Integrin-regulated secretion of interleukin 4: A novel pathway of mechanotransduction in human articular chondrocytes

Journal of Cell Biology

Volumn 145, Issue 1, 1999, Pages 183-189

  Millward Sadler, S J ^a   Wright, M O ^a   Lee, H S ^a   Nishida, K ^a   Caldwell, H ^a   Nuki, G ^b   Salter, D M ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b WESTERN GENERAL HOSPITAL   (United Kingdom)

Author keywords

Chondrocyte; Integrin; Interleukin 4; Ion channels; Mechanotransduction

Indexed keywords

APAMIN; CALCIUM ION; CYTOKINE ANTIBODY; INOSITOL TRISPHOSPHATE; INTEGRIN; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 1BETA; INTERLEUKIN 4; INTERLEUKIN 4 RECEPTOR; PHOSPHOLIPASE C; POTASSIUM CHANNEL; POTASSIUM ION; RECEPTOR ANTIBODY;

ANIMAL CELL; ARTICLE; CARTILAGE CELL; CELL MEMBRANE STEADY POTENTIAL; CONTROLLED STUDY; CYTOKINE PRODUCTION; HUMAN; HUMAN CELL; HYPERPOLARIZATION; MECHANICAL STIMULATION; MOUSE; NONHUMAN; OSTEOARTHRITIS; PATHOGENESIS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ADULT; AGED; AGED, 80 AND OVER; ANIMALS; ANTIGENS, CD29; APAMIN; CALCIUM; CARTILAGE, ARTICULAR; FEMALE; FLUNARIZINE; GADOLINIUM; GENISTEIN; HUMANS; INTERLEUKIN-4; ION CHANNEL GATING; ION TRANSPORT; MALE; MEMBRANE POTENTIALS; MICE; MICE, KNOCKOUT; MIDDLE AGED; NEOMYCIN; PHOSPHATIDYLINOSITOL DIACYLGLYCEROL-LYASE; PHOSPHOLIPASE C; POTASSIUM CHANNELS; RECEPTORS, INTERLEUKIN-4; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; STRESS, MECHANICAL;

ANIMALIA;

EID: 0033526051     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.145.1.183     Document Type: Article

References (56)

