MJ, Meredith MP, Nelson SL, Goodale MB, Wehmeyer KR. A comparison of topical ketorolac, systemic flurbiprofen, and placebo for the inhibition of bone loss in adult periodontitis. J Periodontol 1995: 66: 329-338.
70. Joyce ME, Jingushi S, Bolander ME. Transforming growth factor-β in the regulation of fracture repair. Orthop Clin North Am 1990: 21: 199-209.
71. Kornman KS, Blodgett RF, Brunsvold M, Holt SC. Effects of topical applications of meclofenamic acid and ibuprofen on bone loss, subgingival microbiota and gingival PMN response in the primate Macaca fascicularis. J Periodont Res 1990: 25: 300-307.
72. Kumegawa M, Hiramatsu M, Hatakeyama K, Yajima T, Kodama H, Osaki T, Kurisu K. Effects of epidermal growth factor on osteoblastic cells in vitro. Calcif Tissue Int 1983: 35: 542-548.
73. Laiho M, Weis FM, Boyd FT, Ignotz RA, Massague J. Responsiveness to transforming growth factor-beta (TGF-beta) restored by genetic complementation between cells defective in TGF-beta receptors I and II. J Biol Chem 1991: 266: 9108-9112.
74. Laiho M, Weis MB, Massague J. Concomitant loss of transforming growth factor (TGF)-beta receptor types I and II in TGF-beta-resistant cell mutants implicates both receptor types in signal transduction. J Biol Chem 1990: 265: 18518-18524.
75. 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.
76. Longhurst P, Gillett R, Johnson NW. Electron microscope quantitation of inflammatory infiltrates in childhood gingivitis. J Periodont Res 1980: 15: 255-266.
77. Lopez-Casillas F, Cheifetz S, Doody J, Andres JL, Lane WS, Massague J. Structure and expression of the membrane proteoglycan betaglycan, a component of the TGF-beta receptor system. Cell 1991: 67: 785-795.
78. Lopez-Casillas F, Wrana JL, Massague J. Betaglycan presents ligand to the TGFβ signaling receptor. Cell 1993: 73: 1435-1444.
79. Lorenzo JA, Sousa SL, Alander C, Raisz LG, Dinarello CA. Comparison of the bone-resorbing activity in the supernatants from phytohemagglutinin in stimulated human peripheral blood mononuclear cells with that of cytokines through the use of an antiserum to interleukin 1. Endocrinology 1987: 121: 1164-1170.
80. Lowik CW, van der Pluijm G, Bloys H, Hoekman K, Bijvoet OL, Aarden LA, Papapoulos SE. Parathyroid hormone (PTH) and PTH-like protein (PLP) stimulate interleukin-6 production by osteogenic cells - a possible role of interleukin-6 in osteoclastogenesis. Biochem Biophys Res Commun 1989: 162: 1546-1552.
81. Lundqvist C, Baranov V, Teglund S, Hammarstrom S, Hammarstrom ML. Cytokine profile and ultrastructure of intraepithelial gamma delta T cells in chronically inflamed human gingiva suggest a cytotoxic effector function. J Immunol 1994: 153: 2302-2312.
82. Mann GN, Jacobs TW, Buchinsky FJ, Armstrong EC, Li M, Ke HZ, Ma YF, Jee WS, Epstein S. Interferon-gamma causes loss of bone volume in vivo and fails to ameliorate cyclosporin A-induced osteopenia. Endocrinology 1994: 135: 1077-1083.
83. Marks SC Jr, Hermey DC. The structure and development of bone. In: Bilezikian JP, Raisz LG, Rodan GA, ed. Principles of bone biology. San Diego: Academic Press, 1996: 3-14.
84. Marks SC Jr, Popoff SN. Bone cell biology: The regulation of development, structure, and function in the skeleton. Am J Anat 1988: 183: 1-14.
85. Martin TJ, Ng KW. Mechanisms by which cells of the osteoblast lineage control osteoclast formation and activity. J Cell Biochem 1994: 56: 357-366.
86. Masada MP. Persson R, Kenney JS, Lee SW, Page RC, Allison AC. Measurement of interleukin-1-alpha and 1-beta in gingival crevicular fluid: implications for the pathogenesis of periodontal disease. J Periodont Res 1990: 25: 156-163.
