Urokinase plasminogen activator is a central regulator of macrophage three-dimensional invasion, matrix degradation, and adhesion

Journal of Immunology

Volumn 192, Issue 8, 2014, Pages 3540-3547

  Fleetwood, Andrew J ^a   Achuthan, Adrian ^a   Schultz, Heidi ^b   Nansen, Anneline ^c   Almholt, Kasper ^c   Usher, Pernille ^c   Hamilton, John A ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c NOVO NORDISK A S   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; CELL ADHESION; CELL MOVEMENT; ENZYME ACTIVATION; EXTRACELLULAR MATRIX; FEMALE; HUMANS; MACROPHAGES; MATRIX METALLOPROTEINASE 9; MICE; MICE, KNOCKOUT; MODELS, BIOLOGICAL; PROTEOLYSIS; UROKINASE-TYPE PLASMINOGEN ACTIVATOR;

EID: 84898636342     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1302864     Document Type: Article

References (70)

1. Haringman, J. J., D. M. Gerlag, A. H. Zwinderman, T. J. Smeets, M. C. Kraan, D. Baeten, I. B. McInnes, B. Bresnihan, and P. P. Tak. 2005. Synovial tissue macrophages: a sensitive biomarker for response to treatment in patients with rheumatoid arthritis. Ann. Rheum. Dis. 64: 834-838.
2. Hamilton, J. A., and P. P. Tak. 2009. The dynamics of macrophage lineage populations in inflammatory and autoimmune diseases. Arthritis Rheum. 60: 1210-1221.
3. Gerlag, D. M., J. J. Haringman, T. J. Smeets, A. H. Zwinderman, M. C. Kraan, P. J. Laud, S. Morgan, A. F. Nash, and P. P. Tak. 2004. Effects of oral prednisolone on biomarkers in synovial tissue and clinical improvement in rheumatoid arthritis. Arthritis Rheum. 50: 3783-3791.
4. Carman, C. V., P. T. Sage, T. E. Sciuto, M. A. de la Fuente, R. S. Geha, H. D. Ochs, H. F. Dvorak, A. M. Dvorak, and T. A. Springer. 2007. Transcellular diapedesis is initiated by invasive podosomes. Immunity 26: 784-797.
5. Linder, S., K. Hufner, U. Wintergerst, and M. Aepfelbacher. 2000. Microtubuledependent formation of podosomal adhesion structures in primary human macrophages. J. Cell Sci. 113: 4165-4176.
6. Cougoule, C., E. Van Goethem, V. Le Cabec, F. Lafouresse, L. Dupré, V. Mehraj, J. L. Mége, C. Lastrucci, and I. Maridonneau-Parini. 2012. Blood leukocytes and macrophages of various phenotypes have distinct abilities to form podosomes and to migrate in 3D environments. Eur. J. Cell Biol. 91: 938-949.
7. Van Goethem, E., R. Poincloux, F. Gauffre, I. Maridonneau-Parini, and V. Le Cabec. 2010. Matrix architecture dictates three-dimensional migration modes of human macrophages: differential involvement of proteases and podosome-like structures. J. Immunol. 184: 1049-1061.
8. Friedl, P., and B. Weigelin. 2008. Interstitial leukocyte migration and immune function. Nat. Immunol. 9: 960-969.
9. Lyons, R. M., L. E. Gentry, A. F. Purchio, and H. L. Moses. 1990. Mechanism of activation of latent recombinant transforming growth factor beta 1 by plasmin. J. Cell Biol. 110: 1361-1367.
10. Bugge, T. H., M. J. Flick, M. J. Danton, C. C. Daugherty, J. Romer, K. Dano, P. Carmeliet, D. Collen, and J. L. Degen. 1996. Urokinase-type plasminogen activator is effective in fibrin clearance in the absence of its receptor or tissue-type plasminogen activator. Proc. Natl. Acad. Sci. USA 93: 5899-5904.
