Influence of LPS, TNF, TGF-β1 and IL-4 on the expression of MMPs, TIMPs and selected cytokines in rat synovial membranes incubated in vitro

International Journal of Molecular Medicine

Volumn 27, Issue 1, 2011, Pages 127-137

  Hyc, Anna ^a   Osiecka Iwan, Anna ^a   Niderla Bielinska, Justyna ^a   Moskalewski, Stanislaw ^a  

^a MEDICAL UNIVERSITY OF WARSAW   (Poland)

Author keywords

Cytokines; Interleukin; Lipopolysaccharide; Metalloproteinases; Synovial membrane; Tissue inhibitors of metalloproteinases; Transforming growth factor ; Tumor necrosis factor

Indexed keywords

COLLAGENASE 3; CYTOKINE; GELATINASE A; GELATINASE B; INTERLEUKIN 1BETA; INTERLEUKIN 4; INTERLEUKIN 6; INTERSTITIAL COLLAGENASE; LIPOPOLYSACCHARIDE; MATRIX METALLOPROTEINASE 14; MESSENGER RNA; STROMELYSIN; TISSUE INHIBITOR OF METALLOPROTEINASE; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TISSUE INHIBITOR OF METALLOPROTEINASE 2; TISSUE INHIBITOR OF METALLOPROTEINASE 3; TISSUE INHIBITOR OF METALLOPROTEINASE 4; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BETA RHYTHM; CELL POPULATION; CONTROLLED STUDY; IN VITRO STUDY; INDIVIDUALIZATION; KNEE; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SYNOVIUM; ZYMOGRAPHY;

ANIMALS; CELLS, CULTURED; CYTOKINES; INTERLEUKIN-4; LIPOPOLYSACCHARIDES; MALE; MATRIX METALLOPROTEINASES; PROTEIN ISOFORMS; RATS; RATS, INBRED LEW; SYNOVIAL MEMBRANE; TISSUE INHIBITOR OF METALLOPROTEINASES; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR-ALPHA;

EID: 78651255877     PISSN: 11073756     EISSN: 1791244X     Source Type: Journal    
DOI: 10.3892/ijmm.2010.550     Document Type: Article

References (114)

1. Gardner E, Gray DJ and O'Rahilly R: Joints. In: Anatomy. WB Saunders Company (ed), Philadelphia, London, p25, 1960.
2. Levick JR, Price FM and Mason RM: Synovial matrix-synovial fluid system of joints. In: Extracellular Matrix. Vol 1. Comper WD (ed). Harwood Academic Publishers, Amsterdam, pp328-376, 1996.
3. Wilkinson LS, Pitsillides AA, Worrall JG and Edwards JCW: Light microscopic characterization of the fibroblast-like synovial intimal cell (synoviocyte). Arthritis Rheum 35: 1179-1184, 1992.
4. Barland P, Novikoff AB and Hamerman D: Electron microscopy of the human synovial membrane. J Cell Biol 14: 207-215, 1962.
5. Henderson B: The synovial lining cell and synovitis. Scand J Rheumatol 17 (Suppl. 76): S33-S38, 1988.
6. Revell PA, al-Saffar N, Fish S and Osei D: Extracellular matrix of the synovial intimal cell layer. Ann Rheum Dis 54: 404-407, 1995.
7. + cells from synovium-rich tissues of normal rats: phenotype, comparison with macrophage and dendritic cell lineages and differentiation into mature dendritic cells in vitro. Int Immunol 17: 1103-1115, 2005.
8. Moghaddami M, Mayrhofer G and Celland LG: MHC class II compartment, endocytosis and phagocytic activity of macrophages and putative dendritic cells isolated from normal tissues rich in synovium. Int Immunol 17: 1117-1130, 2005.
9. Nozawa-Inoue K, Amizuka N, Ikeda N, Suzuki A, Kawano Y and Maeda T: Synovial membrane in the temporomandibular joint - its morphology, function and development. Arch Histol Cytol 66: 289-306, 2003.
10. Klareskog L, Forsum U, Kabelitz D, Plöen L, Sundström C, Nillson K, Wigren A and Wigzell H: Immune functions of synovial cells: phenotyppic and T cell regulatory properties of macrophage-like cells that express HLA-DR. Arthritis Rheum 25: 488-501, 1982.
