Abstract
The purpose of this study was to investigate the role of histamine in human rheumatoid synovial fibroblasts in the production of factors responsible for tissue remodelling and cartilage breakdown in rheumatoid arthritis. We examined the effects of histamine of tritiated thymidine incorporation, production of matrix metalloproteinase-1 (MMP-1), histamine H1-receptor expression, phosphoinositide metabolism and intracellular calcium ion concentration ([Ca2+] i ) in human rheumatoid synovial fibroblasts. Tritiated thymidine incorporation studies demonstrated that histamine markedly stimulated the proliferation of rheumatoid synovial fibroblasts. Immunofluorescence and Northern blot analyses revealed that proMMP-1 production was also stimulated by histamine. The levels of inositol phosphates and [Ca2+] i in the cells were elevated in response to histamine, indicating that the cells expressed histamine H1-receptors; and Northern blot analysis indicated that these H1-receptors were up-regulated by histamine. In in situ hybridization, large amounts of histamine H1-receptor mRNA were also detected in rheumatoid synovial tissue. These results suggest that the interaction between H1-receptor expression in rheumatoid synovial fibroblasts and histamine secretion by mast cells and macrophages in the affected sites is an important event responsible for tissue remodelling and joint destruction in rheumatoid arthritis.
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Angel P, Baumann I, Stein B, Delius H, Rahmsdorf HJ, Herrlich P (1987) 12-O-tetradecanoyl-phorbol-13-acetate induction of the human collagenase gene is mediated by an inducible enhancer element located in the 5′-flanking region. Mol Cell Biol 7:2256–2266
Arend WP, Dayer JM (1990) Cytokines and cytokine inhibitors or antagonists in rheumatoid arthritis. Arthritis Rheum 33:305–315
Bartholeyns J, Fozzard JR (1985) Role of histamine in tumour development. Trends Pharmacol Sci 7:123–125
Berridge MJ, Dawson RM, Downes CP, Heslop JP, Irvine RF (1983) Changes in the levels of inositol phosphates after agonist-dependent hydrolysis of membrane phosphoinositides. Biochem J 212:473–482
Bromley M, Woolley DE (1984) Histopathology of the rheumatoid lesion. Identification of cell types at sites of cartilage erosion. Arthritis Rheum 27:857–863
Bromley M, Fisher WD, Woolley DE (1984) Mast cells at sites of cartilage erosion in the rheumatoid joint. Ann Rheum Dis 43:76–79
Bruschi G, Bruschi ME, Regolisti G, Borghetti A (1988) Myoplasmic Ca2+-force relationship studied with fura-2 during stimulation of rat aortic smooth muscle. Am J Physiol 254:H840–854
Buchan G, Barrett K, Turner M, Chantry D, Maini RN, Feldmanns M (1988) Interleukin-1 and tumour necrosis factor mRNA expression in rheumatoid arthritis: prolonged production of IL-1 alpha. Clin Exp Immunol 73:449–455
Case JP, Lafyatis R, Remmers EF, Kumkumian GK, Wilder RL (1989) Transin/stromelysin expression in rheumatoid synovium. A transformation-associated metalloproteinase secreted by phenotypically invasive synoviocytes. Am J Pathol 135:1055–1064
Crisp AJ, Chapman CM, Kirkhan SE, Schiller AL, Krane SM (1984) Articular mastocytosis in rheumatoid arthritis. Arthritis Rheum 27:845–851
Crisp AJ, Wright JK, Hazlemans BL (1986) Effects of heparin, histamine, and salmon calcitonin on mouse calvarial bone resorption. Ann Rheum Dis 45:422–427
Daum PR, Downes CP, Young JM (1984) Histamine stimulation of inositol 1-phosphate accumulation in lithium-treated slices from regions of guinea pig brain. J Neurochem 43:25–32