11. Carmeliet, P., L. Moons, R. Lijnen, M. Baes, V. Lemaître, P. Tipping, A. Drew, Y. Eeckhout, S. Shapiro, F. Lupu, and D. Collen. 1997. Urokinase-generated plasmin activates matrix metalloproteinases during aneurysm formation. Nat. Genet. 17: 439-444.
12. Andreasen, P. A., R. Egelund, and H. H. Petersen. 2000. The plasminogen activation system in tumor growth, invasion, and metastasis. Cell. Mol. Life Sci. 57: 25-40.
13. Smith, H. W., and C. J. Marshall. 2010. Regulation of cell signalling by uPAR. Nat. Rev. Mol. Cell Biol. 11: 23-36.
14. Waltz, D. A., L. R. Natkin, R. M. Fujita, Y. Wei, and H. A. Chapman. 1997. Plasmin and plasminogen activator inhibitor type 1 promote cellular motility by regulating the interaction between the urokinase receptor and vitronectin. J. Clin. Invest. 100: 58-67.
15. Blasi, F., and P. Carmeliet. 2002. uPAR: a versatile signalling orchestrator. Nat. Rev. Mol. Cell Biol. 3: 932-943.
16. Sidenius, N., and F. Blasi. 2003. The urokinase plasminogen activator system in cancer: recent advances and implication for prognosis and therapy. Cancer Metastasis Rev. 22: 205-222.
17. Mondino, A., and F. Blasi. 2004. uPA and uPAR in fibrinolysis, immunity and pathology. Trends Immunol. 25: 450-455.
18. Shen, Y., Y. Guo, P. Mikus, R. Sulniute, M. Wilczynska, T. Ny, and J. Li. 2012. Plasminogen is a key proinflammatory regulator that accelerates the healing of acute and diabetic wounds. Blood 119: 5879-5887.
19. Schuliga, M., G. Westall, Y. Xia, and A. G. Stewart. 2013. The plasminogen activation system: new targets in lung inflammation and remodeling. Curr. Opin. Pharmacol. 13: 386-393.
20. Wei, Y., D. A. Waltz, N. Rao, R. J. Drummond, S. Rosenberg, and H. A. Chapman. 1994. Identification of the urokinase receptor as an adhesion receptor for vitronectin. J. Biol. Chem. 269: 32380-32388.
21. Mondino, A., M. Resnati, and F. Blasi. 1999. Structure and function of the urokinase receptor. Thromb. Haemost. 82(Suppl 1): 19-22.
22. Chapman, H. A., and Y. Wei. 2001. Protease crosstalk with integrins: the urokinase receptor paradigm. Thromb. Haemost. 86: 124-129.
23. Czekay, R. P., K. Aertgeerts, S. A. Curriden, and D. J. Loskutoff. 2003. Plasminogen activator inhibitor-1 detaches cells from extracellular matrices by inactivating integrins. J. Cell Biol. 160: 781-791.
24. Tarui, T., N. Andronicos, R. P. Czekay, A. P. Mazar, K. Bdeir, G. C. Parry, A. Kuo, D. J. Loskutoff, D. B. Cines, and Y. Takada. 2003. Critical role of integrin alpha 5 beta 1 in urokinase (uPA)/urokinase receptor (uPAR, CD87) signaling. J. Biol. Chem. 278: 29863-29872.
25. Chapman, H. A. 1997. Plasminogen activators, integrins, and the coordinated regulation of cell adhesion and migration. Curr. Opin. Cell Biol. 9: 714-724.
26. Ossowski, L., and J. A. Aguirre-Ghiso. 2000. Urokinase receptor and integrin partnership: coordination of signaling for cell adhesion, migration and growth. Curr. Opin. Cell Biol. 12: 613-620.
