Retinoblastoma Suppression of Matrix Metalloproteinase 1, but Not Interleukin-6, Through a p38-Dependent Pathway in Rheumatoid Arthritis Synovial Fibroblasts

Arthritis and Rheumatism

Volumn 50, Issue 1, 2004, Pages 78-87

  Bradley, Kathleen ^a   Scatizzi, John C ^a   Fiore, Stefano ^b   Shamiyeh, Eli ^c   Koch, Alisa E ^c   Firestein, Gary S ^d   Gorges, Laura L ^a   Kuntsman, Kevin ^c   Pope, Richard M ^c   Moore, Terry L ^a   Han, Jiahuai ^e   Perlman, Harris ^a  

^a SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF ILLINOIS   (United States)

^c NORTHWESTERN UNIVERSITY   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GALACTOSIDASE; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERSTITIAL COLLAGENASE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; RETINOBLASTOMA PROTEIN; UNCLASSIFIED DRUG;

ADENOVIRUS; ARTICLE; BONE DESTRUCTION; CARTILAGE DEGENERATION; CELL CYCLE; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME PHOSPHORYLATION; ENZYME RELEASE; ENZYME REPRESSION; FIBROBLAST; FLOW CYTOMETRY; GENE EXPRESSION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; INFLAMMATION; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; REGULATORY MECHANISM; RHEUMATOID ARTHRITIS; STEADY STATE; SYNOVIUM; TUMOR SUPPRESSOR GENE;

ADENOVIRIDAE; ARTHRITIS, RHEUMATOID; CELL CYCLE; CELLS, CULTURED; FIBROBLASTS; GENE EXPRESSION; HUMANS; INTERLEUKIN-6; MATRIX METALLOPROTEINASE 1; MITOGEN-ACTIVATED PROTEIN KINASES; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; RETINOBLASTOMA PROTEIN; RNA, MESSENGER; SYNOVIAL MEMBRANE;

EID: 9144231962     PISSN: 00043591     EISSN: None     Source Type: Journal    
DOI: 10.1002/art.11482     Document Type: Article

References (80)

