Urokinase receptor mediates lung fibroblast attachment and migration toward provisional matrix proteins through interaction with multiple integrins

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 297, Issue 1, 2009, Pages

  Zhu, Sha ^a   Gladson, Candece L ^b,d   White, Kimberly E ^a   Ding, Qiang ^a   Stewart Jr , Jerry ^b   Jin, Tong H ^a,d   Chapman Jr , Harold A ^c   Olman, Mitchell A ^a,b,d  

^a University of Alabama at Birmingham   (United States)

^b University of Alabama at Birmingham   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d LERNER RESEARCH INSTITUTE   (United States)

Author keywords

Fibrosis; Plasmin; Pulmonary

Indexed keywords

ALPHA INTEGRIN; ALPHAVBETA5 INTEGRIN; COLLAGEN; FIBRONECTIN; INTEGRIN; MATRIX PROTEIN; UROKINASE; UROKINASE RECEPTOR; VERY LATE ACTIVATION ANTIGEN 1; VERY LATE ACTIVATION ANTIGEN 2; VERY LATE ACTIVATION ANTIGEN 3; VERY LATE ACTIVATION ANTIGEN 5; VITRONECTIN; VITRONECTIN RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL ADHESION; CELL INVASION; CELL MIGRATION; CELL MOTILITY; CELL SPREADING; CELL TRANSFORMATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; LUNG FIBROBLAST; LUNG FIBROSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

ADULT; ANIMALS; CATTLE; CELL ADHESION; CELL MOVEMENT; CELL SURFACE EXTENSIONS; COLLAGEN; EXTRACELLULAR MATRIX PROTEINS; FIBRINOGEN; FIBROBLASTS; FIBRONECTINS; FIBROSIS; HUMANS; INTEGRINS; LUNG; MICE; PROTEIN BINDING; PROTEIN SUBUNITS; PROTEIN TRANSPORT; RECEPTORS, UROKINASE PLASMINOGEN ACTIVATOR; VITRONECTIN; WOUND HEALING;

EID: 67650069963     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.90283.2008     Document Type: Article

References (72)

