Alendronate regulates cytokine production induced by lipid A through nuclear factor-κB and Smad3 activation in human gingival fibroblasts

Journal of Periodontal Research

Volumn 46, Issue 1, 2011, Pages 13-20

  Tamai, R ^a   Sugiyama, A ^a   Kiyoura, Y ^a  

^a OHU UNIVERSITY   (Japan)

Author keywords

Cytokine; Lipid A; Nitrogen containing bisphosphonate; Transcription factor

Indexed keywords

ALENDRONIC ACID; BONE DENSITY CONSERVATION AGENT; CYTOKINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; LIPID A; MONOCYTE CHEMOTACTIC PROTEIN 1; SMAD3 PROTEIN;

ANALYSIS OF VARIANCE; ARTICLE; BIOSYNTHESIS; CELL CULTURE; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; FIBROBLAST; GENE EXPRESSION REGULATION; GENETICS; GINGIVA; HUMAN; IMMUNOLOGY; METABOLISM; MONONUCLEAR CELL; TRANSCRIPTION INITIATION;

ALENDRONATE; ANALYSIS OF VARIANCE; BONE DENSITY CONSERVATION AGENTS; CELLS, CULTURED; CHEMOKINE CCL2; CYTOKINES; FIBROBLASTS; GENE EXPRESSION REGULATION; GINGIVA; HUMANS; INTERLEUKIN-1BETA; INTERLEUKIN-6; INTERLEUKIN-8; LEUKOCYTES, MONONUCLEAR; LIPID A; NF-KAPPA B; SMAD3 PROTEIN; TRANSCRIPTIONAL ACTIVATION;

EID: 78650872647     PISSN: 00223484     EISSN: 16000765     Source Type: Journal    
DOI: 10.1111/j.1600-0765.2010.01302.x     Document Type: Article

References (56)