1. Firestein GS. Invasive fibroblast-like synoviocytes in rheumatoid arthritis: passive responders or transformed aggressors? Arthritis Rheum 1996;39:1781-90.
2. Hashimoto S, Ochs RL, Komiya S, Lotz M. Linkage of chondrocyte apoptosis and cartilage degradation in human osteoarthritis. Arthritis Rheum 1998;41:1632-8.
3. Feldmann M, Brennan FM, Maini RN. Role of cytokines in rheumatoid arthritis. Annu Rev Immunol 1996;14:397-440.
4. Okamoto H, Yamamura M, Morita Y, Harada S, Makino H, Ota Z. The synovial expression and serum levels of interleukin-6, interleukin-11, leukemia inhibitory factor, and oncostatin M in rheumatoid arthritis. Arthritis Rheum 1997;40:1096-105.
5. Houssiau FA, Devogelaer JP, van Damme J, de Deuxchaisnes CN, van Snick J. Interleukin-6 in synovial fluid and serum of patients with rheumatoid arthritis and other inflammatory arthritides. Arthritis Rheum 1988;31:784-8.
6. Cunnane G, Fitzgerald O, Beeton C, Cawston TE, Bresnihan B. Early joint erosions and serum levels of matrix metalloproteinase 1, matrix metalloproteinase 3, and tissue inhibitor of metalloproteinases 1 in rheumatoid arthritis. Arthritis Rheum 2001;44: 2263-74.
7. Maeda S, Sawai T, Uzuki M, Takahashi Y, Omoto H, Seki M, et al. Determination of interstitial collagenase (MMP-1) in patients with rheumatoid arthritis. Ann Rheum Dis 1995;54:970-5.
8. Ohshima S, Saeki Y, Mima T, Sasai M, Nishioka K, Nomura S, et al. Interleukin 6 plays a key role in the development of antigen-induced arthritis. Proc Natl Acad Sci U S A 1998;95:8222-6.
9. Sasai M, Saeki Y, Ohshima S, Nishioka K, Mima T, Tanaka T, et al. Delayed onset and reduced severity of collagen-induced arthritis in interleukin-6-deficient mice. Arthritis Rheum 1999;42: 1635-43.
10. Boe A, Baiocchi M, Carbonatto M, Papoian R, Serlupi-Crescenzi O. Interleukin 6 knock-out mice are resistant to antigen-induced experimental arthritis. Cytokine 1999;11:1057-64.
11. Alonzi T, Fattori E, Lazzaro D, Costa P, Probert L, Kollias G, et al. Interleukin 6 is required for the development of collagen-induced arthritis. J Exp Med 1998;187:461-8.
12. Van Meurs J, van Lent P, Holthuysen A, Lambrou D, Bayne E, Singer I, et al. Active matrix metalloproteinases are present in cartilage during immune complex-mediated arthritis: a pivotal role for stromelysin-1 in cartilage destruction. J Immunol 1999;163: 5633-9.
13. Miyazawa K, Mori A, Miyata H, Akahane M, Ajisawa Y, Okudaira H. Regulation of interleukin-1β-induced interleukin-6 gene expression in human fibroblast-like synoviocytes by p38 mitogen-activated protein kinase. J Biol Chem 1998;273:24832-8.
14. Kyriakis JM, Avruch J. Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol Rev 2001;81:807-69.
15. Reunanen N, Li SP, Ahonen M, Foschi M, Han J, Kahari VM. Activation of p38α MAPK enhances collagenase-1 (matrix metalloproteinase (MMP)-1) and stromelysin-1 (MMP-3) expression by mRNA stabilization. J Biol Chem 2002;277:32360-8.
16. Brauchle M, Gluck D, Di Padova F, Han J, Gram H. Independent role of p38 and ERK1/2 mitogen-activated kinases in the upregulation of matrix metalloproteinase-1. Exp Cell Res 2000;258:135-44.
17. Westermarck J, Li SP, Kallunki T, Han J, Kahari VM. p38 mitogen-activated protein kinase-dependent activation of protein phosphatases 1 and 2A inhibits MEK1 and MEK2 activity and collagenase 1 (MMP-1) gene expression. Mol Cell Biol 2001;21: 2373-83.
18. Westermarck J, Li S, Jaakkola P, Kallunki T, Grenman R, Kahari VM. Activation of fibroblast collagenase-1 expression by tumor cells of squamous cell carcinomas is mediated by p38 mitogen-activated protein kinase and c-Jun NH2-terminal kinase-2. Cancer Res 2000;60:7156-62.
19. Schett G, Tohidast-Akrad M, Smolen JS, Schmid BJ, Steiner CW, Bitzan P, et al. Activation, differential localization, and regulation of the stress-activated protein kinases, extracellular signal-regulated kinase, c-Jun N-terminal kinase, and p38 mitogen-activated protein kinase, in synovial tissue and cells in rheumatoid arthritis. Arthritis Rheum 2000;43:2501-12.