87. Matsuki Y, Yamamoto T, Hara K. Localization of interleukin-1 (IL-1) mRNA-expressing macrophages in human inflamed gingiva and IL-1 activity in gingival crevicular fluid. J Periodont Res 1993: 28: 35-12.
88. McCarthy TL, Centrella M, Canalis E. Cyclic AMP induces insulin-like growth factor I synthesis in osteoblast-enriched cultures. J Biol Chem 1990: 265: 15353-15356.
89. McKee MD, Farach-Carson MC, Butler WT, Hauschka PV, Nanci A. Ultrastructural immunolocalization of noncollagenous (osteopontin and osteocalcin) plasma (albumin and alpha 2HS-glycoprotein) proteins in rat bone. J Bone Miner Res 1993: 8: 485-496.
90. Melsen F, Mosekilde L. Tetracycline double-labeling of iliac trabecular bone in 41 normal adults. Calcif Tissue Res 1978: 26: 99-102.
91. Mergenhagen S. Thermocyte activating factor(s) in human gingival fluids. J Dent Res 1984: 63: 461-464.
92. Metcalf D, Begley CG, Williamson DJ, Nice EC, De Lamarter J, Mermod JJ, Thatcher D, Schmidt A. Hematopoietic response in mice injected with purified recombinant murine GM-CSF. Exp Hematol 1987: 15: 1-9.
93. Mizuno Y, Hosoi T, Inoue S, Ikegami A, Kaneki M, Akedo Y, Nakamura T, Ouchi Y, Chang C, Orimo H. Immunocytochemical identification of androgen receptor in mouse osteoclast-like multinucleated cells. Calcif Tissue Int 1994: 54: 325-326.
94. Morrissey PJ, Bressler L, Charrier K, Alpert A. Response of resident murine peritoneal macrophages to in vivo administration of granulocyte-macrophage colony-stimulating factor. J Immunol 1988: 140: 1910-1915.
95. Motoyama T, Hotta T, Watanabe H, Kumanishi T, Ichikawa T, Sekiguchi M. Differential production of interleukin 6 in human osteosarcoma cells and the possible effects on neoplastic bone metabolism. Virchows Arch 1993: 63: 277-281.
96. Mundy GR. Peptides and growth regulatory factors in bone. Rheumatol Dis Clin North Am 1994: 20: 577-588.
97. Newton RC, Covington M. The activation of human fibroblast prostaglandin E production by interleukin 1. Cell Immunol 1987: 110: 338-349.
98. Nishihara T, Ohsaki Y, Ueda N, Saito N, Mundy GR. Mouse interleukin-1 receptor antagonist induced by Actinobacillus actinomycetemcomitans lipopolysaccharide blocks the effects of interleukin-1 on bone resorption and osteoclast-like cell formation. Infect Immun 1994: 62: 390-397.
99. Offenbacher S, Farr DH, Goodson JM. Measurement of prostaglandin E in crevicular fluid. J Clin Periodontol 1981: 8: 319-327.
100. 2 secretion as a determinant of periodontal disease expression. J Periodontol 1993: 64: 432-444.
101. Offenbacher S, Odle BM, Braswell LD, Johnson HG, Hall CM, McClure H, Orkin JL, Strobert EA, Green MD. Changes in cyclooxygenase metabolites in experimental periodontitis in Macaca mulatta. J Periodont Res 1989: 24: 63-74.
102. Offenbacher S, Odle BM, Gray RC, Van Dyke TE. Crevicular fluid prostaglandin E levels as a measure of the peri-odontal disease status of adult and juvenile periodontitis patients. J Periodont Res 1984: 19: 1-13.
103. 2 levels as a predictor of periodontal attachment loss. J Periodont Res 1986: 21: 101-112.
104. Ohm K, Albers HK, Lisboa BP. Measurement of 8 prostaglandins in human gingival and periodontal disease using high pressure liquid chromatography and radioimmunoassay. J Periodont Res 1984: 19: 501-511.
105. Orwoll ES. Androgens. In: Bilezikian JP, Raisz LG, Rodan GA, ed. Principles of bone biology. San Diego: Academic Press, 1996: 563-580.