11. Dijkstra CD, Dopp EA, Vogels IM and Van Noorden CJF: Macrophages and dendritic cells in antigen-induced arthritis. Scand J Immunol 26: 513-523, 1987.
12. Kakudo K, Takasu J and Yamamoto Y: Ultrastructural observations of horseradish peroxidase in synovial lining cells of the rats' temporomandibular joint. J Dent Res 56: 1376, 1977.
13. Senda H, Sakuma E, Wada I, Wang HJ, Maruyama H and Matsui N: Ultrastructural study of cells at the synovium-cartilage junction: response of synovial cells of the rat knee to intra-articularly injected latex particles. Kaibogaku Zasshi 74: 525-535, 1999.
14. Linck G and Porte A: Cytophysiology of the synovial membrane: distinction of two types of cells of the intima revealed by their reaction with horseradish peroxidase and iron saccharate in the mouse. Biol Cell 42: 147-152, 1981.
15. Okada Y, Nakanishi I and Kajikawa K: Ultrastructure of the mouse synovial membrane. Development and organization of the extracellular matrix. Arthitis Rheum 24: 835-843, 1981.
16. Graabæk PM: Absorption of intraarticularly injected horseradish peroxidase in synoviocytes of rat synovial membrane: an ultrastructural- cytochemical study. J Ultrastruct Res 92: 86-100, 1985.
17. Stuhlmeier KM and Pollaschek CP: Differential effect of transforming growth factor β (TGF-β1) on the genes encoding hyaluronan synthases and utilization of the p38 MAPK pathway in TGF-β1-induced hyaluronan synthase 1 activation. J Biol Chem 279: 8753-8760, 2004.
18. Stuhlmeier KM and Pollaschek CP: Adenovirus-mediated gene transfer of mutated IκB kinase and IκBa reveal NF-κB dependent as well as NF-κB-independent pathways of HAS1 activation. J Biol Chem 280: 42766-42773, 2005.
19. Worrall JG, Bayliss MT and Edwards JCW: Morphological localization of hyaluronan in normal and diseased synovium. J Rheumatol 18: 1466-1472, 1991.
20. Anggiansah CL, Scott D, Poli A, Coleman PJ, Badrick E, Mason RM and Levick JR: Regulation of hyaluronan secretion into rabbit synovial joints in vitro by protein kinase C. J Physiol 550: 631-640, 2003.
21. Swann DA: Structure and function of lubricin, the glycoprotein responsible for the boundary lubrication of articular cartilage. In: Articular Synovium. Franchimont P and Karger S (eds). Basel, pp45-58, 1982.
22. Edwards JCW: Fibroblast biology: Development and differentiation of synovial fibroblasts in arthritis. Arthritis Res 2: 344-347, 2000.
23. Mapp PI and Revel PA: Fibronectin production by synovial intimal cells. Rheumatol Int 5: 229-237, 1985.
24. Nozawa-Inoue K, Ajima H, Takagi R and Maeda T: Immunocytochemical demonstration of laminin in the synovial lining layer of the rat temporomandibular joint. Arch Histol Cytol 44: 531-534, 1999. (Pubitemid 29264474)
25. Wilkinson LS, Edwards JCW, Poston RN and Haskard DO: Expression of vascular cell adhesion molecule-1 in normal and inflamed synovium. Lab Invest 68: 82-88, 1993.
26. Valentia X, Higgins JM, Kiener HP, Lee DM, Podrebarac TA, Dascher CC, Watts GF, Mizoguchi E, Simmons B, Patel DD, Bhan AK and Brenner MB: Cadherin-11 provides specific cellular adhesion between fibroblast-like synoviocytes. J Exp Med 200: 1673-1679, 2004.
27. Andoh E, Kawano Y, Ajima H, Nozawa-Inoue K, Kohno S and Maeda T: Expression of 25 kDa heat shock protein by synovial type B cells of the mouse temporomandibulat joint. Arch Oral Biol 46: 947-954, 2001.
28. Nozawa-Inoue K, Oshima H, Kawano Y, Yamamoto H, Takagi R and Maeda T: Immunocytochemical demonstration of heat shock protein 25 in the rat temporomandibular joint. Arch Histol Cytol 62: 483-491, 1999. (Pubitemid 30095575)
29. Shikichi M, Kitamura HP, Yanase H, Konno A, Takahashi-Iwanaga H and Iwanaga T: Three-dimentional ultrastructure of synoviocytes in the horse joint as revealed by the scanning electron microscope. Arch Histol Cytol 62: 219-229, 1999.