27. Czekay, R. P., and D. J. Loskutoff. 2009. Plasminogen activator inhibitors regulate cell adhesion through a uPAR-dependent mechanism. J. Cell. Physiol. 220: 655-663.
28. Ye, S., and E. J. Goldsmith. 2001. Serpins and other covalent protease inhibitors. Curr. Opin. Struct. Biol. 11: 740-745.
29. Seiffert, D., G. Ciambrone, N. V. Wagner, B. R. Binder, and D. J. Loskutoff. 1994. The somatomedin B domain of vitronectin. Structural requirements for the binding and stabilization of active type 1 plasminogen activator inhibitor. J. Biol. Chem. 269: 2659-2666.
30. Kjøller, L., S. M. Kanse, T. Kirkegaard, K. W. Rodenburg, E. Rønne, S. L. Goodman, K. T. Preissner, L. Ossowski, and P. A. Andreasen. 1997. Plasminogen activator inhibitor-1 represses integrin-and vitronectin-mediated cell migration independently of its function as an inhibitor of plasminogen activation. Exp. Cell Res. 232: 420-429.
31. Deng, G., S. A. Curriden, G. Hu, R. P. Czekay, and D. J. Loskutoff. 2001. Plasminogen activator inhibitor-1 regulates cell adhesion by binding to the somatomedin B domain of vitronectin. J. Cell. Physiol. 189: 23-33.
32. Hamilton, J. A., and J. Slywka. 1981. Stimulation of human synovial fibroblast plasminogen activator production by mononuclear cell supernatants. J. Immunol. 126: 851-855.
33. Hamilton, J. H., A. Bootes, P. E. Phillips, and J. Slywka. 1981. Human synovial fibroblast plasminogen activator. Modulation of enzyme activity by antiinflammatory steroids. Arthritis Rheum. 24: 1296-1303.
34. Hamilton, J. A., I. K. Campbell, J. Wojta, and D. Cheung. 1992. Plasminogen activators and their inhibitors in arthritic disease. Ann. N. Y. Acad. Sci. 667: 87-100.
35. Ronday, H. K., H. H. Smits, G. N. Van Muijen, M. S. Pruszczynski, R. J. Dolhain, E. J. Van Langelaan, F. C. Breedveld, and J. H. Verheijen. 1996. Difference in expression of the plasminogen activation system in synovial tissue of patients with rheumatoid arthritis and osteoarthritis. Br. J. Rheumatol. 35: 416-423.
36. Busso, N., V. Péclat, A. So, and A. P. Sappino. 1997. Plasminogen activation in synovial tissues: differences between normal, osteoarthritis, and rheumatoid arthritis joints. Ann. Rheum. Dis. 56: 550-557.
37. Del Rosso, M., G. Fibbi, and M. Matucci Cerinic. 1999. The urokinase-type plasminogen activator system and inflammatory joint diseases. Clin. Exp. Rheumatol. 17: 485-498.
38. Busso, N., and J. A. Hamilton. 2002. Extravascular coagulation and the plasminogen activator/plasmin system in rheumatoid arthritis. Arthritis Rheum. 46: 2268-2279.
39. Jin, T., A. Tarkowski, P. Carmeliet, and M. Bokarewa. 2003. Urokinase, a constitutive component of the inflamed synovial fluid, induces arthritis. Arthritis Res. Ther. 5: R9-R17.
40. Cook, A. D., E. L. Braine, I. K. Campbell, and J. A. Hamilton. 2002. Differing roles for urokinase and tissue-type plasminogen activator in collagen-induced arthritis. Am. J. Pathol. 160: 917-926.
41. Cook, A. D., C. M. De Nardo, E. L. Braine, A. L. Turner, R. Vlahos, K. J. Way, S. K. Beckman, J. C. Lenzo, and J. A. Hamilton. 2010. Urokinase-type plasminogen activator and arthritis progression: role in systemic disease with immune complex involvement. Arthritis Res. Ther. 12: R37.
