Interleukin-4 suppresses IL-1-induced expression of matrix metalloproteinase-3 in human gingival fibroblasts

Journal of Periodontology

Volumn 75, Issue 2, 2004, Pages 283-291

  Jenkins, Kosunique ^a   Javadi, Masoud ^a   Borghaei, Ruth Carter ^a  

^a PHILADELPHIA COLLEGE OF OSTEOPATHIC MEDICINE   (United States)

Author keywords

Fibroblasts, gingival; Gene expression regulation; Intereleukin 1; Interleukin 4; Metalloproteinases, matrix; Periodontitis

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1; INTERLEUKIN 4; MESSENGER RNA; PROSTAGLANDIN E2; STROMELYSIN; TRANSCRIPTION FACTOR AP 1;

CELL CULTURE; CELL ISOLATION; CONCENTRATION (PARAMETERS); CONCENTRATION RESPONSE; CONTROLLED STUDY; DNA BINDING; ENZYME IMMUNOASSAY; ENZYME LINKED IMMUNOSORBENT ASSAY; FIBROBLAST; GEL MOBILITY SHIFT ASSAY; GINGIVA; HUMAN; HUMAN CELL; INCUBATION TIME; NORTHERN BLOTTING; PERIODONTITIS; PROSTAGLANDIN SYNTHESIS; QUANTITATIVE ANALYSIS; REVIEW; RNA ISOLATION; STATISTICAL ANALYSIS; STATISTICAL SIGNIFICANCE;

BLOTTING, NORTHERN; CELLS, CULTURED; DINOPROSTONE; DOSE-RESPONSE RELATIONSHIP, DRUG; FIBROBLASTS; GINGIVA; HUMANS; INTERLEUKIN-1; INTERLEUKIN-4; MATRIX METALLOPROTEINASE 3; NF-KAPPA B; PERIODONTITIS; RNA, MESSENGER; TRANSCRIPTION FACTOR AP-1;

EID: 1642393208     PISSN: 00223492     EISSN: None     Source Type: Journal    
DOI: 10.1902/jop.2004.75.2.283     Document Type: Review

References (89)

