Critical review in oral biology & medicine: Inflammation and uncoupling as mechanisms of periodontal bone loss

Journal of Dental Research

Volumn 90, Issue 2, 2011, Pages 143-153

  Graves, D T ^a   Li, J ^b   Cochran, D L ^c  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b RUTGERS SCHOOL OF DENTAL MEDICINE   (United States)

^c UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

Author keywords

adaptive immunity; bone matrix; cytokine; IL 1; innate immunity; osteoblast; osteoclast; RANK ligand; TNF.

Indexed keywords

AUTACOID; CYTOKINE;

ADAPTIVE IMMUNITY; ALVEOLAR BONE LOSS; ANIMAL; ARTICLE; BONE MATRIX; BONE REMODELING; CD4+ T LYMPHOCYTE; GINGIVITIS; HUMAN; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY; PORPHYROMONAS GINGIVALIS; TOOTH PLAQUE;

ADAPTIVE IMMUNITY; ALVEOLAR BONE LOSS; ANIMALS; BONE MATRIX; BONE REMODELING; CD4-POSITIVE T-LYMPHOCYTES; CYTOKINES; DENTAL PLAQUE; GINGIVITIS; HUMANS; INFLAMMATION MEDIATORS; PORPHYROMONAS GINGIVALIS;

EID: 79951610661     PISSN: 00220345     EISSN: 15440591     Source Type: Journal    
DOI: 10.1177/0022034510385236     Document Type: Article

References (101)

