PAI-1 expression is required for epithelial cell migration in two distinct phases of in vitro wound repair

Journal of Cellular Physiology

Volumn 200, Issue 2, 2004, Pages 297-308

  Providence, Kirwin M ^a   Higgins, Paul J ^a  

^a ALBANY MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; 2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; ANTISENSE OLIGONUCLEOTIDE; DACTINOMYCIN; GREEN FLUORESCENT PROTEIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MYOSIN LIGHT CHAIN; NEUTRALIZING ANTIBODY; PLASMINOGEN ACTIVATOR INHIBITOR 1; SERINE PROTEINASE INHIBITOR;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL MIGRATION; CELL MOTILITY; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; EPIDERMIS; EPITHELIUM CELL; EXTRACELLULAR MATRIX; GENE CONTROL; GENE EXPRESSION; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; IN VITRO STUDY; KERATINOCYTE; KNOCKOUT MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; REPORTER GENE; SIGNAL TRANSDUCTION; SKIN INJURY; WOUND HEALING;

ANIMALS; ANIMALS, NEWBORN; BLOTTING, WESTERN; BUTADIENES; CELL MOVEMENT; CELL SEPARATION; CELLS, CULTURED; COLLAGEN; DOWN-REGULATION; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENZYME ACTIVATION; ENZYME INHIBITORS; FLAVONOIDS; GENE EXPRESSION REGULATION; GREEN FLUORESCENT PROTEINS; IMMUNOHISTOCHEMISTRY; KERATINOCYTES; KINETICS; LUMINESCENT PROTEINS; MICE; MICE, KNOCKOUT; MITOGEN-ACTIVATED PROTEIN KINASES; NITRILES; PLASMINOGEN ACTIVATOR INHIBITOR 1; RATS; RECOMBINANT PROTEINS; RNA, MESSENGER; SERINE PROTEINASE INHIBITORS; SKIN; WOUND HEALING;

EID: 3042775025     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcp.20016     Document Type: Article

References (84)

1. Akiyoshi S, Ishii M, Nemoto N, Kawabata M, Aburatani H, Miyazano K. 2001. Targets of transcriptional regulation by transforming growth factor-β: Expression profile analysis using oligonucleotide arrays. Jpn J Cancer Res 92:252-268.
2. Al-Fakhri N, Chavakis T, Schmidt-Woll T, Huang B, Cherian SM, Bobryshev YV, Lord RS, Katz N, Preissner KT. 2003. Induction of apoptosis in vascular cells by plasminogen activator inhibitor-1 and high molecular weight kininogen correlates with their anti-adhesive properties. Biol Chem 384:423-435.
3. Andreasen PA, Egelund R, Peterson HH. 2000. The plasminogen activation system in tumor growth, invasion, and metastasis. Cell Mol Life Sci 57:25-40.
4. Bajou K, Noel A, Gerard RD, Masson V, Brunner N, Holst-Hansen C, Skobe M, Fusenig NE, Carmeliet P, Collen D, Foidart JM. 1998. Absence of host plasminogen activator inhibitor 1 prevents cancer invasion and vascularization. Nat Med 4:923-928.
5. 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 G, Loskutoff D, Collen D, Carmeliet P, Foidart JM, Noel A. 2001. The plasminogen activator inhibitor PAI-1 controls in vivo tumor vascularization by interaction with proteases, not vitronectin. Implications for antiangiogenic stratagies. J Cell Biol 152:777-784.
6. Boehm JR, Kutz SM, Sage EH, Staiano-Coico L, Higgins PJ. 1999. Growth state-dependent regulation of plasminogen activator inhibitor type-1 gene expression during epithelial cell stimulation by serum and transforming growth factor-β1. J Cell Physiol 181:96-106.
7. Brooks TD, Slomp J, Quax PHA, De Bart ACW, Spencer MT, Verheijen JH, Charlton PA. 2001. Antibodies to PAI-1 alter the invasive and migratory properties of human tumour cells in vitro. Clin Exp Metastasis 18:445-453.
8. Cajot JF, Bamat J, Bergonzelli GE, Kruithof EK, Medcalf RL, Testuz J, Sordat B. 1990. Plasminogen-activator inhibitor type 1 is a potent natural inhibitor of extracellular matrix degradation by fibrosarcoma and colon carcinoma cells. Proc Natl Acad Sci USA 87:6939-6943.
9. Chapman HA. 1997. Plasminogen activators, integrins, the coordinate regulation of cell adhesion and migration. Curr Opin Cell Biol 9: 714-724.