Douglas WW (1985) Histamine and 5-hydroxytryptamine (serotonin) and their antagonists. In: Goodman LS, Gilman A (eds) The Pharmacological Basis of Therapeutics. Macmillan, New York
Ekblom P, Lehtonen E, Saxén L, Timpl R (1981) Shift in collagen type as an early response to induction of the metanephric mesenchyme. J Cell Biol 89:276–283
Frewin DB, Cleland LG, Jonsson JR, Robertsons PW (1986) Histamine levels in human synovial fluid. J Rheumatol 13:13–14
Fukui H, Fujimoto K, Mizuguchi H, Sakamoto K, Horio Y, Takai S, Yamada K, Ito S (1994) Molecular cloning of the human histamine H1 receptor gene. Biochem Biophys Res Commun 201:894–901
Gantz I, Schaffer M, DelValle J, Logsdon C, Campbell V, Uhler M, Yamada T (1991) Molecular cloning of a gene encoding the histamine H2 receptor. Proc Natl Acad Sci USA 88:5937
Godfrey HP, Ilardi C, Engber W, Graziano FM (1984) Quantitation of human synovial mast cells in rheumatoid arthritis and other rheumatic diseases. Arthritis Rheum 27:852–856
Gravallese EM, Darling JM, Ladd AL, Katz JN, Dlimcher LH (1991) In situ hybridization studies of stromelysin and collagenase messenger RNA expression in rheumatoid synovium. Arthritis Rheum 34:1076–1084
Harris ED Jr (1985) Pathogenesis of rheumatoid arthritis. In: Kelly WN, Harris ED Jr, Ruddy S, Sledge CB (eds) Textbook of rheumatology. 2nd edn. W.B. Saunders, Philadelphia, pp 886–915
Henderson B, Pettipher ER (1985) The synovial lining cell: biology and pathobiology. Semin Arthritis Rheum 15:1–32
Hill SJ (1990) Distribution, properties, and functional characteristics of three classes of histamine receptor. Pharmacol Rev 42:45–83
Hiraoka K, Sasaguri Y, Komiya S, Inoue A, Morimatsu M (1992) Cell proliferation-related production of matrix metalloproteinases 1 (tissue collagenase) and 3 (stromelysin) by cultured human rheumatoid synovial fibroblasts. Biochem Int 27:1083–1091
Hiraoka K, Sasaguri Y, Komiya S, Zenmyo M, Inoue A, Morimatsu M (1993) Effects of lipid peroxide on production of matrix metalloproteinase 1 (tissue collagenase) and 3 (stromelysin) and tissue inhibitor metalloproteinase 1 by human rheumatoid synovial fibroblasts. Exp Mol Pathol 59:169–176
Ishikawa E, Toki A, Moriyama T, Matsuoka Y, Aikawa T, Suda M (1970) A study, the induction of histidine decarboxylase in tumor-bearing rat. J Biochem (Tokyo) 68:347–358
Ito A, Itoh Y, Sasaguri Y, Morimatsu M, Mori Y (1992) Effects of interleukin-6 on the metabolism of connective tissue components in rheumatoid synovial fibroblasts. Arthritis Rheum 35:1197–1201
Jordana M, Befus AD, Newhouse MT, Bienenstock J, Daudie J (1988) Effect of histamine on proliferation of normal human adult lung fibroblasts. Thorax 43:552–558
Liotta LA, Rao CN, Barsky SH (1983) Tumor invasion and the extracellular matrix. Lab Invest 49:636–649
Matsumoto T, Kanaide H, Nishimura J, Shogakiuchi Y, Kobayashi S, Nakamura M (1986) Histamine activates H1-receptors to induce cytosolic free calcium transients in cultured vascular smooth muscle cells from rat aorta. Biochem Biophys Res Commun 135:172–177
Murahashi N, Sasaguri Y, Ohuchida M, Kakita N, Morimatsu M (1992) Immortalization of human aortic smooth muscle cells with origin-minus simian virus 40 DNA. Biotechnol Appl Biochem 16:152–160
Nakanishi Y, Sugiura F, Kishi J, Hayakawa T (1986) Collagenase inhibitor stimulates cleft formation during early morphogenesis of mouse salivary gland. Dev Biol 113:201–206