1. Abraham E, Gyetko MR, Kuhn K, Arcaroli J, Strassheim D, Park JS, Shetty S, Idell S. Urokinase-type plasminogen activator potentiates lipopolysaccharide-induced neutrophil activation. J Immunol 170: 5644-5651, 2003.
2. Aguirre Ghiso JA, Kovalski K, Ossowski L. Tumor dormancy induced by downregulation of urokinase receptor in human carcinoma involves integrin and MAPK signaling. J Cell Biol 147: 89-104, 1999.
3. Bajou K, Masson V, Gerard RD, Schmitt PM, Albert V, Praus M, Lund LR, Frandsen TL, Brunner N, Dano K, Fusenig NE, Weidle U, Carmeliet P, Loskutoff D, Collen D, Carmeliet G, Foidart JM, Noel A. The plasminogen activator inhibitor PAI-1 controls in vivo tumor vascularization by interaction with proteases, not vitronectin. Implications for antiangiogenic strategies. J Cell Biol 152: 777-784, 2001.
4. Bajou K, Noel A, Gerard RD, Masson V, Brunner N, Holst-Hansen C, Skobe M, Fusenig NE, Carmeliet P, Collen D, Foidart JM. Absence of host plasminogen activator inhibitor 1 prevents cancer invasion and vascularization. Nat Med 4: 923-928, 1998.
5. Behrendt N, Renne E, Ploug M, Petri T, Lober D, Nielsen LS, Schleuning WD, Blasi F, Appella E, Dano K. The human receptor for urokinase plasminogen activator. J Biol Chem 265: 6453-6460, 1990.
6. Bernstein AM, Twining SS, Warejcka DJ, Tall E, Masur SK. Urokinase receptor clevage: a crucial step in fibroblast-to-myofibroblast differentiation. Mol Biol Cell 18: 2716-2727, 2007.
7. Berrier AL, Yamada KM. Cell-matrix adhesion. J Cell Physiol 213: 565-573, 2007.
8. Besser D, Verde P, Nagamine Y, Blasi F. Signal transduction and the u-PA/u-PAR system. Fibrinolysis 10: 215-237, 1996.
9. Bitterman P. Pathogenesis of fibrosis after lung injury. Am J Med 92: 139S-143S, 1992.
10. Blasi F. The urokinase receptor. A cell surface, regulated chemokine. APMIS 107: 96-101, 1999.
11. Blasi F, Carmeliet P. UPAR: A versatile signalling orchestrator. Nat Rev Mol Cell Biol 3: 932-943, 2002.
12. Carmeliet P, Moons L, Lijnen R, Baes M, Lemaitre V, Tipping P, Drew A, Eeckhout Y, Shapiro S, Lupu F, Collen D. Urokinase-generated plasmin activates matrix metalloproteinases during aneurysm formation. Nat Genet 17: 439-444, 1997.
13. Chapman HA. Plasminogen activators, integrins, and the coordinated regulation of cell adhesion and migration. Curr Opin Cell Biol 9: 714-724, 1997.
14. Chaurasia P, Aguirre-Ghiso JA, Liang OD, Gardsvoll H, Ploug M, Ossowski L. A region in urokinase plasminogen receptor domain III controlling a functional association with alpha5beta1 integrin and tumor growth. J Biol Chem 281: 14852-14863, 2006.
15. Degryse B, Resnati M, Czekay RP, Loskutoff DJ, Blasi F. Domain 2 of the urokinase receptor contains an integrin-interacting epitope with intrinsic signaling activity: generation of a new integrin inhibitor. J Biol Chem 280: 24792-24803, 2005.
16. Ding Q, Gladson CL, Wu H, Hayasaka H, Olman MA. Focal adhesion kinase (FAK)-related non-kinase inhibits myofibroblast differentiation through differential MAPK activation in a FAK-dependent manner. J Biol Chem 283: 26839-26849, 2008.
17. Eitzman DT, McCoy RD, Zheng X, Fay WP, Shen T, Ginsburg D, Simon RH. Bleomycin-induced pulmonary fibrosis in transgenic mice that either lack or overexpress the murine plasminogen activator inhibitor-1 gene. J Clin Invest 1: 232-237, 1996.
18. Ghosh S, Johnson JJ, Sen R, Mukhopadhyay S, Liu S, Zhang F, Wei Y, Chapman HA, Stack MS. Functional relevance of urinary-type plasminogen activator receptor-alpha3beta1 integrin association in proteinase regulatory pathways. J Biol Chem 281: 13021-13029, 2006.
19. Giancotti FG, Ruoslahti E. Integrin signaling. Science 285: 1028-1032, 1999.
20. Gladson CL, Stewart JE, Olman MA, Chang PL, Schnapp LM, Grammer JR, Benveniste EN. Attachment of primary neonatal rat astrocytes to vitronectin is mediated by integrins alphavbeta5 and alpha8beta1: modulation by the type 1 plasminogen activator inhibitor. Neurosci Lett 283: 157-161, 2000.