1. Al-Mashat HA, Kandru S., Liu R., Behl Y., Desta T., Graves DT (2006). Diabetes enhances mRNA levels of proapoptotic genes and caspase activity, which contribute to impaired healing. Diabetes 55: 487-495. (Pubitemid 43343280)
2. Arron JR, Choi Y. (2000). Bone versus immune system. Nature 408: 535-536.
3. Assuma R., Oates T., Cochran D., Amar S., Graves D. (1998). IL-1 and TNF antagonists inhibit the inflammatory response and bone loss in experimental periodontitis. J. Immunol 160: 403-409. (Pubitemid 28116755)
4. Baker P., Evans R., Roopenian D. (1994). Oral infection with Porphyromonas gingivalis and induced alveolar bone loss in immunocompetent and severe combined immunodeficient mice. Arch Oral Biol 39: 1035-1040. (Pubitemid 124034593)
5. Baker P., Dixon M., Evans R., Dufour L., Johnson E., Roopenian D. (1999). CD4(+) T cells and the proinflammatory cytokines gamma interferon and interleukin-6 contribute to alveolar bone loss in mice. Infect Immun 67: 2804-2809. (Pubitemid 29244693)
6. Baker PJ, Dixon M., Roopenian DC (2000). Genetic control of susceptibility to Porphyromonas gingivalis-induced alveolar bone loss in mice. Infect Immun 68: 5864-5868.
7. Bartold PM, Cantley MD, Haynes DR (2010). Mechanisms and control of pathologic bone loss in periodontitis. Periodontol 2000 53: 55-69.
8. Behl Y., Siqueira M., Ortiz J., Li J., Desta T., Faibish D., et al. (2008). Activation of the acquired immune response reduces coupled bone formation in response to a periodontal pathogen. J Immunol 181: 8711-8718.
9. Bertolini DR, Nedwin GE, Bringman TS, Smith DD, Mundy GR (1986). Stimulation of bone resorption and inhibition of bone formation in vitro by human tumour necrosis factors. Nature 319: 516-518. (Pubitemid 16212936)
10. Centrella M., McCarthy TL, Canalis E. (1988). Tumor necrosis factor-alpha inhibits collagen synthesis and alkaline phosphatase activity independently of its effect on deoxyribonucleic acid synthesis in osteoblast-enriched bone cell cultures. Endocrinology 123: 1442-1448.
11. Chang J., Wang Z., Tang E., Fan Z., McCauley L., Franceschi R., et al. (2009). Inhibition of osteoblastic bone formation by nuclear factor-kappaB. Nat Med 15: 682-689.
12. Chen C. -P, Hertzberg M., Jiang Y., Graves DT (1999). IL-1 and TNF receptor signaling is not required for bacteria-induced osteoclastogenesis and bone loss but is essential for protecting the host from a mixed anaerobic infection. Am J Pathol 155: 2145-2152.
13. Cirelli JA, Park CH, MacKool K., Taba M. Jr, Lustig KH, Burstein H., et al. (2009). AAV2/1-TNFR:Fc gene delivery prevents periodontal disease progression. Gene Ther 16: 426-436.
14. Cochran DL (2008). Inflammation and bone loss in periodontal disease. J Periodontol 79 (8 Suppl): S1569 - S1576.
15. De Rossi A., Rocha LB, Rossi MA (2008). Interferon-gamma, interleukin-10, intercellular adhesion molecule-1, and chemokine receptor 5, but not interleukin-4, attenuate the development of periapical lesions. J Endod 34: 31-38.
16. Delima A., Oates T., Assuma R., Schwartz Z., Cochran D., Amar S., et al. (2001). Soluble antagonists to interleukin-1 (IL-1) and tumor necrosis factor (TNF) inhibits (sic) loss of tissue attachment in experimental periodontitis. J Clin Periodontol 28: 233-240. (Pubitemid 33755189)
17. Delima AJ, Karatzas S., Amar S., Graves DT (2002). Inflammation and tissue loss caused by periodontal pathogens is (sic) reduced by IL-1 antagonists. J Infect Dis 186: 511-516. (Pubitemid 34876260)
18. Devlin RD, Reddy SV, Savino R., Ciliberto G., Roodman GD (1998). IL-6 mediates the effects of IL-1 or TNF, but not PTHrP or 1,25(OH)2D3, on osteoclast-like cell formation in normal human bone marrow cultures. J Bone Miner Res 13: 393-399. (Pubitemid 28146221)
19. Diarra D., Stolina M., Polzer K., Zwerina J., Ominsky MS, Dwyer D., et al. (2007). Dickkopf-1 is a master regulator of joint remodeling. Nat Med 13: 156-163.
20. Eguchi Y., Wakitani S., Imai Y., Naka Y., Hashimoto Y., Nakamura H., et al. (2009). Antitumor necrotic factor agent promotes BMP-2-induced ectopic bone formation. J Bone Miner Metab 28: 157-164.