42. Hamilton, J. A. 2008. Plasminogen activator/plasmin system in arthritis and inflammation: friend or foe Arthritis Rheum. 58: 645-648.
43. Lund, L. R., E. Rønne, A. L. Roldan, N. Behrendt, J. Rømer, F. Blasi, and K. Danø. 1991. Urokinase receptor mRNA level and gene transcription are strongly and rapidly increased by phorbol myristate acetate in human monocytelike U937 cells. J. Biol. Chem. 266: 5177-5181.
44. Gyetko, M. R., S. B. Shollenberger, and R. G. Sitrin. 1992. Urokinase expression in mononuclear phagocytes: cytokine-specific modulation by interferon-gamma and tumor necrosis factor-alpha. J. Leukoc. Biol. 51: 256-263.
45. Gyetko, M. R., R. F. Todd, III, C. C. Wilkinson, and R. G. Sitrin. 1994. The urokinase receptor is required for human monocyte chemotaxis in vitro. J. Clin. Invest. 93: 1380-1387.
46. Bryer, S. C., G. Fantuzzi, N. Van Rooijen, and T. J. Koh. 2008. Urokinase-type plasminogen activator plays essential roles in macrophage chemotaxis and skeletal muscle regeneration. J. Immunol. 180: 1179-1188.
47. Fleetwood, A. J., T. Lawrence, J. A. Hamilton, and A. D. Cook. 2007. Granulocyte-macrophage colony-stimulating factor (CSF) and macrophage CSFdependent macrophage phenotypes display differences in cytokine profiles and transcription factor activities: implications for CSF blockade in inflammation. J. Immunol. 178: 5245-5252.
48. Vu, T. H., J. M. Shipley, G. Bergers, J. E. Berger, J. A. Helms, D. Hanahan, S. D. Shapiro, R. M. Senior, and Z. Werb. 1998. MMP-9/gelatinase B is a key regulator of growth plate angiogenesis and apoptosis of hypertrophic chondrocytes. Cell 93: 411-422.
49. Lari, R., A. J. Fleetwood, P. D. Kitchener, A. D. Cook, D. Pavasovic, P. J. Hertzog, and J. A. Hamilton. 2007. Macrophage lineage phenotypes and osteoclastogenesis-complexity in the control by GM-CSF and TGF-beta. Bone 40: 323-336.
50. Lacey, D. C., A. Achuthan, A. J. Fleetwood, H. Dinh, J. Roiniotis, G. M. Scholz, M. W. Chang, S. K. Beckman, A. D. Cook, and J. A. Hamilton. 2012. Defining GM-CSF-and macrophage-CSF-dependent macrophage responses by in vitro models. J. Immunol. 188: 5752-5765.
51. Lenzo, J. C., A. L. Turner, A. D. Cook, R. Vlahos, G. P. Anderson, E. C. Reynolds, and J. A. Hamilton. 2012. Control of macrophage lineage populations by CSF-1 receptor and GM-CSF in homeostasis and inflammation. Immunol. Cell Biol. 90: 429-440.
52. Cougoule, C., V. Le Cabec, R. Poincloux, T. Al Saati, J. L. Mége, G. Tabouret, C. A. Lowell, N. Laviolette-Malirat, and I. Maridonneau-Parini. 2010. Threedimensional migration of macrophages requires Hck for podosome organization and extracellular matrix proteolysis. Blood 115: 1444-1452.
53. Klemke, M., E. Kramer, M. H. Konstandin, G. H. Wabnitz, and Y. Samstag. 2010. An MEK-cofilin signalling module controls migration of human T cells in 3D but not 2D environments. EMBO J. 29: 2915-2929.
54. Clark, E. S., A. S. Whigham, W. G. Yarbrough, and A. M. Weaver. 2007. Cortactin is an essential regulator of matrix metalloproteinase secretion and extracellular matrix degradation in invadopodia. Cancer Res. 67: 4227-4235.