30. Iwanaga T, Shikichi M, Kitamura H, Yanase H and Nozawa-Inoue K: Morphology and functional roles of synoviocytes in the joint. Arch Histol Cytol 63: 17-31, 2000.
31. Huber LC, Distler O, Tarner I, Gay RE, Gay S and Pap T: Synovial fibroblasts: key players in rheumatoid arthritis. Rheumatology 45: 669-675, 2006.
32. Kinne RW, Stuhlmüller B and Burmester GR: Cells of the synovium in rheumatoid arthritis. Macrophages. Arthritis Res Ther 9: 224, 2007.
33. Bondeson J, Wainwright SD, Lauder S, Amos N and Hughes CE: The role of synovial macrophages and macrophage-produced cytokines in driving aggrecanases, matrix metalloproteinases, and other destructive and inflammatory responses in osteoarthritis. Arthritis Res Ther 8: R187, 2006.
34. Schwachula A, Riemann D, Kehlen A and Langner J: Characterization of the immunophenotype and functional properties of fibroblast-like synoviocytes in comparison to skin fibroblasts and umbilical vein endothelial cells. Immunobiology 190: 67-92, 1994.
35. Sweet MJ and Hume DA: CSF-1 as a regulator of macrophage activation and immune responses. Arch Immunol Ther Exp 51: 169-177, 2003.
36. Galley HF and Webster NR: Physiology of the endothelium. Br J Anaesth 93: 105-113, 2004.
37. Kern PA, Saghizadeh M, Ong JM, Bosch RJ, Deem R and Sinsolo RB: The expression of tumor necrosis factor in human adipose tissue. J Clin Invest 95: 2111-2119, 1995.
38. Dumond H, Presle N, Terlain B, Mainard D, Loeuille D, Netter P and Pottie P: Evidence for a key role of leptin in osteoarthritis. Arthritis Rheum 48: 3118-3129, 2003.
39. Ehling A, Schäffler A, Herfarth H, Tarner IH, Anders S, Distler O, Paul G, Distler J, Gay S, Schölmerich J, Neumann E and Müller-Ladner U: The potential of adiponectin in driving arthritis. J Immunol 176: 4468-4478, 2006.
40. Mohamed-Ali V, Goodrick S, Ravesh A, Katz DR, Miles JM, Yudkin JS, Klein S and Coppack SW: Subcutaneous adipose tissue releases interleukin-6, but not tumor necrosis factor - in vivo. J Clin Endocrinol Metab 82: 4196-4200, 1997.
41. Hyc A, Osiecka-Iwan A, Niderla-Bielinska J, Jankowska-Steifer E and Moskalewski S: Pro- and anti-inflammatory cytokines increase hyaluronan production by rat synovial membrane in vitro. Int J Mol Med 24: 579-585, 2009.
42. Hyc A, Osiecka-Iwan A and Moskalewski S: Preparation of rat synovial membrane for studies of cytokine secretion. Folia Histochem Cytobiol 45: 57-60, 2007.
43. Scotté M, Hiron M, Masson S, Lyoumi S, Banine F, Téniére P, Lebreton JP and Daveau M: Differential expression of cytokine genes in monocytes, peritoneal macrophages and liver following endotoxin- or turpentine-induced inflammation in rat. Cytokine 8: 115-120, 1996.
44. Fiorentino DF, Zlotnik A, Mosmann TR, Howard M and O'Garra A: IL-10 inhibits cytokine production by activated macrophages. J Immunol 147: 3815-3822, 1991.
45. Mukherjee S, Chen L-Y, Papadimos TJ, Huang S, Zuraw BL and Pan ZK: Lipopolisaccharide driven Th2 cytokine production in macrophages is regulated by both MyD88 and TRAM. J Biol Chem 284: 29391-29398, 2009.
46. Hofman C, Lorenz K, Braithwaite SS, Colca JR, Palazuk BJ, Hotamisligil GS and Spiegelman BM: Altered gene expression for tumor necrosis factor-alpha and its receptors during drug and dietary modulation of insulin resistance. Endocrinology 134: 264-270, 1994.
47. Distel E, Cadoudal T, Durant S, Poignard A, Chevalier X and Benelli C: The intrapatellar fat pad in knee osteoarthritis. An important source of interleukin-6 and its soluble receptor. Arthritis Rheum 60: 3374-3377, 2009.