21. Gyetko MR, Chen GH, McDonald RA, Goodman R, Huffnagle GB, Wilkinson CC, Fuller JA, Toews GB. Urokinase is required for the pulmonary inflammatory response to Cryptococcus neoformans. J Clin Invest 97: 1818-1826, 1996.
22. Gyetko MR, Sud S, Kendall T, Fuller JA, Newstead MW, Standiford TJ. Urokinase receptor-deficient mice have impaired neutrophil recruitment in response to pulmonary pseudomonas aeruginosa infection. J Immunol 165: 1513-1519, 2000.
23. Gyetko MR, Todd RF, Wilkinson CC, Sitrin RG. The urokinase receptor is required for human monocyte chemotaxis in vitro. J Clin Invest 93: 1380-1387, 1994.
24. Heiligenhaus A, Steinmetz B, Lapuente R, Krallmann P, Althaus C, Steinkamp WK, Dick B. Recombinant tissue plasminogen activator in cases with fibrin formation after cataract surgery: a prospective randomised multicentre study. Br J Ophthalmol 82: 810-815, 1998.
25. Hemler ME. Tetraspanin proteins mediate cellular penetration, invasion, and fusion events and define a novel type of membrane microdomain. Annu Rev Cell Dev Biol 19: 397-422, 2003.
26. Horan GS, Wood S, Ona V, Li dJ, Lukashev ME, Weinreb PH, Simon KJ, Hahm K, Allaire NE, Rinaldi NJ, Goyal J, Feghali-Bostwick CA, Matteson EL, O'Hara C, Lafyatis R, Davis GS, Huang X, Sheppard D, Violette SM. Partial inhibition of integrin alpha(v)beta6 prevents pulmonary fibrosis without exacerbating inflammation. Am J Respir Crit Care Med 177: 56-65, 2008.
27. Horowitz JC, Rogers DS, Simon RH, Sisson TH, Thannickal VJ. Plasminogen activation induced pericellular fibronectin proteolysis promotes fibroblast apoptosis. Am J Respir Cell Mol Biol 38: 78-87, 2008.
28. Kaikita K, Fogo AB, Ma L, Schoenhard JA, Brown NJ, Vaughan DE. Plasminogen activator inhibitor-1 deficiency prevents hypertension and vascular fibrosis in response to long-term nitric oxide synthase inhibition. Circulation 104: 839-844, 2001.
29. Kim KK, Kugler MC, Wolters PJ, Robillard L, Galvez MG, Brumwell AN, Sheppard D, Chapman HA. Alveolar epithelial cell mesenchymal transition develops in vivo during pulmonary fibrosis and is regulated by the extracellular matrix. Proc Natl Acad Sci USA 103: 13180-13185, 2006.
30. Kitching AR, Holdsworth SR, Ploplis VA, Plow EF, Collen D, Carmeliet P, Tipping PG. Plasminogen and plasminogen activators protect against renal injury in crescentic glomerulonephritis. J Exp Med 185: 963-968, 1997.
31. Kjoller L, Hall A. Rac mediates cytoskeletal rearrangements and increased cell motility induced by urokinase-type plasminogen activator receptor binding to vitronectin. J Cell Biol 152: 1145-1157, 2001.
32. Li S, Van Den Diepstraten C, D'Souza SJ, Chan BM, Pickering JG. Vascular smooth muscle cells orchestrate the assembly of type I collagen via alpha2beta1 integrin, RhoA, and fibronectin polymerization. Am J Pathol 163: 1045-1056, 2003.
33. Liu D, Aguirre Ghiso J, Estrada Y, Ossowski L. EGFR is a transducer of the urokinase receptor initiated signal that is required for in vivo growth of a human carcinoma. Cancer Cells 1: 445-457, 2002.
34. Lu M, Munger JS, Steadele M, Busald C, Tellier M, Schnapp LM. Integrin alpha8beta1 mediates adhesion to LAP-TGFbeta1. J Cell Sci 15: 4641-4648, 2002.
35. Madsen CD, Ferraris GM, Andolfo A, Cunningham O, Sidenius N. uPAR-induced cell adhesion and migration: vitronectin provides the key. J Cell Biol 177: 927-939, 2007.
36. Monaghan E, Gueorguiev V, Wilkins-Port C, McKeown-Longo PJ. The receptor for urokinase-type plasminogen activator regulates fibronectin matrix assembly in human skin fibroblasts. J Biol Chem 279: 1400-1407, 2004.
37. Munger JS, Huang X, Kawakatsu H, Griffiths MJ, Dalton SL, Wu J, Pittet JF, Kaminski N, Garat C, Matthay MA, Rifkin DB, Sheppard D. The integrin αvβ6 binds and activates latent TGF-β1: a mechanism for regulating pulmonary inflammation and fibrosis. Cell 96: 319-328, 1999.