20. Badger AM, Griswold DE, Kapadia R, Blake S, Swift BA, Hoffman SJ, et al. Disease-modifying activity of SB 242235, a selective inhibitor of p38 mitogen-activated protein kinase, in rat adjuvant-induced arthritis. Arthritis Rheum 2000;43:175-83.
21. Inazuka M, Tahira T, Horiuchi T, Harashima S, Sawabe T, Kondo M, et al. Analysis of p53 tumour suppressor gene somatic mutations in rheumatoid arthritis synovium. Rheumatology (Oxford) 2000;39:262-6.
22. Reme T, Travaglio A, Gueydon E, Adla L, Jorgensen C, Sany J. Mutations of the p53 tumour suppressor gene in erosive rheumatoid synovial tissue. Clin Exp Immunol 1998;111:353-8.
23. Firestein GS, Echeverri F, Yeo M, Zvaifler NJ, Green DR. Somatic mutations in the p53 tumor suppressor gene in rheumatoid arthritis synovium. Proc Natl Acad Sci U S A 1997;94: 10895-900.
24. Kullmann F, Judex M, Neudecker I, Lechner S, Justen HP, Green DR, et al. Analysis of the p53 tumor suppressor gene in rheumatoid. arthritis synovial fibroblasts. Arthritis Rheum 1999;42: 1594-600.
25. Han Z, Boyle DL, Shi BY, Green DR, Firestein GS. Dominant-negative p53 mutations in rheumatoid arthritis. Arthritis Rheum 1999;42:1088-92.
26. Santhanam U, Ray A, Sehgal PB. Repression of the interleukin 6 gene promoter by p53 and the retinoblastoma susceptibility gene product. Proc Natl Acad Sci U S A 1991;88:7605-9.
27. Sun Y, Sun Y, Wenger L, Rutter JL, Brinckerhoff CE, Cheung HS. Human metalloproteinase-1 (collagenase-1) is a tumor suppressor protein p53 target gene. Ann N Y Acad Sci 1999;878: 638-41.
28. Sun Y, Sun Y, Wenger L, Rutter JL, Brinckerhoff CE, Cheung HS. p53 down-regulates human matrix metalloproteinase-1 (collagenase-1) gene expression. J Biol Chem 1999;274:11535-40.
29. Perlman H, Bradley K, Liu H, Cole S, Shamiyeh E, Smith RC, et al. IL-6 and matrix metalloproteinases-1 are regulated by the cyclin-dependent kinase inhibitor p21 in synovial fibroblasts. J Immunol 2003;170:838-45.
30. Nasu K, Kohsaka H, Nonomura Y, Terada Y, Ito H, Hirokawa K, et al. Adenoviral transfer of cyclin-dependent kinase inhibitor genes suppresses collagen-induced arthritis in mice. J Immunol 2000;165:7246-52.
31. Nonomura Y, Kohsaka H, Nasu K, Terada Y, Ikeda M, Miyasaka N. Suppression of arthritis by forced expression of cyclin-dependent kinase inhibitor p21(Cip1) gene into the joints. Int Immunol 2001;13:723-31.
32. Taniguchi K, Kohsaka H, Inoue N, Terada Y, Ito H, Hirokawa K, et al. Induction of the p16INK4a senescence gene as a new therapeutic strategy for the treatment of rheumatoid arthritis. Nat Med 1999;5:760-7.
33. Kuenzler P, Kuchen S, Rihoskova V, Michel BA, Gay RE, Neidhart M, et al. Induction of p16 at sites of cartilage invasion in the SCID mouse coimplantation model of rheumatoid arthritis. Arthritis Rheum 2003;48:2069-73.
34. Weinberg RA. The retinoblastoma protein and cell cycle control. Cell 1995;81:323-30.
35. Helin K. Regulation of cell proliferation by the E2F transcription factors. Curr Opin Genet Dev 1998;8:28-35.
36. Arnett FC, Edworthy SM, Bloch DA, McShane DJ, Fries JF, Cooper NS, et al. The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum 1988;31:315-24.
37. Altman R, Alarcon G, Appelrouth D, Bloch D, Borenstein D, Brandt K, et al. The American College of Rheumatology criteria for the classification and reporting of osteoarthritis of the hip. Arthritis Rheum 1991;34:505-14.
38. Sodin-Semrl S, Taddeo B, Tseng D, Varga J, Fiore S. Lipoxin A4 inhibits IL-1β-induced IL-6, IL-8, and matrix metalloproteinase-3 production in human synovial fibroblasts and enhances synthesis of tissue inhibitors of metalloproteinases. J Immunol 2000;164: 2660-6.
39. Koch AE, Kunkel SL, Harlow LA, Johnson B, Evanoff HL, Haines GK, et al. Enhanced production of monocyte chemoattractant protein-1 in rheumatoid arthritis. J Clin Invest 1992;90:772-9.