48. Hoch M, Eberle AN, Peterli R, Peters T, Seboek D, Keller U, Muller B and Linscheid P: LPS induces interleukin-6 and interleukin-8 but not tumor necrosis factor-α in human adipocytes. Cytokine 41: 29-37, 2008.
49. Moskalewski S, Osiecka-Iwan A, Hyc A and Niderla J: Cartilage formed by syngeneic rat chondrocytes in joint surface defects is rejected in animals sensitized with allogeneic chondrocytes: involvement of the synovial lining. Arch Immunol Ther Exp 53: 159-168, 2005.
50. Xing Z, Jordana M, Kirpalani H, Driscoll KE, Schall TJ and Gauldie J: Cytokine expression by neutrophils and macrophages in vivo: endotoxin induces tumor necrosis factor-alpha, macrophage inflammatory protein-2, interleukin-1 beta, and interleukin-6 but not RANTES or transforming growth factor-beta 1 mRNA expression in acute lung inflammation. Am J Respir Cell Mol Biol 10: 148-153, 1994.
51. Jirik FR, Podor TJ, Hirano T, Kishimoto T, Loskutoff DJ, Carson DA and Lotz M: Bacterial lipopolysaccharides and inflammatoty mediators augment IL-6 secretion by human endothelial cells. J Immunol 142: 144-147, 1989.
52. Santangelo KS, Johnson AL, Ruppert AS and Bertone AL: Effects of hyaluronan treatment on lipopolysaccharide-challenged fibroblast-like synovial cells. Arthtitis Res Ther 9: R1, 2007.
53. Batista ML Jr, Santos RV, Cunha LM, Mattos K, Oliveira EM, Seelaender MC and Costa Rosa LF: Changes in the proinflammatory cytokine production and peritoneal macrophage function in rats with chronic heart failure. Cytokine 34: 284-290, 2006.
54. Suttles J, Giri JG and Mizel SB: IL-1 secretion by macrophages. Enhancement of IL-1 secretion and processing by calcium jonofores. J Immunol 144: 175-182, 1990. (Pubitemid 20030473)
55. Dayer JM: The process of identifying and understanding cytokines: from basic studies to treating rheumatic diseases. Best Pract Res Clin Rheumatol 18: 31-45, 2004.
56. Pober JS and Cotran RS: Cytokines and endothelial cell biology. Physiol Rev 70: 427-451, 1990.
57. Fain JN: Release of interleukins and other inflammatory cytokines by human adipose tissue is enhanced in obesity and primarily due to the nonfat cells. Vitam Horm 74: 443-447, 2006.
58. Kuruvilla L and Kartha CC: Treatment with TNF-α or bacterial lipopolisaccharide attenuates endocardial endothelial cell-mediated stimulation of cardiac fibroblasts. J Biomed Sci 16: 21: 16-21, 2009.
59. Lee HC, Vinodhumar R, Yoon JW, Park SK, Lee CW and Kim HY: Enhanced inhibitory effect of ultra-fine granules of red ginseng on LPS-induced cytokine expression in the monocyte-derived macrophage THP-1 cells. Int J Mol Sci 9: 1379-1392, 2008.
60. Bauer J, Ganter U, Geiger T, Jacobshagen U, Hirano T, Matsuda T, Kishimoto T, Andus T, Acs G, Gerok W and Ciliberto G: Regulation of interleukin-6 expression in cultured human blood monocytes and monocyte-derived macrophages. Blood 72: 1134-1140, 1988.
61. Elias JA and Lentz V: IL-1 and tumor necrosis factor synergistically stimulate fibroblast IL-16 production and stabilize IL-6 messenger RNA. J Immunol 145: 161-166, 1990.
62. Eickelberg O, Pansky A, Mussmann R, Bihl M, Tamm M, Hikdebrand P, Perruchoud AP and Roth M: Transforming growth factor-β1 induces interleukin-6 expression via activating protein-1 consisting of Jun D homodimers in primary human lung fibroblasts J Biol Chem 274: 12933-12938, 1999.
63. Seong GJ, Hong S, Jung S-A, Lee J-J, Lim E, Kim S-J and Lee JH: TGF-beta-induced interleukin-6 participates in transdifferentiation of human Tenon's fibroblasts to myofibroblasts. Mol Vis 15: 2123-2128, 2009.
64. Turner M, Chantry D and Feldmann M: Transforming growth factor β induces the production of interleukin 6 by human peripheral blood mononuclear cells. Cytokine 2: 211-216, 1990.