1. Fleisch H. Bisphosphonates, pharmacology and the use in the treatment of tumour induced hypercalcaemia and metastatic bone diseases. Drugs 1991;42:919-944.
2. Rogers MJ, Gordon S, Benford HL et al. Cellular and molecular mechanisms of action of bisphosphonates. Cancer 2000;88:2961-2978.
3. Lipton A. Toward new horizons: the future of bisphosphonates therapy. Oncologist 2004;9:38-47.
4. Adami S, Bhalla AK, Dorizzi R et al. The acute phase response after bisphosphonate administration. Calcif Tissue Int 1987;41:326-331.
5. Siris E. Bisphosphonates and iritis. Lancet 1993;341:436-437.
6. Sauty A, Pecherstorfer M, Zimmer-Roth I et al. Interleukin-6 and tumor necrosis factor α levels after bisphosphonates treatment in vitro and in patients with malignancy. Bone 1996;18:133-139.
7. Thiébaud D, Sauty A, Burckhardt P et al. An in vitro and in vivo study of cytokines in the acute-phase response associated with bisphosphonates. Calcif Tissue Int 1997;61:386-392.
8. Marx RE, Cillo JE Jr, Ulloa JJ. Oral bisphosphonate-induced osteonecrosis: risk factors, prediction of risk using serum CTX testing, prevention, and treatment. J Oral Maxillofac Surg 2007;65:2397-2410.
9. Lee DM, Weinblatt ME. Rheumatoid arthritis. Lancet 2001;358:903-911.
10. Charo IF, Taubman MB. Chemokines in the pathogenesis of vascular disease. Circ Res 2004;95:858-866.
11. Gauldie J, Bonniaud P, Sime P, Ask K, Kolb M. TGF-β, Smad3 and the process of progressive fibrosis. Biochem Soc Trans 2007;35:661-664.
12. Tamura T, Udagawa N, Takahashi N et al. Soluble interleukin-6 receptor triggers osteoclast formation by interleukin 6. Proc Natl Acad Sci USA 1993;90:11924-11928.
13. Suda T, Takahashi N, Udagawa N, Jimi E, Gillespie MT, Martin TJ. Modulation of osteoclast differentiation and function by the new members of the tumor necrosis factor receptor and ligand families. Endocr Rev 1999;20:345-357.
14. Lu Y, Cai Z, Xiao G et al. Monocyte chemotactic protein-1 mediates prostate cancer-induced bone resorption. Cancer Res 2007;67:3646-3653.
15. Hsu YL, Hung JY, Ko YC, Hung CH, Huang MS, Kuo PL. Phospholipase D signaling pathway is involved in lung cancer-derived IL-8 increased osteoclastogenesis. Carcinogenesis 2010;31:587-596.
16. Deng X, Yu ZQ, Funayama H et al. Mutual augmentation of the induction of the histamine-forming enzyme, histidine decarboxylase, between alendronate and immuno-stimulants (IL-1, TNF, and LPS), and its prevention by clodronate. Toxicol Appl Pharmacol 2006;213:64-73.
17. Geurs N. Osteoporosis and periodontal disease. Periodontol 2000 2007;44:29-43.
18. Edwards BJ, Migliorati CA. Osteoporosis and its implications for dental patients. J Am Dent Assoc 2008;139:545-552.
19. Fine DH, Mendieta C, Barnett ML, Furgang D, Naini A, Vincent JW. Endotoxin levels in periodontally healthy and diseased sites: correlation with levels of gram-negative bacteria. J Periodontol 1992;63:897-901.
20. Socransky SS, Haffajee AD, Cugini MA, Smith C, Kent RL Jr. Microbial complexes in subgingival plaque. J Clin Periodontol 1998;25:134-144.
21. Simon BI, Goldman HM, Ruben MP, Baker E. The role of endotoxins in periodontal disease. II. Correlation of the quantity of endotoxin in human gingival exudate with the clinical degree of inflammation. J Periodontol 1970;41:81-86.
22. Simon BI, Goldman HM, Ruben MP, Baker E. The role of endotoxins in periodontal disease. III. Correlation of the quantity of endotoxin in human gingival exudate with the histologic degree of inflammation. J Periodontol 1971;42:210-216.
23. Shapiro L, Lodato FM Jr, Courant PR, Stallard RE. Endotoxin determinations in gingival inflammation. J Periodontol 1972;43:591-596.
24. Tzamouranis A, Matthys J, Ishikawa I, Cimasoni G. Increase of endotoxin concentration in gingival washings during experimental gingivitis in man. J Periodontol 1979;50:175-177.
25. Kotani S, Takada H, Tsujimoto M et al. Synthetic lipid A with endotoxic and related biological activities comparable to those of a natural lipid A from an Escherichia coli re-mutant. Infect Immun 1985;49:225-237.
26. + fibroblasts primed with gamma interferon increase production of interleukin-8 in response to lipopolysaccharide through up-regulation of membrane CD14 and MyD88 mRNA expression. Infect Immun 2002;70:1272-1278.
27. + T cells isolated from inflamed human gingival tissues. Clin Exp Immunol 1996;103:422-428.
28. Frostegård J, Ulfgren AK, Nyberg P et al. Cytokine expression in advanced human atherosclerotic plaques: dominance of pro-inflammatory (Th1) and macrophage-stimulating cytokines. Atherosclerosis 1999;145:33-43.
29. Takada H, Iki K, Sakuta T et al. Lipopolysaccharides of oral black pigmented bacteria and periodontal diseases. A novel immunomodulator different from endotoxin was extracted from Prevotella intermedia ATCC 25611 with hot phenol-water. Prog Clin Biol Res 1995;392:59-68.
30. Pahl HL. Activators and target genes of Rel/NF-κB transcription factors. Oncogene 1999;18:6853-6866.