40. Koch AE, Kunkel SL, Harlow LA, Mazarakis DD, Haines GK, Burdick MD, et al. Epithelial neutrophil activating peptide-78: a novel chemotactic cytokine for neutrophils in arthritis. J Clin Invest 1994;94:1012-8.
41. Han Z, Boyle DL, Chang L, Bennett B, Karin M, Yang L, et al. c-jun N-terminal kinase is required for metalloproteinase expression and joint destruction in inflammatory arthritis. J Clin Invest 2001;108:73-81.
42. Han Z, Boyle DL, Aupperle KR, Bennett B, Manning AM, Firestein GS. Jun N-terminal kinase in rheumatoid arthritis. J Pharmacol Exp Ther 1999;291:124-30.
43. Johnson BA, Haines GK, Harlow LA, Koch AE. Adhesion molecule expression in human synovial tissue. Arthritis Rheum 1993;36:137-46.
44. Perlman H, Georganas C, Pagliari U, Koch AE, Haines K III, Pope RM. Bcl-2 expression in synovial fibroblasts is essential for maintaining mitochondrial homeostasis and cell viability. J Immunol 2000;164:5227-35.
45. CIP1-mediated inhibition of cell proliferation by overexpression of the gax homeodomain gene. Genes Dev 1997; 11:1674-89.
46. Smith RC, Wills KN, Antelman D, Perlman H, Truong LN, Krasinski K, et al. Adenoviral constructs encoding phosphorylation-competent full-length and truncated forms of the human retinoblastoma protein inhibit myocyte proliferation and neointima formation. Circulation 1997;96:1899-905.
47. Perlman H, Sata M, Krasinski K, Dorai T, Buttyan R, Walsh R. Adenovirus-encoded hammerhead ribozyme to Bcl-2 inhibits neointimal hyperplasia and induces vascular smooth muscle cell apoptosis. Cardiovasc Res 2000;45:570-8.
48. Perlman H, Sata M, Le Roux A, Sedlak TW, Branellec D, Walsh K. Bax-mediated cell death by the Gax homeoprotein requires mitogen activation but is independent of cell cycle activity. EMBO J 1998;17:3576-86.
49. Gniadek P, Aktas O, Wandinger KP, Bellmann-Strobl J, Wengert O, Weber A, et al. Systemic IFN-β treatment induces apoptosis of peripheral immune cells in MS patients. J Neuroimmunol 2003; 137:187-96.
50. Birks EJ, Burton PB, Owen V, Mullen AJ, Hunt D, Banner NR, et al. Elevated tumor necrosis factor-α and interleukin-6 in myocardium and serum of malfunctioning donor hearts. Circulation 2000;102(19 Suppl 3):352-8.
51. Lu J, Chua HH, Chen SY, Chen JY, Tsai CH. Regulation of matrix metalloproteinase-1 by Epstein-Barr virus proteins. Cancer Res 2003;63:256-62.
52. Mohr W, Beneke G, Mohing W. Proliferation of synovial lining cells and fibroblasts. Ann Rheum Dis 1975;34:219-24.
53. Qu Z, Garcia CH, O'Rourke LM, Planck SR, Kohli M, Rosenbaum JT. Local proliferation of fibroblast-like synoviocytes contributes to synovial hyperplasia: results of proliferating cell nuclear antigen/cyclin, c-myc, and nucleolar organizer region staining. Arthritis Rheum 1994;37:212-20.
54. Sugiyama M, Tsukazaki T, Yonekura A, Matsuzaki S, Yamashita S, Iwasaki K. Localization of apoptosis and expression of apoptosis related proteins in the synovium of patients with rheumatoid arthritis. Ann Rheum Dis 1996;55:442-9.
55. Zarkowska T, Mittnacht S. Differential phosphorylation of the retinoblastoma protein by G1/S cyclin-dependent kinases. J Biol Chem 1997;272:12738-46.
56. Knudsen ES, Wang JY. Differential regulation of retinoblastoma protein function by specific Cdk phosphorylation sites. J Biol Chem 1996;271:8313-20.
57. Wang J, Guo K, Wills KN, Walsh K. Rb functions to inhibit apoptosis during myocyte differentiation. Cancer Res 1997;57: 351-4.
58. Fueyo J, Gomez-Manzano C, Yung WK, Liu TJ, Alemany R, Bruner JM, et al. Suppression of human glioma growth by adenovirus-mediated Rb gene transfer. Neurology 1998;50: 1307-15.
59. Demers GW, Harris MP, Wen SF, Engler H, Nielsen LL, Maneval DC. A recombinant adenoviral vector expressing full-length human retinoblastoma susceptibility gene inhibits human tumor cell growth. Cancer Gene Ther 1998;5:207-14.