10. Chazaud B, Ricoux R, Christov C, Plonquet A, Gherardi RK, Barlovatz-Meimon G. 2002. Promigratory effect of plasminogen activator inhibitor-1 on invasive breast cancer cell populations. Am J Path 160:237-246.
11. Ciambrone GJ, McKeown-Longo PJ. 1990. Plasminogen activator inhibitor type 1 stabilizes vitronectin-dependent adhesions in HT-1080 cells. J Cell Biol 111:2183-2195.
12. Coulombe PA. 1997. Towards a molecular definition of keratinocyte activation after acute injury to stratified epithelia. Biochem Biophys Res Comm 18:231-238.
13. Czekay RP, Aertgeerts K, Curriden SA, Loskutoff DJ. 2003. Plasminogen activator inhibitor-1 detaches cells from extracellular matrices by inactivating integrins. J Cell Biol 160:781-791.
14. Decline F, Rousselle P. 2001. Keratinocyte migration requires α2β1 integrin-mediated interaction with the laminin 5 72 chain. J Cell Sci 114:811-823.
15. Decline F, Okamoto O, Mallein-Gerin F, Helbert B, Bernaud J, Rigal D, Rousselle P. 2003. Keratinocyte motility induced by TGF-β1 is accompanied by dramatic changes in cellular interactions with laminin 5. Cell Motil Cytoskeleton 54:64-80.
16. Deng G, Curriden SA, Wang S, Rosenberg S, Loskutoff DJ. 1996. Is plasminogen activator inhibitor-1 the molecular switch that governs urokinase receptor-mediated cell adhesion and release? J Cell Biol 134:1563-1571.
17. Deng G, Curriden SA, Hu G, Czekay R-P, Loskutoff DJ. 2001. Plasminogen activator inhibitor-1 regulates cell adhesion by binding to the somatomedin B domain of vitronectin. J Cell Physiol 189:23-33.
18. Dieckgraefe BK, Weems DM, Santoro SA, Alpers DH. 1997. ERK and p38 MAP kinase pathways are mediators of intestinal epithelial wound-induced signal transduction. Biochem Biophys Res Comm 233:389-394.
19. Dlugosz AA, Glick AB, Tennenbaum T, Weinberg WC, Yuspa SH. 1995. Isolation and utilization of epidermal keratinocytes for oncogene research. Methods Enzymol 254:3-20.
20. Ellis PD, Hadfield KM, Pascall JC, Brown KD. 2001. Heparin-binding epidermal-growth-factor-like growth factor gene expression is induced by scrape-wounding epithelial cell monolayers: Involvement of mitogen-activated protein kinase cascades. Biochem J 354:99-106.
21. Farina AR, Coppa A, Tiberio A, Tacconelli A, Turco A, Colletta G, Gulino A, Mackay A,R. 1998. Transforming growth factor-β1 enhances the invasiveness of human MDA-MB-231 breast cancer cells by up-regulating urokinase activity. Int J Cancer 75:721-730.
22. Garlick JA, Taichman LB. 1994. Fate of human keratinocytes during reepithelialization in an organotypic culture model. Lab Invest 70: 916-924.
23. Goke M, Kanai M, Lynch-Davaney K, Podolsky DK. 1998. Rapid mitogen-activated protein kinase activation by transforming growth factor alpha in wounded rat intestinal epithelial cells. Gastroenterol 114:697-705.
24. Goldberg PL, MacNaughton DE, Clements RT, Minnear FL, Vincent PA. 2002. p38 MAPK activation by TGF-β1 increases MLC phorphorylation and endothelial monolayer permeability. Am J Physiol 282:L146-L154.
25. Gutierrez LS, Schulman A, Brito-Robinson T, Noria F, Ploplis VA, Castellino FJ. 2000. Tumor development is retarded in mice lacking the gene for urokinase-type plasminogen activator or its inhibitor, plasminogen activator inhibitor-1. Cancer Res 60:5839-5847.
26. Haase I, Evans R, Pofahl R, Watt FM. 2003. Regulation of keratinocyte shape, migration and wound epithelialization by IGF-1- and EGF-dependent signaling pathways. J Cell Sci 116: 3227-3238.
27. Higgins PJ, Ryan MP. 1989. Biochemical localization of the transformation-sensitive 52 kDa (p52) protein to the substratum contact regions of cultured rat fibroblasts. Butyrate induction, characterization, and quantification of p52 in v-ras transformed cells. Biochem J 257:173-182.