21. Fine DH, Velliyagounder K., Furgang D., Kaplan JB (2005). The Actinobacillus actinomycetemcomitans autotransporter adhesin Aae exhibits specificity for buccal epithelial cells from humans and old world primates. Infect Immun 73: 1947-1953. (Pubitemid 40470791)
22. Foster BL, Popowics TE, Fong HK, Somerman MJ (2007). Advances in defining regulators of cementum development and periodontal regeneration. Curr Top Dev Biol 78: 47-126.
23. Frost A., Jonsson KB, Nilsson O., Ljunggren O. (1997). Inflammatory cytokines regulate proliferation of cultured human osteoblasts. Acta Orthop Scand 68: 91-96. (Pubitemid 27202065)
24. Gao Y., Grassi F., Ryan MR, Terauchi M., Page K., Yang X., et al. (2007). IFN-gamma stimulates osteoclast formation and bone loss in vivo via antigen-driven T cell activation. J Clin Invest 117: 122-132. (Pubitemid 46048459)
25. Gargiulo AW, Wentz FM, Orban B. (1961). Dimensions and relations of the dentogingival junction in humans. J Periodontol 32: 261-267.
26. Garlet GP, Cardoso CR, Silva TA, Ferreira BR, Avila-Campos MJ, Cunha FQ, et al. (2006). Cytokine pattern determines the progression of experimental periodontal disease induced by Actinobacillus actinomycetemcomitans through the modulation of MMPs, RANKL, and their physiological inhibitors. Oral Microbiol Immunol 21: 12-20.
27. Garlet GP, Cardoso CR, Campanelli AP, Ferreira BR, Avila-Campos MJ, Cunha FQ, et al. (2007). The dual role of p55 tumour necrosis factor-alpha receptor in Actinobacillus actinomycetemcomitans-induced experimental periodontitis: host protection and tissue destruction. Clin Exp Immunol 147: 128-138. (Pubitemid 44915564)
28. Garlet GP, Cardoso CR, Campanelli AP, Garlet TP, Avila-Campos MJ, Cunha FQ, et al. (2008). The essential role of IFN-gamma in the control of lethal Aggregatibacter actinomycetemcomitans infection in mice. Microbes Infect 10: 489-496.
29. Gilbert L., He X., Farmer P., Boden S., Kozlowski M., Rubin J., et al. (2000). Inhibition of osteoblast differentiation by tumor necrosis factor-alpha. Endocrinology 141: 3956-3964.
30. Gilbert L., He X., Farmer P., Rubin J., Drissi H., van Wijnen AJ, et al. (2002). Expression of the osteoblast differentiation factor RUNX2 (Cbfa1/ AML3/Pebp2alpha A) is inhibited by tumor necrosis factor-alpha. J Biol Chem 277: 2695-2701. (Pubitemid 34953297)
31. Gilbert LC, Rubin J., Nanes MS (2005). The p55 TNF receptor mediates TNF inhibition of osteoblast differentiation independently of apoptosis. Am J Physiol Endocrinol Metab 288: E1011 - E1018.
32. Graves D. (2008). Cytokines that promote periodontal tissue destruction. J Periodontol 79 (8 Suppl): S1585 - S1591.
33. Graves D., Delima A., Assuma R., Amar S., Oates T., Cochran D. (1998). Interleukin-1 and tumor necrosis factor antagonists inhibit the progression of inflammatory cell infiltration toward alveolar bone in experimental periodontitis. J Periodontol 69: 1419-1425.
34. Graves D., Oskoui M., Volejnikova S., Naguib G., Cai S., Desta T., et al. (2001). Tumor necrosis factor modulates fibroblast apoptosis, PMN recruitment, and osteoclast formation in response to P. gingivalis infection. J Dent Res 80: 1875-1879. (Pubitemid 33038053)
35. Graves DT, Fine D., Teng YT, Van Dyke TE, Hajishengallis G. (2008). The use of rodent models to investigate host-bacteria interactions related to periodontal diseases. J Clin Periodontol 35: 89-105.
36. Han X., Kawai T., Eastcott JW, Taubman MA (2006). Bacterial-responsive B lymphocytes induce periodontal bone resorption. J Immunol 176: 625-631. (Pubitemid 43023311)
37. Han X., Kawai T., Taubman MA (2007). Interference with immune-cell-mediated bone resorption in periodontal disease. Periodontol 2000 45: 76-94.
38. Handfield M., Baker HV, Lamont RJ (2008). Beyond good and evil in the oral cavity: insights into host-microbe relationships derived from transcriptional profiling of gingival cells. J Dent Res 87: 203-223.