31. Aderem A, Ulevitch RJ. Toll-like receptors in the induction of the innate immune response. Nature 2000;406:782-787.
32. Kelley TJ, Elmer HL, Corey DA. Reduced Smad3 protein expression and altered transforming growth factor-β1-mediated signaling in cystic fibrosis epithelial cells. Am J Respir Cell Mol Biol 2001;25:732-738.
33. Feinberg MW, Watanabe M, Lebedeva MA et al. Transforming growth factor-β1 inhibition of vascular smooth muscle cell activation is mediated via Smad3. J Biol Chem 2004;279:16388-16393.
34. Ashcroft GS, Yang X, Glick AB et al. Mice lacking Smad3 show accelerated wound healing and an impaired local inflammatory response. Nat Cell Biol 1999;1:260-266.
35. Anthoni M, Wang G, Deng C, Wolff HJ, Lauerma AI, Alenius HT. Smad3 signal transducer regulates skin inflammation and specific IgE response in murine model of atopic dermatitis. J Invest Dermatol 2007;127:1923-1929.
36. Lin JH, Chen IW, Deluna FA. On the absorption of alendronate in rats. J Pharm Sci 1994;83:1741-1746.
37. Porras AG, Holland SD, Gertz BJ. Pharmacokinetics of alendronate. Clin Pharmacokinet 1999;36:315-328.
38. Kaji H, Naito J, Inoue Y, Sowa H, Sugimoto T, Chihara K. Statin suppresses apoptosis in osteoblastic cells: role of transforming growth factor-β-Smad3 pathway. Horm Metab Res 2008;40:746-751.
39. Masuda T, Deng X, Tamai R. Mouse macrophages primed with alendronate down-regulate monocyte chemoattractant protein-1 (MCP-1) and macrophage inflammatory protein-1α (MIP-1α) production in response to Toll-like receptor (TLR) 2 and TLR4 agonist via Smad3 activation. Int Immunopharmacol 2009;9:1115-1121.
40. Jinnin M, Ihn H, Tamaki K. Characterization of SIS3, a novel specific inhibitor of Smad3, and its effect on transforming growth factor-β1-induced extracellular matrix expression. Mol Pharmacol 2006;69:597-607.
41. Deng X, Tamai R, Endo Y, Kiyoura Y. Alendronate augments interleukin-1β release from macrophages infected with periodontal pathogenic bacteria through activation of caspase-1. Toxicol Appl Pharmacol 2009;235:97-104.
42. Sanders JL, Tarjan G, Foster SA, Stern PH. Alendronate/interleukin-1β cotreatment increases interleukin-6 in bone and UMR-106 cells: dose dependence and relationship to the antiresorptive effect of alendronate. J Bone Miner Res 1998;13:786-792.
43. Pacifici R, Carano A, Santoro SA et al. Bone matrix constituents stimulate interleukin-1 release from human blood mononuclear cells. J Clin Invest 1991;87:221-288.
44. Lenart BA, Lorich DG, Lane JM. Atypical fractures of the femoral diaphysis in postmenopausal women taking alendronate. N Engl J Med 2008;358:1304-1306.
45. Weinstein RS, Roberson PK, Manolagas SC. Giant osteoclast formation and long-term oral bisphosphonate therapy. N Engl J Med 2009;360:53-62.
46. Asensi V, Valle E, Meana A et al. In vivo interleukin-6 protects neutrophils from apoptosis in osteomyelitis. Infect Immun 2004;72:3823-3828.
47. Li X, Qin L, Bergenstock M, Bevelock LM, Novack DV, Partridge NC. Parathyroid hormone stimulates osteoblastic expression of MCP-1 to recruit and increase the fusion of pre/osteoclasts. J Biol Chem 2007;282:33098-33106.
48. Gazzaniga S, Bravo AI, Guglielmotti A et al. Targeting tumor-associated macrophages and inhibition of MCP-1 reduce angiogenesis and tumor growth in a human melanoma xenograft. J Invest Dermatol 2007;127:2031-2041.
49. Loppnow H, Stelter F, Schönbeck U et al. Endotoxin activates human vascular smooth muscle cells despite lack of expression of CD14 mRNA or endogenous membrane CD14. Infect Immun 1995;63:1020-1026.
50. Hayashi J, Masaka T, Ishikawa I. Increased levels of soluble CD14 in sera of periodontitis patients. Infect Immun 1999;67:417-420.
51. Akashi S, Saitoh S, Wakabayashi Y et al. Lipopolysaccharide interaction with cell surface Toll-like receptor 4-MD-2: higher affinity than that with MD-2 or CD14. J Exp Med 2003;198:1035-1042.
52. Feinberg MW, Shimizu K, Lebedeva M et al. Essential role for Smad3 in regulating MCP-1 expression and vascular inflammation. Circ Res 2004;94:601-608.
53. Lu S, Lee J, Revelo M, Wang X, Lu S, Dong Z. Smad3 is overexpressed in advanced human prostate cancer and necessary for progressive growth of prostate cancer cells in nude mice. Clin Cancer Res 2007;13:5692-5702.
54. Leivonen SK, Chantry A, Hakkinen L, Han J, Kahari VM. Smad3 mediates transforming growth factor-β-induced collagenase-3 (matrix metalloproteinase-13) expression in human gingival fibroblasts. Evidence for cross-talk between Smad3 and p38 signaling pathways. J Biol Chem 2002;277:46338-46346.
55. Menezes AM, Rocha FA, Chaves HV, Carvalho CB, Ribeiro RA, Brito GA. Effect of sodium alendronate on alveolar bone resorption in experimental periodontitis in rats. J Periodontol 2005;76:1901-1909.
56. Fleisch HA. Bisphosphonates: preclinical aspects and use in osteoporosis. Ann Med 1997;29:55-62.