65. Musso T, Espinoza-Delgado I, Pulkki K, Gusella GL, Longo DL and Varesio L: IL-2 induces IL-6 production in human monocytes. J Immunol 148: 795-800, 1992.
66. Espevik T, Figari IS, Shalaby MR, Lackides GA, Lewis GD, Shepard HM and Palladino MA Jr: Inhibition of cytokine production by cyclosporin A and transforming growth factor β. J Exp Med 166: 571-576, 1987.
67. Bogdan C and Nathan C: Modulation of macrophage function by transforming growth factor β, interleukin-4, and interleukin 10. Ann NY Acad Sci 23: 713-739, 1993. (Pubitemid 23238554)
68. Bogdan C, Paik J, Vodovots Y and Nathan C: Contrasting mechanisms for suppression of macrophage cytokine release by transforming growth factor-β and interleukin-10. J Biol Chem 267: 23301-23308, 1992.
69. Turner M, Chantry D, Katsikis P, Berge A, Brenna FM and Feldmann M: Induction of interleukin 1 receptor antagonist protein by transforming growth factor-β. Eur J Immunol 21: 1635-1639, 1991.
70. Chantry D, Turner M, Abney E and Feldmann M: Modulation of cytokine production by transforming growth factor-β. J Immunol 142: 4295-4300, 1989.
71. Piek E, Ju WJ, Heyer J, Escalante-Alcadle D, Steward CL, Weinstein M, Deng C, Kucherlapati R, Böttinger EP and Roberts A: Functional characterization of transforming growth factor b signaling in Smad2- and Smad3- deficient fibroblasts. J Biol Chem 276: 19945-19953, 2001.
72. Kim S-J, Angel P, Lafyatis R, Hattori K, Kim KY, Sporn MB, Karin M and Roberts AB: Autoinduction of transforming growth factor β1 is mediated by the AP-1 complex. Mol Cell Biol 10: 1492-1497, 1990. (Pubitemid 120004750)
73. Van Obberghen-Schilling E, Roche NS, Flanders KC, Sporn MB and Roberts AB: Transforming growth factor β1 positively regulates its own expression in normal and transformed cells. J Biol Chem 263: 7741-7746, 1988.
74. Donnelly RP, Crofford LJ, Freeman SL, Buras J, Remmers E, Wilder RL and Fenton MJ: Tissue specific regulation of IL-6 production by IL-4. Differential effects of IL-4 on nuclear factor-κB activity in monocytes and fibroblasts. J Immunol 151: 5603-5612, 1993.
75. Lacraz S, Nicod L, Galve-de Rochemonteix B, Baumberger C, Dayer J-M and Welgus HG: Suppression of metalloproteinase biosynthesis in human alveolar macrophages by interleukin-4. J Clin Invest 90: 382-388, 1992.
76. Colotta F, Sironi M, Borrè A, Luini W, Maddalena F and Mantovani A: Interleukin 4 amplifies monocyte chemotactic protein and interleukin 6 production by endothelial cells. Cytokine 4: 24-28, 1992.
77. Howell G, Pham P, Taylor D, Foxwell B and Feldman M: Interleukin 4 induces interleukin 6 production by endothelial cells; synergy with interferon-γ. Eur J Immunol 21: 97-101, 1991.
78. Te Velde AA, Huijbens RJ, Heije K, de Vries JE and Figdor CG: Interleukin-4 (IL-4) inhibits secretion of IL-1 beta, tumor necrosis factor alpha, and IL-6 by human monocytes. Blood 76: 1392-1397, 1990.
79. Okada Y, Morodomi T, Enghild JJ, Suzuki K, Yasui A, Nakanishi I, Salvesen G and Nagase H: Matrix metalloproteinase 2 from human rheumatoid synovial fibroblasts. Purification and activation of the precursor and enzymic properties. Eur J Biochem 194: 721-730, 1990.
80. Ohuchi E, Imai K, Fujii Y, Sato H, Seiki M and Okada Y: Membrane type 1 matrix metalloproteinase digests interstitial collagens and other extracellular matrix macromolecules. J Biol Chem 272: 2446-2451, 1997. (Pubitemid 27058534)
81. Chang Y-C, Yang S-F, Lai C-C, Liu J-Y and Hsieh Y-S: Regulation of matrix metalloproteinase production by cytokines, pharmacological agents and periodontal pathogens in human periodontal ligament fibroblast cultures. J Periodontal Res 37: 196-203, 2002.