28. PAI-1 gene expression in butyrate-induced flat revertants of v-ras-transformed rat kidney cells: Mechanism of induction and involvement in the morphologic response. Biochem J 321:431-437.
29. Higgins PJ, Slack JK, Diegelmann RF, Staiano-Coico L. 1999. Differential regulation of PAI-1 gene expression in human fibroblasts pre-disposed to a fibrotic phenotype. Exp Cell Res 248:634-642.
30. Hua X, Liu X, Ansari DO, Lodish HF. 1998. Synergistic cooperation of TFE3 and smad proteins in TGF-β-induced transcription of the plasminogen activator inhibitor-1 gene. Genes Dev 12:3084-3095.
31. Irigoyen JP, Besser D, Nagamine Y. 1997. Cytoskeleton reorganization induces the urokinase-type plasminogen activator gene via the Ras/extracellular signal-regulated kinase (ERK) signaling pathway. J Biol Chem 272:1904-1909.
32. Jaakkola P, Kontusaari S, Kauppi T, Maata A, Jalkanen M. 1998. Wound reepithelialization activates a growth factor-responsive enhancer in migrating keratinocytes. FASEB J 12:959-969.
33. Jeffers M, Rong S, Vande Woude GF. 1996. Enhanced tumorigenicity and invasion-metastasis by hepatocyte growth factor/scatter factor-met signalling in human cells concomitant with induction of the urokinase proteolysis network. Mol Cell Biol 16:1115-1125.
34. Jensen PJ, Lavker RM. 1996. Modulation of the plasminogen activator cascade during enhanced epidermal proliferation in vivo. Cell Growth Differ 7:1793-1804.
35. Kjoller L, Kanse SM, Kirkegaard T, Rodenburg KW, Ronne E, Goodman SL, Preissner KT, Ossawski L, Andreasen PA. 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.
36. Klemke RL, Cai S, Giannini AL, Gallagher PJ, de Lanerolle P, Cheresh DA. 1997. Regulation of cell motility by mitogen-activated protein kinase. J Cell Biol 137:481-492.
37. Kutz SM, Nickey S, White LA, Higgins PJ. 1997. Induced PAI-1 mRNA expression and targeted protein accumulation are early G1 events in serum-stimulated rat kidney cell. J Cell Physiol 170:8-18.
38. Kutz SM, Hordines J, McKeown-Longo PJ, Higgins PJ. 2001. TGF-β1-induced PAI-1 gene expression requires MEK activity and cell-to-substrate adhesion. J Cell Sci 114:3905-3914.
39. Lawrence DA, Palaniappan S, Stefansson S, Olson ST, Francis-Chmura AM, Shore JD, Ginsburg D. 1997. Characterization of the binding of different conformational forms of plasminogen activator inhibitor-1 to vitronectin. Implications for the regulation of pericellular proteolysis. J Biol Chem 272:7676-7680.
40. Legrand C, Polette M, Tournier JM, de Bentzmann S, Huet E, Monteau M, Birembaut P. 2001. uPA/plasmin system-mediated MMP-9 activation is implicated in bronchial cell migration. Exp Cell Res 264:326-333.
41. Li F, Goncalves J, Faughnan K, Steiner MG, Pagan-Charry I, Esposito D, Chin B, Providence KM, Higgins PJ, Staiano-Coico L. 2000. Targeted inhibition of wound-induced PAI-1 expression alters migration and differentiation in human epidermal keratinocytes. Exp Cell Res 258:245-253.
42. Liu G, Shuman MA, Cohen RL. 1995. Co-expression of urokinase, urokinase receptor, and PAI-1 is necessary for optimum invasiveness of cultured lung cancer cells. Int J Cancer 60:501-506.
43. Loskutoff DJ, Curriden SA, Hu G, Deng G. 1999. Regulation of cell adhesion by PAI-1. APMIS 107:54-61.
44. Lund LR, Romer J, Bugge TH, Nielsen BS, Frandsen TL, Degen JL, Stephens RW, Dano K. 1999. Functional overlap between two classes of matrix-degrading proteases in wound healing. EMBO J 18:4645-4656.
45. Martin P. 1997. Wound healing-Aiming for perfect skin regeneration. Science 276:75-81.
46. Mazzalupo S, Wawersik MJ, Coulombe PA. 2002. An ex vivo assay to assess the potential of skin keratinocytes for wound epithelialization. J Invest Dermatol 118:866-870.
47. Mazzieri R, Masiero L, Zanetta L, Monea S, Onisto M, Garbisa S, Mignatti P. 1997. Control of type IV collagenase activity by components of the urokinase-plasmin system: A regulatory mechanism with cell-bound reactants. EMBO J 16:2319-2332.