1. Akiama, T., J. Ishida, S. Nakagana, H. Ogawara, S. Watanabe, N. Itoh, M. Sibuya, and Y. Fukami. 1987. Genistein, a specific inhibitor of tyrosine-specific protein kinases. J. Biol. Chem. 262:5592-5595.
2. Aman, M.J., N. Tayebi, N.I. Obiri, R.K. Puri, W.S. Modi, and W.J. Leonard. 1996. cDNA cloning and characterization of the human interleukin-13 receptor alpha chain. J. Biol. Chem. 271:29265-29270.
3. Arai, N., D. Nomura, D. Villaret, D.R. Malefijt, M. Seiki, M. Yoshida, S. Minoshima, R. Fukuyama, M. Maekawa, J. Kudoh, et al. 1989. Complete nucleotide sequence of the chromosomal gene for human IL-4 and its expression. J. Immunol. 142:274-282.
4. Ayajiki, K., M. Kindermann, M. Hecker, I. Fleming, and R. Busse. 1996. Intracellular pH and tyrosine phosphorylation but not calcium determine shear stress-induced nitric oxide production in native endothelial cells. Circ. Res. 78:750-758.
5. + channels of small conductance in cultured rat skeletal muscle. Nature. 323: 718-720.
6. Chen, B.M., and A.D. Grinnell. 1995. Integrins and modulation of transmitter release from motor nerve terminals by stretch. Science. 269:1578-1580.
7. Chevalier, X., P. Claudepierre, N. Groult, L. Zardi, and W. Hornebeck. 1996. Presence of ED-A containing fibronectin in human articular cartilage from patients with osteoarthritis and rheumatoid arthritis. J. Rheumatol. 23:1022-1030.
8. Cockcroft, S., and B.D Gomperts. 1985. Role of guanine nucleotide binding protein in the activation of polyphosphoinositide phosphodiesterase. Nature. 314:534-536.
9. Davies, P.F. 1995. Flow-mediated endothelial mechanotransduction. Physiol. Rev. 75:519-560.
10. Davies, P.F., and S.C Tripathi. 1993. Mechanical stress mechanisms and the cell. Circ. Res. 72:239-245.
11. Dean, D.D. 1991. Proteinase-mediated cartilage degradation in osteoarthritis. Semin. Arthritis Rheum. 20(Suppl. 2):2-11.
12. Friedlander, M., P.C. Brooks, R.W. Sharfer, C.M. Kincaid, J.A. Varner, and D.A. Cheresh. 1995. Definition of two angiogenic pathways by distinct aV integrins. Science. 270:1500-1502.
13. Glogauer, M., P. Arora, G. Yao, I. Sokholov, J. Ferrier, and C.A.G. McCulloch. 1997. Calcium ions and tyrosine phosphorylation interact coordinately with actin to regulate cytoprotective responses to stretching. J. Cell. Sci. 110:11-21.
14. Harter, L.V., K.A. Hruska, and R.L. Duncan. 1995. Human osteoblast-like bone cells respond to mechanical strain with increased bone matrix protein production independent of hormonal regulation. Endocrinology. 136:528-535.
15. Hynes, R.O. 1992. Integrins: versatility, modulation, and signaling in cell adhesion. Cell. 69:11-25.
16. Idzerda, R.L., C.J. March, B. Mosley, S.D. Lyman, T. Vanden Bos, S.D. Gimpel, W.S. Din, K.H. Grabstein, M.B. Widmer, L.S. Park, et al. 1990. Human interleukin 4 receptor confers biological responsiveness and defines a novel receptor superfamily. J. Exp. Med. 171:861-873.
17. Jobanputra, P., H. Lin, K. Jenkins, C. Bavington, F.R. Brennan, G. Nuki, D.M. Salter, and J.L. Godolphin. 1996. Modulation of human chondrocyte integrins by inflammatory synovial fluid. Arthritis Rheum. 39:1430-1432.
18. 2. Nature. 337:557-560.
19. Kimono, I., S. Kudo, T. Yamakazi, Y. Zou, I. Shiojimi, and Y. Yazaki. 1996. Mechanical stretch activates the stress activated protein kinases in cardiac myocytes. FASEB (Fed. Am. Soc. Exp. Biol.) J. 10:631-636.
20. Kopf, M., G. Le Gros, M. Bachmann, M.C. Lamers, H. Bluethmann, and G. Kohler. 1993. Disruption of the murine IL-4 gene blocks Th2 cytokine responses. Nature. 362:245-248.
21. Lapadula, G., F. Iannone, C. Zuccaro, V. Grattagliano, M. Covelli, V. Patella, G. Lobianco, and V. Pipitone. 1997. Integrin expression on chondrocytes: correlations with the degree of cartilage damage in human osteoarthritis. Clin. Exp. Rheumatol. 15:247-254.
22. Loeser, R.F., C.S. Carlson, and M.P. McGee. 1995. Expression of beta 1 integrins by cultured articular chondrocytes and in osteoarthritic cartilage. Exp. Cell Res. 217:248-257.
23. 2-terminal kinase activation by mechanical stretch is integrin-dependent and matrix-specific in rat cardiac fibroblasts. J. Clin. Invest. 101:301-310.
24. Maniotis, A.J., C.S. Chen, and D.E. Ingber. 1997. Demonstration of mechanical connections between integrins, cytoskelelal filaments, and nucleoplasm that stabilize nuclear structure. Proc. Natl. Acad. Sci. USA. 94:849-854.
25. Miyake, S., H. Yagita, T. Maruyama, H. Hashimoto, N. Miyasaka, and K Okumura. 1993. β1 integrin-mediated interaction with extracellular matrix proteins regulates cytokine gene expression in synovial fluid cells of rheumatoid arthritis patients. J. Exp. Med. 177:863-868.
26. Mow, V.C., A. Ratcliffe, and A.R. Poole. 1992. Cartilage and diarthrodial joints as paradigms for hierarchical materials and structures. Biomaterials. 13:67-97.
27. Muller, J.M., W.M. Chilian, and M.J. Davis. 1997. Integrin signaling transduces shear stress-dependent vasodilation of coronary arterioles. Circ. Res. 80: 320-326.
28. Nemoto, O., H. Yamada, T. Kikuchi, M. Shimmei, K. Obata, H. Sato, and M. Seiki. 1997. Suppression of matrix metalloproteinase-3 synthesis by interleukin-4 in human articular chondrocytes. J. Rheumatol. 24:1774-1779.