39. Hasturk H., Kantarci A., Ohira T., Arita M., Ebrahimi N., Chiang N., et al. (2006). RvE1 protects from local inflammation and osteoclast-mediated bone destruction in periodontitis. FASEB J 20: 401-403. (Pubitemid 46671185)
40. Hikiji H., Takato T., Shimizu T., Ishii S. (2008). The roles of prostanoids, leukotrienes, and platelet-activating factor in bone metabolism and disease. Prog Lipid Res 47: 107-126.
41. Huang GT, Do M., Wingard M., Park JS, Chugal N. (2001). Effect of interleukin-6 deficiency on the formation of periapical lesions after pulp exposure in mice. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 92: 83-88. (Pubitemid 33601706)
42. Jilka RL (2007). Molecular and cellular mechanisms of the anabolic effect of intermittent PTH. Bone 40: 1434-1446. (Pubitemid 46756429)
43. Jin Q., Cirelli JA, Park CH, Sugai JV, Taba M. Jr, Kostenuik PJ, et al. (2007). RANKL inhibition through osteoprotegerin blocks bone loss in experimental periodontitis. J Periodontol 78: 1300-1308.
44. Kawai T., Matsuyama T., Hosokawa Y., Makihira S., Seki M., Karimbux NY, et al. (2006). B and T lymphocytes are the primary sources of RANKL in the bone resorptive lesion of periodontal disease. Am J Pathol 169: 987-998. (Pubitemid 44411961)
45. Keffer J., Probert L., Cazlaris H., Georgopoulos S., Kaslaris E., Kioussis D., et al. (1991). Transgenic mice expressing human tumour necrosis factor: a predictive genetic model of arthritis. EMBO J 10: 4025-4031. (Pubitemid 21905432)
46. Kenworthy R., Baverel M. (1981). Studies of a periodontal tissue lesion in the rat, untreated or treated with chlorhexidine digluconate. J Clin Periodontol 8: 349-358. (Pubitemid 11008409)
47. Keyes PH, Jordan HV (1964). Periodontal lesions in the Syrian hamster. III. Findings related to an infectious and transmissible component. Arch Oral Biol 32: 377-400.
48. Kirkwood KL, Cirelli JA, Rogers JE, Giannobile WV (2007). Novel host response therapeutic approaches to treat periodontal diseases. Periodontol 2000 43: 294-315.
49. Kuzushima M., Mogi M., Togari A. (2006). Cytokine-induced nitric-oxide-dependent apoptosis in mouse osteoblastic cells: involvement of p38MAP kinase. Arch Oral Biol 51: 1048-1053. (Pubitemid 44442099)
50. Lalla E., Lamster I., Feit M., Huang L., Schmidt A. (1998). A murine model of accelerated periodontal disease in diabetes. J Periodontal Res 33: 387-399. (Pubitemid 128527122)
51. Leone CW, Bokhadhoor H., Kuo D., Desta T., Yang J., Siqueira MF, et al. (2006). Immunization enhances inflammation and tissue destruction in response to Porphyromonas gingivalis. Infect Immun 74: 2286-2292.
52. Lewiecki EM (2009). Denosumab update. Curr Opin Rheumatol 21: 369-373.
53. Lin WL, McCulloch CA, Cho MI (1994). Differentiation of periodontal ligament fibroblasts into osteoblasts during socket healing after tooth extraction in the rat. Anat Rec 240: 492-506. (Pubitemid 24350484)
54. Lindhe J., Hamp SE, Löe H. (1975). Plaque induced periodontal disease in beagle dogs. A 4-year clinical, roentgenographical and histometrical study. J Periodontal Res 10: 243-255.
55. Liu R., Bal HS, Desta T., Behl Y., Graves DT (2006 a). Tumor necrosis factor-alpha mediates diabetes-enhanced apoptosis of matrix-producing cells and impairs diabetic healing. Am J Pathol 168: 757-764. (Pubitemid 43327728)
56. Liu R., Bal HS, Desta T., Krothapalli N., Alyassi M., Luan Q., et al. (2006 b). Diabetes enhances periodontal bone loss through enhanced resorption and diminished bone formation. J Dent Res 85: 510-514. (Pubitemid 43945487)
57. Löe H., Theilade E., Jensen SB (1965). Experimental gingivitis in man. J Periodontol 36: 177-187.
58. Nagahata T., Kiyoshige T., Tomono S., Abe R., Sasaki S., Takazoe I. (1982). Oral implantation of Bacteroides asaccharolyticus and Eikenella corrodens in conventional hamsters. Infect Immun 36: 304-309. (Pubitemid 12156440)
59. Nguyen L., Dewhirst FE, Hauschka PV, Stashenko P. (1991). Interleukin-1 beta stimulates bone resorption and inhibits bone formation in vivo. Lymphokine Cytokine Res 10: 15-21.