1. Williams RC. Periodontal disease. N Engl J Med 1990; 322:373-382.
2. Brown LJ, Brunelle JA, Kingman A. Periodontal status in the United States, 1988-1991: Prevalence, extent, and demographic variation. J Dent Res 1996;75(Spec. No.): 672-683.
3. Li X, Kolltveit KM, Tronstad L, Olsen I. Systemic diseases caused by oral infection. Clin Microbiol Rev 2000;13: 547-558.
4. Fowler EB, Breault LG, Cuenin MF. Periodontal disease and its association with systemic disease. Mil Med 2001; 166:85-89.
5. American Academy of Periodontology. Epidemiology of periodontal diseases (position paper). J Periodontol 1996;67:935-945.
6. Stashenko P, Fujiyoshi P, Obernesser MS, Prostak L, Haffajee AD, Socransky SS. Levels of interleukin 1 beta in tissue from sites of active periodontal disease. J Clin Periodontol 1991;18:548-554.
7. Stashenko P, Jandinski JJ, Fujiyoshi P, Rynar J, Socransky SS. Tissue levels of bone resorptive cytokines in periodontal disease. J Periodontol 1991;62: 504-509.
8. Honig J, Rordorf-Adam C, Siegmund C, Wiedemann W, Erard F. Increased interleukin-1 beta (IL-1 beta) concentration in gingival tissue from periodontitis patients. J Periodont Res 1989;24:362-367.
9. Yamamoto M, Fujihashi K, Hiroi T, McGhee JR, Van Dyke TE, Kiyono H. Molecular and cellular mechanisms for periodontal diseases: Role of Th1 and Th2 type cytokines in induction of mucosal inflammation. J Periodont Res 1997;32:115-119.
10. Ukai T, Mori Y, Onoyama M, Hara Y. Immunohistological study of interferon-gamma- and interleukin-4-bearing cells in human periodontitis gingiva. Arch Oral Biol 2001; 46:901-908.
11. Shapira L, Van Dyke TE, Hart TC. A localized absence of interleukin-4 triggers periodontal disease activity: A novel hypothesis. Med Hypotheses 1992;39:319-322.
12. Ejeil AL, Gaultier F, Igondjo-Tchen S, et al. Are cytokines linked to collagen breakdown during periodontal disease progression? J Periodontol 2003;74:196-201.
13. Michel J, Gonzales JR, Wunderlich D, Diete A, Herrmann JM, Meyle J. Interleukin-4 polymorphisms in early onset periodontitis. J Clin Periodontol 2001;28:483-488.
14. Jorgensen C, Apparailly F, Couret I, Canovas F, Jacquet C, Sany J. Interleukin-4 and interleukin-10 are chondroprotective and decrease mononuclear cell recruitment in human rheumatoid synovium in vivo. Immunology 1998; 93:518-523.
15. Lubberts E, Joosten LA, van Den Bersselaar L, et al. Adenoviral vector-mediated overexpression of IL-4 in the knee joint of mice with collagen-induced arthritis prevents cartilage destruction. J Immunol 1999;163: 4546-4556.
16. Parsons SL, Watson SA, Brown PD, Collins HM, Steele RJ. Matrix metalloproteinases. Br J Surg 1997;84:160-166.
17. Knauper V, Wilhelm SM, Seperack PK, et al. Direct activation of human neutrophil procollagenase by recombinant stromelysin. Biochem J 1993;295:581-586.
18. Knauper V, Lopez-Otin C, Smith B, Knight G, Murphy G. Biochemical characterization of human collagenase-3. J Biol Chem 1996;271:1544-1550.
19. Murphy G, Cockett MI, Stephens PE, Smith BJ, Docherty AJ. Stromelysin is an activator of procollagenase. A study with natural and recombinant enzymes. Biochem J 1987;248:265-268.
20. Ogata Y, Enghild JJ, Nagase H. Matrix metalloproteinase 3 (stromelysin) activates the precursor for the human matrix metalloproteinase 9. J Biol Chem 1992;267:3581-3584.
21. Suzuki K, Enghild JJ, Morodomi T, Salvesen G, Nagase H. Mechanisms of activation of tissue procollagenase by matrix metalloproteinase 3 (stromelysin). Biochemistry 1990;29:10261-10270.
22. Lijnen HR, Arza B, Van Hoef B, Collen D, Declerck PJ. Inactivation of plasminogen activator inhibitor-1 by specific proteolysis with stromelysin-1 (MMP-3). J Biol Chem 2000;275:37645-37650.
23. Matsuno H, Yudoh K, Watanabe Y, Nakazawa F, Aono H, Kimura T. Stromelysin-1 (MMP-3) in synovial fluid of patients with rheumatoid arthritis has potential to cleave membrane bound Fas ligand. J Rheumatol 2001;28:22-28.
24. Aiba T, Akeno N, Kawane T, Okamoto H, Horiuchi N. Matrix metalloproteinases-1 and -8 and TIMP-1 mRNA levels in normal and diseased human gingivae. Eur J Oral Sci 1996;104:562-569.