82. Clegg PD and Carter SD: Matrix metalloproteinase-2 and -9 are activated in joint disease. Equine Vet J 31: 324-330, 1999.
83. Welgus HG, Campbell EJ, Cury JD, Eisen AZ, Senior RM Wilhelm SM and Goldberg GI: Neutral metalloproteinases produced by human mononuclear phagocytes. J Clin Invest 86: 1494-1502, 1990.
84. Lamoreaux WJ, Fitzgerald MEC, Reiner A, Hasty KA and Charles ST: Vascular endothelial growth factor increases release of gelatinase A and decreases release of tissue inhibitor of metalloproteinases by microvascular endothelial cell in vitro. Microvasc Res 55: 29-42, 1998.
85. Taraboletti G, D'Ascenzo S, Borsotti P, Giavazzi R, Pavan A and Dolo V: Shedding of matrix metalloproteinases MMP2, MMP9, and MT1/MMP as membrane vesicle-associated components by endothelial cells. Am J Pathol 160: 673-680, 2002.
86. Puyraimond A, Weitzman JB, Babiole E and Menashi S: Examining the relationship between the gelatinolytic balance and the invasive capacity of endothelial cells. J Cell Sci 112: 1283-1290, 1999.
87. Kim HG and Koh GY: Lipopolysaccharide activates matrix metalloproteinase-2 in endothelial cells through an NF-κB-dependent pathway. Biochem Biophys Res Comm 269: 401-405, 2000.
88. Moon H-S, Lee H-G, Seo J-H, Chung C-S, Guo D-D, Kim T-G, Choi Y-J and Cho C-S: Leptin induced matrix metalloproteinase-2 secretion is suppressed by trans-1-,cis-12 conjugated linoleic acid. Biochem Biophys Res Comm 356: 955-960, 2007.
89. Atkinson JJ and Senior RM: Matrix metalloproteinase-9 in lung remodelling. Am J Respir Cell Mol Biol 28: 12-24, 2003.
90. Goldberg GI, Strongin A, Collier IE, Genrich LT and Marmer BL: Interaction of 92-kDa type IV collagenase with the tissue inhibitor of metalloproteinases prevents dimerization, complex formation with interstitoal collagenase, and activation of the proenzyme with stromelysin. J Biol Chem 267: 4583-4591, 1992.
91. Shapiro SD, Fliszar CJ, Broekelmann TJ, Mecham RP, Senior RM and Welgus HG: Activation of the 92-kDa gelatinase by stromelysin and 4-aminophenylmercuric acetate. J Biol Chem 270: 6351-6356, 1995.
92. Sarén P, Welgus HG and Kovanen PT: TNF-α and IL-1β selectively induce expression of 92-kDa gelatinase by human macrophages. J Immunol 157: 4159-4165, 1996.
93. Zhang Y, McCluskey K, Fujii K and Wahl LM: Differential regulation of monocyte matrix metalloprotease and TIMP1 production by TNF-α, granulocyte-macrophage CSF, and IL-1β through prostaglandin-dependent mechanism. J Immunol 61: 3071-3076, 1998.
94. Lepidi S, Kenagy RD, Raines EW, Chiu ES, Chair A, Ross R and Clowes A: MMP9 production by human monocyte-derived macrophages is decreased on polymerized type I collagen. J Vasc Surg 34: 1111-1118, 2001.
95. Partridge CA, Jeffrey JJ and Malik AB: A 96-kDa gelatinase induced by TNF-alpha contributes to increased microvascular endothelial permeability. Am J Physiol 265: L438-L447, 1993.
96. O'Hara A, Lim F-L, Mazzatti DJ and Trayhurn P: Microarray analysis identifies matrix metalloproteinases (MMPs) as the genes whose expression is up-regulated in human adipocytes by macrophage-conditioned medium. Pflugers Arch 458: 1103-1114, 2009.
97. Cawston TE: Proteinases and inhibitors. Br Med Bull 51: 385-401, 1995.
98. Baker AH, Edwarda DR and Murphy G: Metalloproteinase inhibitors: biological action and therapeutic opportunities. J Cell Sci 115: 3719-3727, 2002.