60. Noguchi K., Ishikawa I. (2007). The roles of cyclooxygenase-2 and prostaglandin E2 in periodontal disease. Periodontol 2000 43: 85-101.
61. Nualart Grollmus ZC, Morales Chavez MC, Silvestre Donat FJ (2007). Periodontal disease associated to systemic genetic disorders. Med Oral Patol Oral Cir Bucal 12 (3). E211 - E215.
62. Page R., Schroeder H. (1976). Pathogenesis of inflammatory periodontal disease. A summary of current work. Lab Invest 34: 235-249.
63. Page RC, Schroeder HE (1981). Current status of the host response in chronic marginal periodontitis. J Periodontol 52: 477-491. (Pubitemid 12208233)
64. Paquette DW, Lawrence HP, McCombs GB, Wilder R., Binder TA, Troullos E., et al. (2000). Pharmacodynamic effects of ketoprofen on crevicular fluid prostanoids in adult periodontitis. J Clin Periodontol 27: 558-566.
65. Parfitt A. (1982). 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 Relat Res 4: 1-6.
66. Persson GR, Engel D., Whitney C., Darveau R., Weinberg A., Brunsvold M., et al. (1994). Immunization against Porphyromonas gingivalis inhibits progression of experimental periodontitis in nonhuman primates. Infect Immun 62: 1026-1031. (Pubitemid 24065591)
67. Pouliot M., Clish CB, Petasis NA, Van Dyke TE, Serhan CN (2000). Lipoxin A(4) analogues inhibit leukocyte recruitment to Porphyromonas gingivalis: a role for cyclooxygenase-2 and lipoxins in periodontal disease. Biochemistry 39: 4761-4768. (Pubitemid 30225341)
68. Rached MT, Kode A., Silva BC, Jung DY, Gray S., Ong H., et al. (2010). FoxO1 expression in osteoblasts regulates glucose homeostasis through regulation of osteocalcin in mice. J Clin Invest 120: 357-368.
69. Rauner M., Sipos W., Pietschmann P. (2007). Osteoimmunology. Int Arch Allergy Immunol 143: 31-48. (Pubitemid 46625234)
70. Reddy M., Geurs N., Gunsolley J. (2003). Periodontal host modulation with antiproteinase, anti-inflammatory, and bone-sparing agents. A systematic review. Ann Periodontol 8: 12-37.
71. Rogers JE, Li F., Coatney DD, Otremba J., Kriegl JM, Protter TA, et al. (2007). A p38 mitogen-activated protein kinase inhibitor arrests active alveolar bone loss in a rat periodontitis model. J Periodontol 78: 1992-1998.
72. Rossa C. Jr, Liu M., Kirkwood KL (2008). A dominant function of p38 mitogen-activated protein kinase signaling in receptor activator of nuclear factor-kappaB ligand expression and osteoclastogenesis induction by Aggregatibacter actinomycetemcomitans and Escherichia coli lipopolysaccharide. J Periodontal Res 43: 201-211.
73. Rovin S., Costich ER, Gordon HA (1966). The influence of bacteria and irritation in the initiation of periodontal disease in germfree and conventional rats. J Periodontal Res 1: 193-204.
74. Rowe DJ, Bradley LS (1981). Quantitative analyses of osteoclasts, bone loss and inflammation in human periodontal disease. J Periodontal Res 16: 13-19. (Pubitemid 11141554)
75. Saxe SR, Greene JC, Bohannan HM, Vermillion JR (1967). Oral debris, calculus, and periodontal disease in the beagle dog. Periodontics 5: 217-225.
76. Schreiner HC, Sinatra K., Kaplan JB, Furgang D., Kachlany SC, Planet PJ, et al. (2003). Tight-adherence genes of Actinobacillus actinomycetemcomitans are required for virulence in a rat model. Proc Natl Acad Sci USA 100: 7295-7300. (Pubitemid 36706432)
77. Schroeder H., Lindhe J. (1980). Conditions and pathological features of rapidly destructive, experimental periodontitis in dogs. J Periodontol 51: 6-19. (Pubitemid 10145546)
78. Serhan CN, Jain A., Marleau S., Clish C., Kantarci A., Behbehani B., et al. (2003). Reduced inflammation and tissue damage in transgenic rabbits overexpressing 15-lipoxygenase and endogenous anti-inflammatory lipid mediators. J Immunol 171: 6856-6865. (Pubitemid 37532121)
79. Sharma A., Inagaki S., Honma K., Sfintescu C., Baker PJ, Evans RT (2005). Tannerella forsythia-induced alveolar bone loss in mice involves leucine-rich-repeat BspA protein. J Dent Res 84: 462-467. (Pubitemid 43827880)
80. Silva TA, Garlet GP, Fukada SY, Silva JS, Cunha FQ (2007). Chemokines in oral inflammatory diseases: apical periodontitis and periodontal disease. J Dent Res 86: 306-319.