48. McMahon GA, Petitclerc E, Stefansson S, Smith E, Wong MK, Westrick RJ, Ginsburg D, Brooks PC, Lawrence DA. 2001. Plasminogen activator inhibitor-1 regulates tumor growth and angiogenesis. J Biol Chem 276:33964-33968.
49. Mignatti P, Rifkin DB. 2000. Nonenzymatic interactions between proteinases and the cell surface: Novel roles in normal and malignant cell physiology. Adv Cancer Res 78:103-157.
50. Mu XC, Staiano-Coico L, Higgins PJ. 1998. Increased transcription and modified growth state-dependent expression of the plasminogen activator inhibitor type-1 gene characterize the senescent phenotype in human diploid fibroblasts. J Cell Physiol 174:90-98.
51. Nguyen DH, Catling AD, Webb DJ, Sankovic M, Walker LA, Somlyo AV, Weber MJ, Gonias SL. 1999. Myosin light chain kinase functions downstream of Ras/ERK to promote migration of urokinase-type plasminogen activator-stimulated cells in an integrin-selective manner. J Cell Biol 146:149-164.
52. Okedon LE, Sato Y, Rifkin DB. 1992. Urokinase-type plasminogen activator mediates basic growth factor-induced bovine endothelial migration independent of its proteolytic activity. J Cell Physiol 150: 258-263.
53. Pages G, Lenormand P, L'Allemain G, Chambaard JC, Meloche S, Pouyssegur J. 1993. Mitogen-activated protein kinases p42mapk and p44mapk are required for fibroblast proliferation. Proc Natl Acad Sci USA 90:8319-8323.
54. Palmieri D, Lee JW, Juliano RL, Church FC. 2002. Plasminogen activator inhibitor-1 and -3 increase cell adhesion and motility of MDA-MB-435 breast cancer cells. J Biol Chem 277:40950-40957.
55. Pawar S, Kartha S, Toback FG. 1995. Differential gene expression in migrating renal epithelial cells after wounding. J Cell Physiol 165: 556-565.
56. Pepper MS, Vassalli JD, Montesano R, Orci L. 1987. Urokinase-type plasminogen activator is induced in migrating capillary endothelial cells. J Cell Biol 105:2535-2541.
57. Pepper MS, Sappino AP, Montesano R, Orci L, Vassalli JD. 1992. Plasminogen activator inhibitor-1 is induced in migrating capillary endothelial cells. J Cell Physiol 153:129-139.
58. Pintucci G, Steinberg BM, Seghezzi G, Yun J, Apazidis A, Baumann FG, Grossi EA, Colvin SB, Mignatti P, Galloway AC. 1999. Mechanical endothelial damage results in basic fibroblast growth factor-mediated activation of extracellular signal-regulated kinases. Surgery 126:422-427.
59. Providence KM, Kutz SM, Staiano-Coico L, Higgins PJ. 2000. PAI-1 gene expression is regionally induced in wounded epithelial cell monolayers and required for injury repair. J Cell Physiol 182:269-280.
60. Providence KM, White LA, Tang J, Gonclaves J, Staiano-Coico L, Higgins PJ. 2002. Epithelial monolayer wounding stimulates binding of USF-1 to an E-box motif in the plasminogen activator inhibitor type 1 gene. J Cell Sci 115:3767-3777.
61. Reidy M, Irwin C, Linder V. 1995. Migration of arterial wall cells. Circ Res 78:405-414.
62. Reijerkerk A, Voest EE, Gebbink MF. 2000. No grip, no growth: The conceptual basis of excessive proteolysis in the treatment of cancer. Eur J Cancer 36:1695-1705.
63. Riccio A, Pedone PV, Lund LR, Olsen T, Olsen HS, Andreasen PA. 1992. Transforming growth factor β1-responsive element: Closely associated binding sites for USF and CCAAT-binding transcription factor-nuclear factor 1 in the type-1 plasminogen activator inhibitor gene. Mol Cell Biol 12:1846-1855.
64. Romer J, Lund LR, Kriksen J, Ralkiaer E, Zeheb R, Gelehrter TD, Dano K, Kristensen P. 1991. Differential expression of urokinase-type plasminogen activator and its type-1 inhibitor during healing of mouse skin wounds. J Invest Dermatol 97:803-811.
65. Romer J, Lund LR, Kriksen J, Pyke C, Kristensen P, Dano K. 1994. The receptor for urokinase-type plasmingoen activator is expressed by keratinocytes at the leading edge during re-epithelialization of mouse skin wounds. J Invest Dermatol 102:519-522.