Okada Y, Konomi H, Yada T, Kimata K, Nagase H (1989) Degradation of type IX collagen by matrix metalloproteinase-3 (stromelysin) from human rheumatoid synovial cells. FEBS Lett 244:473–476
Okada Y, Takeuchi N, Tomita K, Nakanishi I, Nagase H (1989) Immunolocalization of matrix metalloproteinase 3 (stromelysin) in rheumatoid synovioblasts (B cells): correlation with rheumatoid arthritis. Ann Rheum Dis 48:645–653
Panettieri RA, Yadvish PA, Kelly AM, Rubinstein NA, Kotlikoff MI (1990) Histamine stimulates proliferation of airway smooth muscle and induces c-fos expression. Am J Physiol 259:L365–671
Prockop DJ, Kivirikko KI, Tuderman L, Guzman NA (1979) The biosynthesis of collagen and its disorders (second of two parts). N Engl J Med 301:77–85
Sasaguri Y, Murahashi N, Sugama K, Kato S, Hiraoka K, Satoh T, Isomoto H, Morimatsu M (1994) Development-related changes in matrix metalloproteinase expression in human aortic smooth muscle cells. Lab Invest 71:261–269
Sasaguri Y, Yanagi H, Nagase H, Nakano R, Fukuda S, Morimatsu M (1991) Collagenase production by immortalized human aortic endothelial cells infected with simian virus 40. Virchows Arch [B] 60:91–97
Satoh T, Sugama K, Matsuo A, Kato S, Ito S, Hatanaka M, Sasaguri Y (1994) Histamine as an activator of cell growth and extracellular matrix reconstruction for human vascular smooth muscle cells. Atherosclerosis 110:53–61
Shima I, Sasaguri Y, Kusukawa J, Nakano R, Yamama H, Fujita H, Kakegawa T, Morimatsu M (1993) Production of matrix metalloproteinase 92 (92-kDa gelatinase) by human oesophageal squamous cell carcinoma in response to epidermal growth factor. Br J Cancer 67:721–727
Takagishi T, Sasaguri Y, Nakano R, Arima N, Tanimoto A, Fukui H, Morimatsu M (1995) Expression of the histamine H1 receptor gene in relation to atherosclerosis. Am J Pathol 146:981–988
Taylor DJ, Woolley DE (1987) Histamine H1 receptors on adherent rheumatoid synovial cells in culture: demonstration by radioligand binding and inhibition of histamine-stimulated prostaglandin E production by histamine H1 antagonists. Ann Rheum Dis 46:425–430
Taylor DJ, Yoff JR, Brown DM, Woolley DE (1986) Histamine stimulates prostaglandin E production by rheumatoid synovial cells and human articular chondrocytes in culture. Arthritis Rheum 29:160–165
Tilly BC, Tertoolen LG, Remorie R, Ladoux A, Verlaan I, Laat SW de, Moolenaar WH (1990) Histamine as a growth factor and chemoattractant for human carcinoma and melanoma cells: action through Ca2(+)-mobilizing H1 receptors. J Cell Biol 110:1211–1215
Watanabe T, Yaguchi Y, Maeyama K, Wada H (1991) Formation of histamine:histidine decarboxylase. In: Born, GVR, Cuatrecasas P, Herken H (eds) Histamine and histamine antagonist. Handbook of experimental pharmacology, vol 97, Springer, Berlin Heidelberg New York, p 347
Welgus HG, Jeffrey JJ, Eisen AZ (1981) The collagen substrate specificity of human skin fibroblast collagenase. J Biol Chem 256:9511–9515
Woolley DE, Yoffe JR, Evansons JM (1986) Mast cells and matrix degradation in the rheumatoid joint. In: Tschesche H (ed) Proteinases in inflammation and tumor invasion. Water de Gruyter, Berlin, pp 61–76
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Zenmyo, M., Morimatsu, M., Hiraoka, K. et al. Histamine-stimulated production of matrix metalloproteinase 1 by human rheumatoid synovial fibroblasts is mediated by histamine H1-receptors. Vichows Archiv A Pathol Anat 427, 437–444 (1995). https://doi.org/10.1007/BF00199394
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DOI: https://doi.org/10.1007/BF00199394