81. Sims NA, Gooi JH (2008). Bone remodeling: multiple cellular interactions required for coupling of bone formation and resorption. Semin Cell Dev Biol 19: 444-451.
82. Stashenko P., Dewhirst FE, Rooney M., Desjardins L., Heeley J. (1987). Interleukin-1B is potent inhibitor of bone formation in vitro. J Bone Min Res 2: 559-565.
83. Taichman RS, Hauschka PV (1992). Effects of interleukin-1 beta and tumor necrosis factor-alpha on osteoblastic expression of osteocalcin and mineralized extracellular matrix in vitro. Inflammation 16: 587-601.
84. Teng Y. (2006). Protective and destructive immunity in the periodontium: Part 2-T-cell-mediated immunity in the periodontium. J Dent Res 85: 209-219. (Pubitemid 43827727)
85. Teng Y., Nguyen H., Gao X., Kong Y., Gorczynski R., Singh B., et al. (2000). Functional human T-cell immunity and osteoprotegerin ligand control alveolar bone destruction in periodontal infection. J Clin Invest 106: R59 - R67.
86. Thammasitboon K., Goldring SR, Boch JA (2006). Role of macrophages in LPS-induced osteoblast and PDL cell apoptosis. Bone 38: 845-852. (Pubitemid 44498576)
87. Theilade E., Wright WH, Jensen SB, Löe H. (1966). Experimental gingivitis in man. II. A longitudinal clinical and bacteriological investigation. J Periodontal Res 1: 1-13.
88. Troen BR (2003). Molecular mechanisms underlying osteoclast formation and activation. Exp Gerontol 38: 605-614. (Pubitemid 36694163)
89. Tsuboi M., Kawakami A., Nakashima T., Matsuoka N., Urayama S., Kawabe Y., et al. (1999). Tumor necrosis factor-alpha and interleukin-1beta increase the Fas-mediated apoptosis of human osteoblasts. J Lab Clin Med 134: 222-231. (Pubitemid 29423094)
90. Van Dyke TE (2008). The management of inflammation in periodontal disease. J Periodontol 79 (8 Suppl): S1601 - S1608.
91. Walsh NC, Reinwald S., Manning CA, Condon KW, Iwata K., Burr DB, et al. (2009). Osteoblast function is compromised at sites of focal bone erosion in inflammatory arthritis. J Bone Miner Res 24: 1572-1585.
92. Wang GL, Fu YC, Xu WC, Feng YQ, Fang SR, Zhou XH (2009). Resveratrol inhibits the expression of SREBP1 in cell model of steatosis via Sirt1-FOXO1 signaling pathway. Biochem Biophys Res Commun 380: 644-649.
93. Wei S., Kitaura H., Zhou P., Ross FP, Teitelbaum SL (2005). IL-1 mediates TNF-induced osteoclastogenesis. J Clin Invest 115: 282-290. (Pubitemid 40385470)
94. Weiner GS, DeMarco TJ, Bissada NF (1979). Long term effect of systemic tetracycline administration on the severity of induced periodontitis in the rat. J Periodontol 50: 619-623. (Pubitemid 10177345)
95. Weitzmann MN, Pacifici R. (2006). Estrogen regulation of immune cell bone interactions. Ann NY Acad Sci 1068: 256-274. (Pubitemid 43824158)
96. Williams R., Jeffcoat M., Kaplan M., Goldhaber P., Johnson H., Wechter W. (1985). Flurbiprofen: a potent inhibitor of alveolar bone resorption in beagles. Science 227: 640-642. (Pubitemid 15157484)
97. Yamashita K., Eastcott JW, Taubman MA, Smith DJ, Cox DS (1991). Effect of adoptive transfer of cloned Actinobacillus actinomycetemcomitans-specific T helper cells on periodontal disease. Infect Immun 59: 1529-1534.
98. Yang S., Madyastha P., Ries W., Key LL (2002). Characterization of interferon gamma receptors on osteoclasts: effect of interferon gamma on osteoclastic superoxide generation. J Cell Biochem 84: 645-654. (Pubitemid 34111198)
99. Yin MT, Dobkin JF, Grbic JT (2007). Epidemiology, pathogenesis, and management of human immunodeficiency virus infection in patients with periodontal disease. Periodontol 2000 44: 55-81.
100. Yu JJ, Ruddy MJ, Wong GC, Sfintescu C., Baker PJ, Smith JB, et al. (2007). An essential role for IL-17 in preventing pathogen-initiated bone destruction: recruitment of neutrophils to inflamed bone requires IL-17 receptor-dependent signals. Blood 109: 3794-3802. (Pubitemid 46641730)
101. Yu X., Graves D. (1995). Fibroblasts, mononuclear phagocytes and endothelial cells express MCP-1 in inflamed human gingiva. J Periodontol 66: 80-88.