29. Prasad, A.R.S., S.A. Logan, R.M. Nerem, C.J. Schwartz, and E.A. Sprague. 1993. Flow-related responses of intracellular inositol phosphate levels in cultured aortic endothelial cells. Circ. Res. 72:827-836.
30. Puck, J.M., S.M. Deschenes, J.C. Porter, A.S. Dutra, C.J. Brown, H.F. Willard, and P.S. Henthorn. 1993. The interleukin-2 receptor gamma chain maps to Xq13.1 and is mutated in X-linked severe combined immunodeficiency, SCIDX1. Hum. Mol. Genet. 2:1099-1104.
31. Ra, C., M. Yasuda, H. Yagita, and K. Okumara. 1994. Fibronectin receptor integrins are involved in mast cell activation. J. Allergy Clin. Immunol. 94: 625-628.
32. Sachs, F. 1988. Mechanical transduction in biological systems. Crit. Rev. Biomed. Eng. 16:141-169.
33. Salter, D.M., D.E. Hughes, R. Simpson, D.L. Gardner. 1992. Integrin expression by human articular chondrocytes. Br. J. Rheumatol. 31:231-234.
34. Salter, D.M. 1993. Tenascin is increased in cartilage and synovium from arthritic knees. Br. J. Rheumatol. 32:780-786.
35. Salter, D.M., G. Nuki, and M.O. Wright. 1996. Interleukin-4 expression in normal and osteoarthritic human articular cartilage. J. Rheumatol. 23:1314-1315.
36. Salter, D.M., J.E. Robb, and M.O. Wright. 1997. Electrophysiological responses of human bone cells to mechanical stimulation: evidence for specific integrin function in mechanotransduction. J. Bone Miner. Res. 12:1133-1141.
37. Sanger, F., S. Nicklen, and A.R. Coulson. 1977. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA. 74:5436-5467.
38. Schmidt, C., H. Pommerenke, F. Durr, B. Nebe, and J. Rychly. 1998. Mechanical stressing of integrin receptors induces enhanced tyrosine phosphorylation of cytoskeletally anchored proteins. J. Biol. Chem. 273:5081-5085.
39. 2+ release from isolated platelet membrane vesicles. Biochem. Pharmacol. 36:3331-3337.
40. Shingu, M., S. Miyauchi, Y. Nagai, C. Yasutake, and K. Horie. 1995. The role of IL4 and IL6 in IL1-dependent cartilage matrix degradation. Br. J. Rheumatol. 34:101-106.
41. Shyy, J.Y.-J., and S. Chien. 1997. Role of integrins in cellular responses to mechanical stress and adhesion. Curr. Opin. Cell. Biol. 9:707-713.
42. Somjen, D., I. Binderman, E. Berger, and A. Harell. 1980. Bone remodelling induced by physical stress is proslaglandin E2 mediated. Biochim. Biophys. Acta. 627:91-100.
43. Stockwell, R.A. 1991. Cartilage failure in osteoarthritis: relevance of normal structure and function. A review. Clin. Anat. 4:161-191.
44. Sundberg, C., and K. Rubin. 1996. Stimulation of β1 integrins on fibroblasts induces PDGF independent tyrosine phosphorylation of PDGF β receptors. J. Cell Biol. 132:741-752.
45. Takeshita, T., H. Asao, K. Ohtani, N. Ishii, S. Kumaki, N. Tanaka, H. Munakata, M. Nakamura, and K. Sugamura. 1992. Cloning of the gamma chain of the human IL-2 receptor. Science. 257:379-382.
46. Urban, J.P. 1994. The chondrocyte: a cell under pressure. Br. J. Rheumatol. 33: 901-908.
47. Veldhuijzen, J.P., L.A. Bourret, and G.A. Rodan. 1979. In vitro studies of the effect of intermittent compressive forces on cartilage cell proliferation. J. Cell. Physiol. 98:299-306.
48. Wang, N., J.P. Butler, and D.E. Ingber. 1993. Mechanotransduction across the cell surface and through the cytoskeleton. Science. 260:1124-1127.
49. Wilson, E., Q. Mai, K. Sudhir, R.H. Weiss, and H.E. Ives. 1993. Mechanical strain induces growth of vascular smooth muscle cells via autocrine action of PDGF. J. Cell Biol. 123:741-747.
50. Wright, M.O., R.A. Stockwell, and G. Nuki. 1992. Response of plasma membrane to applied hydrostatic pressure in chondrocytes and fibroblasts. Connect. Tissue Res. 28:49-70.
51. Wright, M.O., P. Jobanputra, C. Bavington, D.M. Salter, and G. Nuki. 1995. Intracellular signal transduction pathways in human chondrocytes stimulated by intermittent pressurization. Trans. Orth. Res. Soc. 29:88.
52. Wright, M.O., P. Jobanputra, C. Bavington, D.M. Salter, and G. Nuki. 1996. The effects of intermittent pressurization on the electrophysiology of cultured human chondrocytes: evidence for the presence of stretch activated membrane ion channels. Clin. Sci. 90:61-71.
53. Wrighl, M.O., K. Nishida, C. Bavington, J.L. Godolphin, E. Dunne, S. Walmsley, P. Jobanputra, G. Nuki, and D.M. Salter. 1997. Hyperpolarization of cultured human chondrocytes follows cyclical pressure-induced strain: evidence of a role for α5β1 integrin as a chondrocyte mechanoreceptor. J. Orthop. Res. 15:742-747.
54. Wright, M.O., S.J. Millward-Sadler, G. Nuki, and D.M. Salter. 1998. Aberrant membrane depolarization in cultured chondrocytes from osteoarthritic cartilage following cyclical mechanical strain and exposure to IL4. Br. J. Rheumatol. 37(Suppl. 1):154.
55. Yang, X.C., and F. Sachs. 1989. Block of stretch-activated ion channels in Xenopus oocytes by gadolinium and calcium ions. Science. 243:1068-1071.
56. Yano, Y., J. Geibel, and B.E. Sumpio. 1996. Tyrosine phosphorylation of pp125FAK and paxillin in aortic endothelial cells induced by mechanical strain. J. Cell. Physiol. 271:c635-c649.