99. Balbin M, Fueyo A, Knäuper V, López JM, Álvarez J, Sánchez LM, Quesada V, Bordallo J, Murphy M and López-Otín C: Identification and enzymatic characterization of two diverging murine counterparts of human interstitial collagenase (MMP-1) expressed at sites of embryo implantation. J Biol Chem 276: 10253-10262, 2001.
100. Pearse E, Tregouet D-A, Samnegård A, Morgan AR, Cox C, Hamsten A, Eriksson P and Ye S: Haplotype effect of the matrix metalloproteinase-1 gene on risk of myocardial infarction. Circ Res 97: 1070-1076, 2005. (Pubitemid 41668921)
101. Stricklin GP, Bauer EA, Jeffrey JJ and Eisen AZ: Human skin collagenase: isolation of precursor and active forms from both fibroblasts and organ cultures. Biochemistry 16: 1607-1615, 1977.
102. Suzuki K, Enghild JJ, Morodomi T, Salvesen G and Nagase H: Mechanisms of activation of tissue procollagenase by matrix metalloproteinase 3 (stromelysin). Biochemistry 29: 10261-10270, 1990. (Pubitemid 20384533)
103. Dayer J-M, Beutler B and Cerami A: Cachectin/tumor necrosis factor stimulates collagenase and prostaglandin E2 production by human synovial cells and dermal fibroblasts. J Exp Med 162: 2163-2168, 1985.
104. Cury JD, Campbell EJ, Lazarus CJ, Albin RJ and Welgus HG: Selective up-regulation of human alveolar macrophage collagenase production by liposaccharide and comparison to collagenase production by fibroblasts. J Immunol 141: 4306-4312, 1988.
105. Nelimarkka LO, Nikkari ST, Ravanti LS, Kähäri VM and Järveläinen HT: Collagenase-1, stromelysin-1 and 92 kDa gelatinase are associated with tumor necrosis factor-alpha induced morphological change of human endothelial cells in vitro. Matrix Biol 17: 293-304, 1998.
106. Bujor AM, Pannu J, Bu S, Smith EA, Muise-Helmericks RC and Trojanowska M: Akt blockade downregulates collagen and upregulates MMP1 in human dermal fibroblasts. J Invest Dermatol 128: 1906-1914, 2008.
107. Awad AE, Kandalan V, Chakrabarti S, Wang X, Penninger JM, Davidge ST, Oudit GY and Kassiri Z: Tumor necrosis factor induces matrix metalloproteinases in cardiomyocytes and cardiofibroblasts differentially via superoxide production in a P13K {gamma}-dependent manner. Am J Physiol Cell Physiol 298: 679-692, 2010.
108. Rossa C Jr, Min L, Bronson P and Kirkwood KL: Transcriptional activation of MMP13 by periodontal pathogenic LPS requires p38 MAP kinase. J Endotoxin Res 13: 85-93, 2007.
109. Rossa C Jr, Liu M, Patil C and Kirkwood KL: MKK3/6-p38 MAKP negatively regulates murine MMP13 gene expression induced by IL-1 beta and TNF-alpha in immortalized periodontal ligament fibroblasts. Matrix Biol 7: 478-488, 2005.
110. Gomez DE, Alonso DF, Yoshiji H and Thorgeirsson UP: Tissue inhibitors of metalloproteinases: structure, regulation and biological functions. Eur J Cell Biol 74: 111-112, 1997.
111. Dasu MR, Barrow RE, Spies M and Herndon DN: Matrix metalloproteinase expression in cytokine stimulated dermal fibroblasts. Burns 29: 527-531, 2003.
112. Ihn H, Yamane K, Asano Y, Kubo M and Tamaki K: IL-4 upregulates the expression of tissue inhibitor of metalloproteinase-2 in dermal fibroblasts via the p38 mitogenactivated protein kinase-dependent pathway. J Immunol 168: 1895-1902, 2002.
113. Gatsios P, Haubeck HD, Van de Leur E, Frisch W, Apte SS, Greiling H, Heinrich OC and Graeve L: Oncostatin M differentially regulates tissue inhibitors of metalloproteinases TIMP1 and TIMP3 gene expression in human synovial lining cells. Eur J Biochem 24: 56-63, 1996.
114. Leco KJ, Khokha R, Pavloff N, Hawkes SP and Edwards DR: Tissue inhibitor of metalloproteinases 3 (TIMP3) is an extracellular matrix-associated protein with a distinctive pattern of expression in mouse cells and tissues. J Biol Chem 269: 9352-9360, 1994.