25. Haerian A, Adonogianaki E, Mooney J, Docherty JP, Kinane DF. Gingival crevicular stromelysin, collagenase and tissue inhibitor of metalloproteinases levels in healthy and diseased sites. J Clin Periodontol 1995;22:505-509.
26. Ingman T, Sorsa T, Michaelis J, Konttinen YT. Immunohistochemical study of neutrophil- and fibroblast-type collagenases and stromelysin-1 in adult periodontitis. Scand J Dent Res 1994;102:342-349.
27. Kubota T, Nomura T, Takahashi T, Hara K. Expression of mRNA for matrix metalloproteinases and tissue inhibitors of metalloproteinases in periodontitis-affected human gingival tissue. Arch Oral Biol 1996;41:253-262.
28. Alpagot T, Bell C, Lundergan W, Chambers DW, Rudin R. Longitudinal evaluation of GCF MMP-3 and TIMP-1 levels as prognostic factors for progression of periodontitis. J Clin Periodontol 2001;28:353-359.
29. Reynolds JJ, Hembry RM, Meikle MC. Connective tissue degradation in health and periodontal disease and the roles of matrix metalloproteinases and their natural inhibitors. Adv Dent Res 1994;8:312-319.
30. Prontera C, Crescenzi G, Rotilio D. Inhibition by Interleukin-4 of stromelysin expression in human skin fibroblasts: Role of PKC. Exp Cell Res 1996;224:183-188.
31. Shingu M, Miyauchi S, Nagai Y, Yasutake C, Horie K. The role of IL-4 and IL-6 in IL-1-dependent cartilage matrix degradation. Br J Rheumatol 1995;34:101-106.
32. Nemoto O, Yamada H, Kikuchi T, et al. Suppression of matrix metalloproteinase-3 synthesis by interleukin-4 in human articular chondrocytes. J Rheumatol 1997;24: 1774-1779.
33. Borghaei RC, Rawlings PL Jr, Mochan E. Interleukin-4 suppression of interleukin-1-induced transcription of collagenase (MMP-1) and stromelysin 1 (MMP-3) in human synovial fibroblasts. Arthritis Rheum 1998;41:1398-1406.
34. Mochan E, Uhl J, Newton R. IL-1 stimulation of synovial plasminogen activator production. J Rheumatol 1986;13: 15-19.
35. 2 and cyclic AMP. Arthritis Rheum 1986;29:1078-1084.
36. Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid-guanidinium-thiocyanate-phenol-chloroform extraction. Anal Biochem 1987;162:156-159.
37. Schreiber E, Matthais P, Muller MM, Schaffner W. Rapid detection of octamer binding protein with 'mini-extracts' prepared from a small number of cells. Nucleic Acids Res 1989;17:6419.
38. Dechanet J, Rissoan MC, Banchereau J, Miossec P. Interleukin 4, but not interleukin 10, regulates the production of inflammation mediators by rheumatoid synoviocytes. Cytokine 1995;7:176-183.
39. 2 synthesis by human lung fibroblasts. Am J Respir Cell Mol Biol 1995;12:358-365.
40. Seitz M, Loetscher P, Dewald B, Towbin H, Ceska M, Baggiolini M. Production of interleukin-1 receptor antagonist, inflammatory chemotactic proteins, and prostaglandin E by rheumatoid and osteoarthritic synoviocytes-regulation by IFN-gamma and IL-4. J Immunol 1994;152:2060-2065.
41. 2 production by freshly prepared adherent rheumatoid synovial cells via inhibition of biosynthesis and gene expression of cyclo-oxygenase II but not of cyclooxygenase I. Ann Rheum Dis 1996;55:375-382.
42. Hayashi Y, Kobayashi M, Kuwata H, et al. Interferon-gamma and interleukin 4 inhibit interleukin 1 beta-induced delayed prostaglandin E(2) generation through suppression of cyclooxygenase-2 expression in human fibroblasts. Cytokine 2000;12:603-612.
43. Yamada H, Kikuchi T, Nemoto O, et al. Effects of indomethacin on the production of matrix metalloproteinase-3 and tissue inhibitor of metalloproteinases-1 by human articular chondrocytes. J Rheumatol 1996;23: 1739-1743.
44. 2 on the expression of MMPs in human periodontal ligament fibroblasts. J Periodont Res 2002;37:167-176.
45. 2 on recombinant equine interleukin-1-beta-stimulated matrix metalloproteinases 1, 3, and 13 and tissue inhibitor of matrix metalloproteinase 1 expression in equine chondrocyte cultures. Am J Vet Res 2002;63:987-993.
46. 2 selective enhancement of collagenase gene expression in human dermal fibroblasts in culture. J Cell Biochem 1994;54:465-472.
47. Domeij H, Yucel-Lindberg T, Modeer T. Signal pathways involved in the production of MMP-1 and MMP-3 in human gingival fibroblasts. Eur J Oral Sci 2002;110:302-306.