38. Oda T, Jung YO, Kim HS, Cai X, Lopez-Guisa JM, Ikeda Y, Eddy AA. PAI-1 deficiency attenuates the fibrogenic response to ureteral obstruction. Kidney Int 60: 587-596, 2001.
39. Olman MA. Mechanisms of fibroproliferation in acute lung injury. In: Acute Respiratory Distress Syndrome, edited by Matthay MA, Lenfant C. New York: Marcel Dekker, 2003, p. 313-354.
40. Olman MA, Simmons WL, Pollman DJ, Loftis AY, Bini A, Miller EJ, Fuller GM, Rivera K. Polymerization of fibrinogen in murine bleomycin-induced lung injury. Am J Physiol Lung Cell Mol Physiol 271: L519-L526, 1996.
41. Olman MA, White KE, Ware L, Simmons WL, Pugin J, Benveniste EN, Matthay MA, Zhu S. Pulmonary edema fluid from patients with early lung injury stimulates fibroblast proliferation through IL-1beta-induced IL-6 expression. J Immunol 172: 2668-2677, 2004.
42. Ossowski L, Aguirre-Ghiso JA. Urokinase receptor and integrin partnership: coordination of signaling for cell adhesion, migration and growth. Curr Opin Cell Biol 12: 613-620, 2000.
43. Pijuan-Thompson V, Gladson CL. Ligation of integrin alphavbeta1 is required for integrin alphavbeta3 internalization of vitronectin. J Biol Chem 272: 2736-2743, 1997.
44. Ploug M, Ronne E, Behrendt N, Jensen AL, Blasi F, Dano K. Cellular receptor for urokinase plasminogen activator. J Biol Chem 266: 1926-1933, 1991.
45. Puthawala K, Hadjiangelis N, Jacoby SC, Bayongan E, Zhao Z, Yang Z, Devitt ML, Horan GS, Weinreb PH, Lukashev ME, Violette SM, Grant KS, Colarossi C, Formenti SC, Munger JS. Inhibition of integrin alpha(v)beta6, an activator of latent transforming growth factor-beta, prevents radiation-induced lung fibrosis. Am J Crit Care 177: 82-90, 2008.
46. Resnati M, Pallavicini I, Wang JM, Oppenheim J, Serhan CN, Romano M, Blasi F. The fibrinolytic receptor for urokinase activates the G protein-coupled chemotactic receptor FPRL1 LXA4R. Proc Natl Acad Sci USA 99: 1359-1364, 2002.
47. Sheppard D. Roles of alphav integrins in vascular biology and pulmonary pathology. Curr Opin Cell Biol 16: 552-557, 2004.
48. Shetty S, Kumar A, Johnson AR, Pueblitz S, Holiday D, Raghu G, Idell S. Differential expression of the urokinase receptor in fibroblasts from normal and fibrotic human lungs. Am J Respir Cell Mol Biol 15: 78-87, 1996.
49. Sidenius N, Andolfo A, Fesce R, Blasi F. Urokinase regulates vitronectin binding in vivo and in vitro by controlling urokinase receptor oligomerization. J Biol Chem 277: 27982-27990, 2002.
50. Simon DI, Ezratty AM, Francis S, Rennke H, Loscalzo J. Fibrin(ogen) is internalized and degraded by activated human monocytiod cells via mac-1 (CD11b/CD18): A non-plasmin fibrinolytic pathway. Blood 82: 2414-2422, 1993.
51. Simon DI, Rao NK, Xu H, Majdic O, Ronne E, Kobzik L, Chapman HA. Mac-1 (CD11b/CD18) and the urokinase receptor (CD87) form a functional unit on monocytic cells. Blood 88: 3185-3194, 1996.
52. Simon DI, Wei Y, Zhang L, Rao NK, Xu H, Chen Z, Liu Q, Rosenberg S, Chapman HA. Identification of a urokinase receptor-integrin interaction site. Promiscuous regulator of integrin function. J Biol Chem 275: 10228-10234, 2000.
53. Sitrin RG, Johnson DR, Pan PM, Harsh DM, Huang J, Petty HR, Blackwood RA. Lipid raft compartmentalization of urokinase receptor signaling in human neutrophils. Am J Respir Cell Mol Biol 30: 233-241, 2004.
54. Sitrin RG, Pan PM, Blackwood RA, Huang J, Petty HR. Cutting edge: evidence for a signaling partnership between urokinase receptors (CD87) and L-selectin (CD62L) in human polymorphonuclear neutrophils. J Immunol 166: 4822-4825, 2001.
55. Stefansson S, Petitclerc E, Wong MK, McMahan GA, Brooks PC, Lawrence DA. Inhibition of angiogenesis in vivo by plasminogen activator inhibitor-1. J Biol Chem 276: 8135-8141, 2001.
56. Suganuma H, Sata A, Tamura R, Chida K. Enhanced migration of fibroblasts derived from lungs with fibrotic lesions. Thorax 50: 984-989, 1995.