106. Oursler MJ, Osdoby P, Pyfferoen J, Riggs BL, Spelsberg TC. Avian osteoclasts as estrogen target cells. Proc Natl Acad Sci USA 1991: 88: 6613-6617.
107. Page R. The role of inflammatory mediators in the pathogenesis of periodontal disease. J Periodont Res 1991: 26: 230-242.
108. Page RC, Schroeder HE. Pathogenesis of inflammatory periodontal disease: a summary of current work. Lab Invest 1976: 34: 235.
109. Parfitt AM. The coupling of bone formation to bone resorption: a critical analysis of the concept and of its relevance to the pathogenesis of osteoporosis. Metab Bone Dis Rel Res 1982: 4: 1-6.
110. Parfitt AM. The physiologic and clinical significance of bone histomorphometric data. In: Recker RR, ed. Bone histomorphometry, techniques and interpretation. Boca Raton, FL: CRC Press, 1983: 143-223.
111. Passeri G, Girasole G, Manolagas SC, Jilka RL. Endogenous production of tumor necrosis factor by primary cultures of murine calvarial cells: influence on IL-6 production and osteoclast development. Bone Miner 1994: 24: 109-126.
112. Payne WA, Page RC, Ogilvie AL, Hall WB. Histopathologic features of the initial and early stages of experimental gingivitis in man. J Periodont Res 1975: 10: 51-64.
113. Pfeilschifter J, Oechsner M, Naumann A, Gronwald RG, Minne HW, Ziegler R. Stimulation of bone matrix apposition in vitro by local growth factors: a comparison between insulin-like growth factor I, platelet-derived growth factor, and transforming growth factor beta. Endocrinology 1990: 127: 69-75.
114. Pilbeam CC, Klein-Nulend J, Raisz LG. Inhibition by 17-beta-estradiol of PTH stimulated resorption and prostaglandin production in cultured neonatal mouse calvariae. Biochem Biophys Res Commun 1989: 163: 1319-1324.
115. Prabhu A, Michalowicz BS, Mathur A. Detection of local and systemic cytokines in adult periodontitis. J Periodontol 1996: 67: 515-522.
116. Reddi AH, Wientroub S, Muthukumaran N. Biologic principles of bone induction. Orthop Clin North Am 1987: 18: 207-212.
117. Reinhardt RA, Masada MP, Johnson GK, DuBois LM, Seymour GJ, Allison AC. IL-1 in gingival crevicular fluid following closed root planing and papillary flap debridement. J Clin Periodontol 1993: 20: 514-519.
118. Richards D, Rutherford RB. The effects of interleukin 1 on collagenolytic activity and prostaglandin-E secretion by human periodontal-ligament and gingival fibroblast. Arch Oral Biol 1988: 33: 237-243.
119. Scheven BA, Visser JW, Nijweide PJ. In vitro osteoclast generation from different bone marrow fractions, including a highly enriched hematopoietic stem cell population. Nature 1986: 321: 79-81.
120. Schroeder HE, Graf-De Beer M, Attstrom R. Initial gingivitis in dogs. J Periodont Res 1975: 10: 128-142.
121. 3 in three osteoblast-like cell lines (MC-3T3-E1, ROS 17/2.8, and MG-63). Bone 1992: 13: 51-58.
122. 2 production by vitamin D metabolites in growth zone and resting zone chondrocyte cultures is dependent on cell maturation. Bone 1992: 13: 395-401.
123. Sedlin ED. The ratio of cortical area to total cross section area in rib diaphysis. A quantitative index of osteoporosis. Clin Orthop 1964: 36: 161-168.
124. Selvig KA. Ultrastructural changes in cementum and adjacent connective tissue in periodontal disease. Acta Odontol Scand 1966: 24: 459-500.
125. Selvig KA. Nonbanded fibrils of collagenous nature in human periodontal connective tissue. J Periodont Res 1968: 3: 169-179.
126. Seyedin SM, Thompson AY, Bentz H, Rosen DM, McPherson JM, Conti A, Siegel NR, Galluppi GR, Piez KA. Cartilage-inducing factor-A. Apparent identity to transforming growth factor-beta. J Biol Chem 1986: 261: 5693-5695.