48. DiBattista JA, Pelletier JP, Zafarullah M, Fujimoto N, Obata K, Martel-Pelletier J. Coordinate regulation of matrix metalloproteinases and tissue inhibitor of metalloproteinase expression in human synovial fibroblasts. J Rheumatol 1995;43(Suppl.):123-128.
49. 1 inhibit cytokine-induced metalloprotease expression in human synovial fibroblasts. Mediation by cyclic-AMP signalling pathway. Lab Invest 1994;71:270-278.
50. Case JP, Lafyatis R, Kumkumian GK, Remmers EF, Wilder RL. IL-1 regulation of transin/stromelysin transcription in rheumatoid synovial fibroblasts appears to involve two antagonistic transduction pathways, an inhibitory, prostaglandin-dependent pathway mediated by cAMP, and a stimulatory, protein kinase C-dependent pathway. J Immunol 1990;145:3755-3761.
51. Buttice G, Quinones S, Kurkinen M. The AP-1 site is required for basal expression but is not necessary for TPA-response of the human stromelysin gene. Nucleic Acids Res 1991;19:3723-3731.
52. Quinones S, Buttice G, Kurkinen M. Promoter elements in the transcriptional activation of the human stromelysin-1 gene by the inflammatory cytokine, interleukin 1. Biochem J 1994;302:471-477.
53. Quinones S, Saus J, Otani Y, Harris ED Jr, Kurkinen M. Transcriptional regulation of human stromelysin. J Biol Chem 1989;264:8339-8344.
54. Sirum-Connolly K, Brinckerhoff CE. Interleukin-1 or phorbol induction of the stromelysin promoter requires an element that cooperates with AP-1. Nucleic Acids Res 1991;19:335-341.
55. Bond M, Baker AH, Newby AC. Nuclear factor kappa B activity is essential for matrix metalloproteinase-1 and -3 upregulation in rabbit dermal fibroblasts. Biochem Biophys Res Commun 1999;264:561-567.
56. Bond M, Chase AJ, Baker AH, Newby AC. Inhibition of transcription factor NF-kappa B reduces matrix metalloproteinase-1, -3 and -9 production by vascular smooth muscle cells. Cardiovasc Res 2001;50:556-565.
57. Chase AJ, Bond M, Crook MF, Newby AC. Role of nuclear factor-kappa B activation in metalloproteinase-1, -3, and -9 secretion by human macrophages in vitro and rabbit foam cells produced in vivo. Arterioscler Thromb Vasc Biol 2002;22:765-771.
58. Dokter WH, Esselink MT, Halie MR, Vellenga E. Interleukin-4 inhibits the lipopolysaccharide-induced expression of c-jun and c-fos messenger RNA and activator protein-1 binding activity in human monocytes. Blood 1993;81:337-343.
59. Dokter WHA, Koopmans SB, Vellenga E. Effects of IL-10 and IL-4 on LPS-induced transcription factors (AP-1, NF-IL6, and NF-kappa B) which are involved in IL-6 regulation. Leukemia 1996;10:1308-1316.
60. Donnelly RP, Crofford LJ, Freeman SL, et al. Tissue-specific regulation of IL-6 production by IL-4. Differential effects of IL-4 on nuclear factor-kappa B activity in monocytes and fibroblasts. J Immunol 1993;151:5603-5612.
61. Beppu M, Ikebe T, Shirasuna K. The inhibitory effects of immunosuppressive factors, dexamethasone and interleukin-4, on NF-kappa B-mediated protease production by oral cancer. Biochim. Biophys Acta 2002;1586: 11-22.
62. Abu-Amer Y. IL-4 abrogates osteoclastogenesis through STAT6-dependent inhibition of NF-kappa B. J Clin Invest 2001;107:1375-1385.
63. Wasylyk C, Gutman A, Nicholson R, Wasylyk B. The c-Ets oncoprotein activates the stromelysin promoter through the same elements as several non-nuclear oncoproteins. EMBO J 1991;10:1127-1134.
64. Borghaei RC, Sullivan C, Mochan E. Identification of a cytokine-induced repressor of interleukin-1 stimulated expression of stromelysin 1 (MMP-3). J Biol Chem 1999; 274:2126-2131.
65. Oriente A, Fedarko NS, Pacocha SE, Huang SK, Lichtenstein LM, Essayan DM. Interleukin-13 modulates collagen homeostasis in human skin and keloid fibroblasts. J Pharmacol Exp Ther 2000;292:988-994.
66. Suk K, Erickson KL. Differential regulation of tumour necrosis factor-alpha mRNA degradation in macrophages by interleukin-4 and interferon-gamma. Immunology 1996;87:551-558.
67. 2 synthesis blocks interstitial collagenase and 92-kDa type IV collagenase/gelatinase production by human monocytes. J Biol Chem 1992;267:515-519.
68. 2-dependent collagenase gene expression through their action on cyclooxygenase-2 and cytosolic phospholipase A2. Lab Invest 1996;75:529-538.