60. Riley DJ, Nikitin AY, Lee WH. Adenovirus-mediated retinoblastoma gene therapy suppresses spontaneous pituitary melanotroph tumors in Rb+/- mice. Nat Med 1996;2:1316-21.
61. Perlman H, Bradley K, Hongtao L, Cole S, Shamiyeh E, Smith RC, et al. IL-6 and MMP-1 are regulated by the cyclin-dependent kinase inhibitor p21 in synovial fibroblasts. J Immunol 2003;170: 838-45.
62. Wang Y, Huang S, Sah VP, Ross J Jr, Brown JH, Han J, et al. Cardiac muscle cell hypertrophy and apoptosis induced by distinct members of the p38 mitogen-activated protein kinase family. J Biol Chem 1998;273:2161-8.
63. Ravanti L, Hakkinen L, Larjava H, Saarialho-Kere U, Foschi M, Han J, et al. Transforming growth factor-β induces collagenase-3 expression by human gingival fibroblasts via p38 mitogen-activated protein kinase. J Biol Chem 1999;274:37292-300.
64. 2. J Biol Chem 1996;271:26981-8.
65. Han J, Wang X, Jiang Y, Ulevitch RJ, Lin S. Identification and characterization of a predominant isoform of human MKK3. FEBS Lett 1997;403:19-22.
66. El-Deiry WS, Tokino T, Velculescu VE, Levy DB, Parsons R, Trent JM, et al. WAF1, a potential mediator of p53 tumor suppression. Cell 1993;75:817-25.
67. El-Deiry WS, Harper JW, O'Connor PM, Velculescu VE, Canman CE, Jackman J, et al. WAF1/CIP1 is induced in p53-mediated G1 arrest and apoptosis. Cancer Res 1994;54:1169-74.
68. Sherr CJ, Roberts JM. CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev 1999;13:1501-12.
69. Juge-Morineau N, Harousseau JL, Amiot M, Bataille R. The retinoblastoma susceptibility gene RB-1 in multiple myeloma. Leuk Lymphoma 1997;24:229-37.
70. Dao DD, Sawyer JR, Epstein J, Hoover RG, Barlogie B, Tricot G. Deletion of the retinoblastoma gene in multiple myeloma. Leukemia 1994;8:1280-4.
71. Zhu YM, Bradbury DA, Keith FJ, Russell N. Absence of retino-blastoma protein expression results in autocrine production of interleukin-6 and promotes the autonomous growth of acute myeloid leukemia blast cells. Leukemia 1994;8:1982-8.
72. Zhu YM, Bradbury D, Russell N. Decreased retinoblastoma protein expression in acute myeloblastic leukaemia is associated with the autonomous proliferation of clonogenic blasts. Br J Haematol 1994;86:533-9.
73. Vincenti MP, Brinckerhoff CE. Transcriptional regulation of collagenase (MMP-1, MMP-13) genes in arthritis: integration of complex signaling pathways for the recruitment of gene-specific transcription factors. Arthritis Res 2002;4:157-64.
74. Kotlyarov A, Neininger A, Schubert C, Eckert R, Birchmeier C, Volk HD, et al. MAPKAP kinase 2 is essential for LPS-induced TNF-α biosynthesis. Nat Cell Biol 1999;1:94-7.
75. Neininger A, Kontoyiannis D, Kotlyarov A, Winzen R, Eckert R, Volk HD, et al. MK2 targets AU-rich elements and regulates biosynthesis of tumor necrosis factor and interleukin-6 independently at different post-transcriptional levels. J Biol Chem 2002; 277:3065-8.
76. Knauf U, Tschopp C, Gram H. Negative regulation of protein translation by mitogen-activated protein kinase-interacting kinases 1 and 2. Mol Cell Biol 2001;21:5500-11.
77. Nikolcheva T, Pyronnet S, Chou SY, Sonenberg N, Song A, Clayberger C, et al. A translational rheostat for RFLAT-1 regulates RANTES expression in T lymphocytes. J Clin Invest 2002; 110:119-26.
78. Banerjee S, Narayanan K, Mizutani T, Makino S. Murine corona-virus replication-induced p38 mitogen-activated protein kinase activation promotes interleukin-6 production and virus replication in cultured cells. J Virol 2002;76:5937-48.
79. Chauhan D, Hideshima T, Treon S, Teoh G, Raje N, Yoshihimito S, et al. Functional interaction between retinoblastoma protein and stress-activated protein kinase in multiple myeloma cells. Cancer Res 1999;59:1192-5.
80. Shim J, Park HS, Kim MJ, Park J, Park E, Cho SG, et al. Rb protein down-regulates the stress-activated signals through inhibiting c-Jun N-terminal kinase/stress-activated protein kinase. J Biol Chem 2000;275:14107-11.