66. Ryan MP, Higgins PJ. 1993. Growth state-regulated expression of p52(PAI-1) in normal rat kidney cells. J Cell Physiol 155:376-384.
67. Ryan MP, Kutz SM, Higgins PJ. 1996. Complex regulation of plasminogen activator inhibitor-type-1 (PAI-1) gene expression by serum and substrate adhesion. Biochem J 31:1041-1046.
68. Samarakoon R, Higgins PJ. 2002. MEK/ERK pathway mediates cell-shape-dependent plasminogen activator inhibitor type 1 gene expression upon drug-induced disruption of the microfilament and microtubule networks. J Cell Sci 115:3093-3103.
69. Santibanez JF, Frontelo P, Iglesias M, Martinez J, Quintanilla M. 1999. Urokinase expression and binding activity associated with transforming growth factor β1-induced migratory and invasive phenotype of mouse epidermal keratinocytes. J Cell Biochem 74:61-73.
70. Sato Y, Rifkin DB. 1988. Autocrine activities of basic fibroblast growth factor: Regulation of endothelial cell movement, plasminogen activator synthesis, and DNA synthesis. J Cell Biol 107:1199-1205.
71. Seebacher T, Manske M, Zoller J, Crabb J, Bade EG. 1992. The EGF-inducible protein EIP-1 of migrating normal and malignant rat liver epithelial cells is identical to plasminogen activator inhibitor 1 and is a component of the migration tracks. Exp Cell Res 203:504-507.
72. Seiffert D, Mimuro J, Schleef RR, Loskutoff DJ. 1994. Interactions between type 1 plasminogen activator inhibitor, extracellular matrix, and vitronectin. Cell Differ Dev 32:287-292.
73. Song QH, Singh RP, Richardson TP, Nugent MA, Trinkaus-Randall V. 2000. Transforming growth factor-β1 expression in cultured corneal fibroblasts in response to injury. J Cell Biochem 77:186-199.
74. Stefansson S, Lawrence DA. 1996. The serpin PAI-1 inhibits cell migration by blocking αvβ5 binding to vitronectin. Nature 383:441-443.
75. Stefansson S, Lawrence DA. 2003. Old dogs and new tricks: Proteases, inhibitors, and cell migration. Sci STKE 189:pe24.
76. Stefansson S, Petitclerc E, Wong MK, McMahon GA, Brooks PC, Lawrence DA. 2001. Inhibition of angiogenesis in vivo by plasminogen activator inhibitor-1. J Biol Chem 276:8135-8141.
77. Turchi L, Chassot AA, Rezzonico R, Yeow K, Loubat A, Ferrua B, Lenegrate G, Ortonne JP, Ponzio G. 2002. Dynamic characterization of the molecular events during in vitro epidermal wound healing. J Invest Dermatol 119:56-63.
78. Waltz DA, Natkin LR, Fujita RM, Wei Y, Chapman HA. 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.
79. Wawersik MJ, Mazzalupo S, Nguyen D, Coulombe PA. 2001. Increased level of keratin 16 alter epithelialization potential of mouse skin keratinocytes in vivo and ex vivo. Mol Biol Cell 12:3439-3450.
80. White LA, Bruzdzinski C, Kutz SM, Gelehrter TD, Higgins PJ. 2000. Growth state-dependent binding of USF-1 to a proximal promoter E box element in the rat plasminogen activator inhibitor type 1 gene. Exp Cell Res 260:127-135.
81. Zahm JM, Kaplan H, Herar AL, Doriot F, Pierrot D, Somelette P, Puchelle E. 1997. Cell migration and proliferation during the in vitro wound repair of the respiratory epithelium. Cell Motil Cytoskel 37:33-43.
82. Zavadil J, Bitzer M, Liang D, Yang YC, Massimi A, Kneitz S, Piek E, Bottinger EP. 2001. Genetic programs of epithelial cell plasticity directed by transforming growth factor-β. Proc Natl Acad Sci USA 98:6686-6691.
83. Zeigler ME, Chi Y, Schmidt T, Varani J. 1999. Role of ERK and JNK pathways in regulating cell motility and matrix metalloproteinase 9 production in growth factor-stimulated human epidermal keratinocytes. J Cell Physiol 180:271-284.
84. Zhou HM, Nichols A, Meda P, Vassalli JD. 2000. Urokinase-type plasminogen activator and its receptor synergize to promote pathogenic proteolysis. EMBO J 19:4817-4826.