57. Swaisgood CM, French EL, Noga C, Simon RH, Ploplis VA. The development of bleomycin-induced pulmonary fibrosis in mice deficient for components of the fibrinolytic system. Am J Pathol 157: 177-187, 2000.
58. Tager AM, Kradin RL, LaCamera P, Bercury SD, Campanella GSV, Leary CP, Polosukhin V, Zhao LH, Sakamoto H, Blackwell TS, Luster AD. Inhibition of pulmonary fibrosis by the chemokine IP-10/CXCL10. Am J Respir Cell Mol Biol 31: 395-404, 2004.
59. Tager AM, LaCamera P, Shea BS, Campanella GS, Selman M, Zhao Z, Polosukhin V, Wain J, Karimi-Shah BA, Kim ND, Hart WK, Pardo A, Blackwell TS, Xu Y, Chung CY, Luster AD. The lysophosphatidic acid receptor LPA1 links pulmonary fibrosis to lung injury by mediating fibroblast recruitment and vascular leak. Nat Med 14: 45-54, 2008.
60. Thannickal VJ, Lee DY, White ES, Cui Z, Larios JM, Chacon R, Horowitz JC, Day RM, Thomas PE. Myofibroblast differentiation by transforming growth factor-beta1 is dependent on cell adhesion and integrin signaling via focal adhesion kinase. J Biol Chem 278: 12384-12389, 2003.
61. Vayalil PK, Olman M, Murphy-Ullrich JE, Postlethwait EM, Liu RM. Glutathione restores collagen degradation in TGF-beta-treated fibroblasts by blocking plasminogen activator inhibitor-1 expression and activating plasminogen. Am J Respir Cell Mol Biol 289: L937-L945, 2005.
62. Velling T, Risteli J, Wennerberg K, Mosher DF, Johansson S. Polymerization of type I and III collagens is dependent on fibronectin and enhanced by integrins alpha11beta1 and alpha2beta1. J Biol Chem 277: 37377-37381, 2002.
63. Waltz DA, Fujita RM, Yang X, Natkin L, Zhuo S, Gerard CJ, Rosenberg S, Chapman HA. Nonproteolytic role for the urokinase receptor in cellular migration in vivo. Am J Respir Cell Mol Biol 22: 316-322, 2000.
64. Wei C, Moller CC, Altintas MM, Li J, Schwarz K, Zacchigna S, Xie L, Henger A, Schmid H, Rastaldi MP, Cowan P, Kretzler M, Parrilla R, Bendayan M, Gupta V, Nikolic B, Kalluri R, Carmeliet P, Mundel P, Reiser J. Modification of kidney barrier function by the urokinase receptor. Nat Med 14: 55-63, 2008.
65. Wei Y, Czekay RP, Robillard L, Kugler MC, Zhang F, Kim KK, Xiong JP, Humphries MJ, Chapman HA. Regulation of alpha5beta1 integrin conformation and function by urokinase receptor binding. J Cell Biol 168: 501-511, 2006.
66. Wei Y, Eble JA, Wang Z, Kreidberg JA, Chapman HA. Urokinase receptors promote beta1 integrin function through interactions with integrin alpha3beta1. Mol Biol Cell 12: 2975-2986, 2001.
67. Wei Y, Lukashev M, Simon DI, Bodary SC, Rosenberg S, Doyle MV, Chapman HA. Regulation of integrin function by the urokinase receptor. Science 273: 1551-1555, 1996.
68. Wei Y, Tang CH, Kim Y, Robillard L, Zhang F, Kugler MC, Chapman HA. Urokinase receptors are required for alpha5beta1 integrin-mediated signaling in tumor cells. J Biol Chem 282: 3929-3939, 2007.
69. Wei Y, Waltz DA, Rao N, Drummond RJ, Rosenberg S, Chapman HA. Identification of the urokinase receptor as an adhesion receptor for vitronectin. J Biol Chem 269: 32380-32388, 1994.
70. White ES, Thannickal VJ, Carskadon SL, Dickie EG, Livant DL, Markwart S, Toews GB, Arenberg DA. Integrin alpha4beta1 regulates migration across basement membranes by lung fibroblasts: a role for phosphatase and tensin homologue deleted on chromosome 10. Am J Respir Crit Care Med 168: 436-442, 2003.
71. Xia H, Diebold D, Nho R, Perlman D, Kleidon J, Kahm J, Avdulov S, Peterson M, Nerva J, Bitterman P, Henke C. Pathological integrin signaling enhances proliferation of primary lung fibroblasts from patients with idiopathic pulmonary fibrosis. J Exp Med 205: 1659-1672, 2008.
72. Zhang F, Tom CC, Kugler MC, Ching TT, Kreidberg JA, Wei Y, Chapman HA. Distinct ligand binding sites in integrin alpha3beta1 regulate matrix adhesion and cell-cell contact. J Cell Biol 163: 177-188, 2003.