55. Lijnen, H. R. 2001. Plasmin and matrix metalloproteinases in vascular remodeling. Thromb. Haemost. 86: 324-333.
56. Wolf, K., and P. Friedl. 2011. Extracellular matrix determinants of proteolytic and non-proteolytic cell migration. Trends Cell Biol. 21: 736-744.
57. Palecek, S. P., J. C. Loftus, M. H. Ginsberg, D. A. Lauffenburger, and A. F. Horwitz. 1997. Integrin-ligand binding properties govern cell migration speed through cell-substratum adhesiveness. Nature 385: 537-540.
58. Falcone, D. J., W. Borth, K. M. Khan, and K. A. Hajjar. 2001. Plasminogenmediated matrix invasion and degradation by macrophages is dependent on surface expression of annexin II. Blood 97: 777-784.
59. Nakayama, M., E. Yoshida, M. Sugiki, K. Anai, M. Maruyama, and H. Mihara. 2002. Up-regulation of the urokinase-type plasminogen activator receptor by monocyte chemotactic proteins. Blood Coagul. Fibrinolysis 13: 383-391.
60. Das, R., T. Burke, and E. F. Plow. 2007. Histone H2B as a functionally important plasminogen receptor on macrophages. Blood 110: 3763-3772.
61. Menshikov, M. Y., E. P. Elizarova, E. Kudryashova, A. V. Timofeyeva, Y. Khaspekov, R. S. Beabealashvilly, and A. Bobik. 2001. Plasmin-independent gelatinase B (matrix metalloproteinase-9) release by monocytes under the influence of urokinase. Biochemistry Mosc. 66: 954-959.
62. Zhang, Y., Z. H. Zhou, T. H. Bugge, and L. M. Wahl. 2007. Urokinase-type plasminogen activator stimulation of monocyte matrix metalloproteinase-1 production is mediated by plasmin-dependent signaling through annexin A2 and inhibited by inactive plasmin. J. Immunol. 179: 3297-3304.
63. O'Connell, P. A., A. P. Surette, R. S. Liwski, P. Svenningsson, and D. M. Waisman. 2010. S100A10 regulates plasminogen-dependent macrophage invasion. Blood 116: 1136-1146.
64. Gong, Y., E. Hart, A. Shchurin, and J. Hoover-Plow. 2008. Inflammatory macrophage migration requires MMP-9 activation by plasminogen in mice. J. Clin. Invest. 118: 3012-3024.
65. Palecek, S. P., C. E. Schmidt, D. A. Lauffenburger, and A. F. Horwitz. 1996. Integrin dynamics on the tail region of migrating fibroblasts. J. Cell Sci. 109: 941-952.
66. Wei, Y., M. Lukashev, D. I. Simon, S. C. Bodary, S. Rosenberg, M. V. Doyle, and H. A. Chapman. 1996. Regulation of integrin function by the urokinase receptor. Science 273: 1551-1555.
67. Novak, M. L., S. C. Bryer, M. Cheng, M. H. Nguyen, K. L. Conley, A. K. Cunningham, B. Xue, T. H. Sisson, J. S. You, T. A. Hornberger, and T. J. Koh. 2011. Macrophage-specific expression of urokinase-type plasminogen activator promotes skeletal muscle regeneration. J. Immunol. 187: 1448-1457.
68. Boyd, N. A., A. R. Bradwell, and R. A. Thompson. 1993. Quantitation of vitronectin in serum: evaluation of its usefulness in routine clinical practice. J. Clin. Pathol. 46: 1042-1045.
69. Kinne, R. W., B. Stuhlmuller, and G. R. Burmester. 2007. Cells of the synovium in rheumatoid arthritis. Macrophages. Arthritis Res. Ther. 9: 224.
70. Fuhrman, B. 2012. The urokinase system in the pathogenesis of atherosclerosis. Atherosclerosis 222: 8-14.