127. Shankar G, Stern PH. Interactions of tumor necrosis factor with local and systemic factors in fetal rat limb bones. Calcif Tissue Int 1992: 51: 387-392.
128. Smith DD, Gowen M, Mundy GR. Effects of interferon gamma and other cytokines on collagen synthesis in fetal rat bone cultures. Endocrinology 1987: 120: 2494-2499.
129. Socransky SS. Relationship of bacteria to the etiology of periodontal disease. J Dent Res 1970: 49: 203-222.
130. Stashenko P, Fujiyoshi P, Obernesser MS, Prostak L, Haffajee AD, Socransky SS. Levels of interleukin 1β in tissue from sites of active periodontal disease. J Clin Periodontol 1991: 18: 548-554.
131. Stashenko P, Jandinski JJ, Fujiyosi P, Rynar J, Socransky SS. Tissue levels of bone resorptive cytokines in periodontal disease. J Periodontol 1991: 62: 504-509.
132. Stepan JJ, Lachman M, Zverina J, Pacovsky V, Baylink DJ. Castrated men exhibit bone loss: effect of calcitonin treatment on biochemical indices of bone remodeling. J Clin Endocrinol Metab 1989: 69: 523-527.
133. Sumitani K, Kawata T, Yoshimoto T, Yamamoto S, Kumegawa M. Fatty acid cyclooxygenase activity stimulated by transforming growth factor-beta in mouse osteoblastic cells (MC3T3-E1). Arch Biochem Biophys 1989: 270: 588-595.
134. Takeichi O, Saito I, Tsurumachi T, Saito T, Moro I. Human polymorphonuclear leukocytes derived from chronically inflamed tissue express inflammatory cytokines in vivo. Cell Immunol 1994: 156: 296-309.
135. Thomson BM, Saklatvala J. Chambers TJ. Osteoblasts mediate interleukin-1 stimulation of bone resorption by rat osteoclasts. J Exp Med 1986: 164: 104-112.
136. 1 in infants with cyanotic congenital heart disease. J Pediatr 1980: 97: 834-836.
137. Urist MR. Bone: formation by autoinduction. Science 1965: 150: 893-899.
138. Urist MR, Delange RJ, Finerman GA. Bone cell differentiation and growth factors. Science 1983: 220: 680-686.
139. Waite IM, Saxton CA, Young A, Wagg BJ, Corbett M. The periodontal status of subjects receiving non-steroidal anti-inflammatory drugs. J Periodont Res 1981: 16: 100-108.
140. Wang XF, Lin HY, Ng-Eaton E, Downward J, Lodish HF, Weinburg RA. Expression cloning and characterization of the TGF-beta type III receptor. Cell 1991: 67: 797-805.
141. Weryha G, Leclere J. Paracrine regulation of bone remodeling. Horm Res 1995: 43: 69-75.
142. Westermark B, Heldin CH. Platelet-derived growth factor. Acta Oncol 1993: 32: 101-105.
143. Williams RC, Jeffcoat MK, Howell TH. Naproxen treatment of periodontitis in beagles. J Dent Res 1989: 68: 243 (abstr).
144. Williams RC, Jeffcoat MK, Howell TH. Three year trial of flurbiprofen treatment in humans: post treatment period. J Dent Res 1991: 70: 468 (abstr).
145. Williams RC, Jeffcoat MK, Howell TH, Rolla A, Stubbs D, Teoh KW, Reddy MS, Goldhaber P. Altering the progression of human alveolar bone loss with the non-steroidal anti-inflammatory drug flurbiprofen. J Periodontol 1989: 60: 485-490.
146. Yewey GL, Tipton AJ, Dunn RL. Evaluation of biodegradable subgingival delivery system for flurbiprofen. J Dent Res 1991: 70: 324 (abstr).
147. Yoon SH. Distribution of fluorine in teeth and alveolar, bone. J Am Dent Assoc 1960: 61: 565-570.
148. Yu X, Antoniades HN, Graves DT. Expression of monocyte chemoattractant protein 1 in human inflamed gingival tissues. Infect Immun 1993: 61: 4622-4628.
149. Zachrisson BU. A histological study of experimental gingivitis in man. J Periodont Res 1968: 3: 293-302.