69. Vignon E, Mathieu P, Louisot P, Richard M. In vitro effect of nonsteroidal antiinflammatory drugs on proteoglycanase and collagenase activity in human osteoarthritic cartilage. Arthritis Rheum 1991;34:1332-1335.
70. Millward-Sadler SJ, Wright MO, Davies LW, Nuki G, Salter DM. Mechanotransduction via integrins and interleukin-4 results in altered aggrecan and matrix metalloproteinase 3 gene expression in normal, but not osteoarthritic, human articular chondrocytes. Arthritis Rheum 2000;43:2091-2099.
71. Salter DM, Millward-Sadler SJ, Nuki G, Wright MO. Differential responses of chondrocytes from normal and osteoarthritic human articular cartilage to mechanical stimulation. Biorheology 2002;39:97-108.
72. Orbak R, Tezel A, Canakci V, Demir T. The influence of smoking and non-insulin-dependent diabetes mellitus on periodontal disease. J Int Med Res 2002;30:116-125.
73. Poggi P, Rota MT, Boratto R. The volatile fraction of cigarette smoke induces alterations in the human gingival fibroblast cytoskeleton. J Periodont Res 2002;37:230-235.
74. Snyder HB, Caughman G, Lewis J, Billman MA, Schuster G. Nicotine modulation of in vitro human gingival fibroblast beta 1 integrin expression. J Periodontol 2002;73:505-510.
75. Schmidt AM, Weidman E, Lalla E, et al. Advanced glycation endproducts (AGEs) induce oxidant stress in the gingiva: A potential mechanism underlying accelerated periodontal disease associated with diabetes. J Periodont Res 1996;31:508-515.
76. Takane M, Sugano N, Iwasaki H, Iwano Y, Shimizu N, Ito K. New biomarker evidence of oxidative DNA damage in whole saliva from clinically healthy and periodontally diseased individuals. J Periodontol 2002;73:551-554.
77. Yin L, Morita A, Tsuji T. Alterations of extracellular matrix induced by tobacco smoke extract. Arch Dermatol Res 2000;292:188-194.
78. Han Z, Boyle DL, Manning AM, Firestein GS. AP-1 and NF-kappa B regulation in rheumatoid arthritis and murine collagen-induced arthritis. Autoimmunity 1998; 28:197-208.
79. Asahara H, Fujisawa K, Kobata T, et al. Direct evidence of high DNA binding activity of transcription factor AP-1 in rheumatoid arthritis synovium. Arthritis Rheum 1997;40:912-918.
80. Mikita T, Campbell D, Wu P, Williamson K, Schindler U. Requirements for interleukin-4-induced gene expression and functional characterization of Stat6. Mol Cell Biol 1996;16:5811-5820.
81. Muller-Ladner U, Judex M, Ballhorn W, et al. Activation of the IL-4 STAT pathway in rheumatoid synovium. J Immunol 2000; 164:3894-3901.
82. Gingras S, Simard J, Groner B, Pfitzner E. p300/CBP is required for transcriptional induction by interleukin-4 and interacts with Stat6. Nucleic Acids Res 1999;27: 2722-2729.
83. Delerive P, De Bosscher K, Besnard S, et al. Peroxisome proliferator-activated receptor alpha negatively regulates the vascular inflammatory gene response by negative cross-talk with transcription factors NF-kappa B and AP-1. J Biol Chem 1999;274:32048-32054.
84. Horvai AE, Xu L, Korzus E, et al. Nuclear integration of JAK/STAT and Ras/AP-1 signaling by CBP and p300. Proc Natl Acad Sci (USA) 1997;94:1074-1079.
85. Jayaraman G, Srinivas R, Duggan C, et al. p300/cAMP-responsive element-binding protein interactions with ets-1 and ets-2 in the transcriptional activation of the human stromelysin promoter. J Biol Chem 1999;274: 17342-17352.
86. Smits PHM, de Wit L, van der Eb AJ, Zantema A. The adenovirus E1A-associated 300 kDa adaptor protein counteracts the inhibition of the collagenase promoter by E1A and represses transformation. Oncogene 1996; 12:1529-1535.
87. Sheppard KA, Rose DW, Haque ZK, et al. Transcriptional activation by NF-kappa B requires multiple coactivators. Mol Cell Biol 1999;19:6367-6378.
88. Yang C, Shapiro LH, Rivera M, Kumar A, Brindle PK. A role for CREB binding protein and p300 transcriptional coactivators in Ets-1 transactivation functions. Mol Cell Biol 1998;18:2218-2229.
89. Wadgaonkar R, Phelps KM, Haque Z, Williams AJ, Silverman ES, Collins T. CREB-binding protein is a nuclear integrator of nuclear factor-kappaB and p53 signaling. J Biol Chem 1999;274:1879-1882.