Matrix-bound PAI-1 supports cell blebbing via RhoA/rock1 signaling

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Cartier Michaud, Amandine ^a   Malo, Michel ^a   Charrière Bertrand, Cécile ^a,b   Gadea, Gilles ^c   Anguille, Christelle ^c   Supiramaniam, Ajitha ^a   Lesne, Annick ^d,e   Delaplace, Franck ^a   Hutzler, Guillaume ^a   Roux, Pierre ^c   Lawrence, Daniel A ^f   Barlovatz Meimon, Georgia ^a,b  

^a UNIVERSITY OF EVRY   (France)

^b UNIVERSITÉ PARIS EST CRÉTEIL   (France)

^c Centre National de la Recherche Scientifique   (France)

^d INSTITUT DES HAUTES ÉTUDES SCIENTIFIQUES   (France)

^e UNIVERSITÉ PIERRE ET MARIE CURIE   (France)

^f UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MYOSIN LIGHT CHAIN PHOSPHATASE; PHOSPHOINOSITIDE DEPENDENT PROTEIN KINASE 1; PLASMINOGEN ACTIVATOR INHIBITOR 1; PROTEIN KINASE; RHO ASSOCIATED COIL CONTAINING PROTEIN KINASE 1; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG; IMMOBILIZED PROTEIN; RHO KINASE; ROCK1 PROTEIN, HUMAN; UROKINASE;

AMOEBOID EPITHELIAL TRANSITION; AMOEBOID MIGRATION; ARTICLE; CANCER CELL CULTURE; CARCINOGENESIS; CELL BLEBBING; CELL FUNCTION; CELL MEMBRANE; CELL MIGRATION; CELL STRAIN SW620; CELL TRANSFORMATION; CELLULAR DISTRIBUTION; COLORECTAL CANCER; CONTROLLED STUDY; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOFLUORESCENCE TEST; METASTASIS; PATHOPHYSIOLOGY; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; BIOLOGICAL MODEL; CELL MOTION; CELL SURFACE; COMPUTER SIMULATION; DRUG EFFECT; ENZYME ACTIVATION; MESODERM; METABOLISM; PATHOLOGY; TUMOR CELL LINE;

CELL LINE, TUMOR; CELL MOVEMENT; CELL SURFACE EXTENSIONS; COMPUTER SIMULATION; ENZYME ACTIVATION; EXTRACELLULAR MATRIX; HUMANS; IMMOBILIZED PROTEINS; MESODERM; MODELS, BIOLOGICAL; PLASMINOGEN ACTIVATOR INHIBITOR 1; PROTEIN BINDING; RHO-ASSOCIATED KINASES; RHOA GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION; UROKINASE-TYPE PLASMINOGEN ACTIVATOR;

EID: 84857395728     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0032204     Document Type: Article

References (57)

1. Pankova K, Rosel D, Novotny M, Brabek J, (2010) The molecular mechanisms of transition between mesenchymal and amoeboid invasiveness in tumor cells. Cell Mol Life Sci 67: 63-71.
2. Sabeh F, Shimizu-Hirota R, Weiss SJ, (2009) Protease-dependent versus-independent cancer cell invasion programs: three-dimensional amoeboid movement revisited. J Cell Biol 185: 11-19.
3. Wolf K, Mazo I, Leung H, Engelke K, von Andrian UH, et al. (2003) Compensation mechanism in tumor cell migration: mesenchymal-amoeboid transition after blocking of pericellular proteolysis. J Cell Biol 160: 267-277.
4. Wyckoff JB, Pinner SE, Gschmeissner S, Condeelis JS, Sahai E, (2006) ROCK- and myosin-dependent matrix deformation enables protease-independent tumor-cell invasion in vivo. Curr Biol 16: 1515-1523.
5. Sahai E, Marshall CJ, (2003) Differing modes of tumour cell invasion have distinct requirements for Rho/ROCK signalling and extracellular proteolysis. Nat Cell Biol 5: 711-719.
6. Kimura K, Ito M, Amano M, Chihara K, Fukata Y, et al. (1996) Regulation of myosin phosphatase by Rho and Rho-associated kinase (Rho-kinase). Science 273: 245-248.
7. Riento K, Ridley AJ, (2003) Rocks: multifunctional kinases in cell behaviour. Nat Rev Mol Cell Biol 4: 446-456.
8. Pinner S, Sahai E, (2008) PDK1 regulates cancer cell motility by antagonising inhibition of ROCK1 by RhoE. Nat Cell Biol 10: 127-137.
9. Friedl P, Wolf K, (2010) Plasticity of cell migration: a multiscale tuning model. J Cell Biol 188: 11-19.
10. Mantovani A, (2009) Cancer: Inflaming metastasis. Nature 457: 36-37.
11. Duffy MJ, Duggan C, (2004) The urokinase plasminogen activator system: a rich source of tumour markers for the individualised management of patients with cancer. Clin Biochem 37: 541-548.
12. Umeda T, Eguchi Y, Okino K, Kodama M, Hattori T, (1997) Cellular localization of urokinase-type plasminogen activator, its inhibitors, and their mRNAs in breast cancer tissues. J Pathol 183: 388-397.
13. Chorostowska-Wynimko J, Skrzypczak-Jankun E, Jankun J, (2004) Plasminogen activator inhibitor type-1: its structure, biological activity and role in tumorigenesis (Review). Int J Mol Med 13: 759-766.
14. Planus E, Barlovatz-Meimon G, Rogers RA, Bonavaud S, Ingber DE, et al. (1997) Binding of urokinase to plasminogen activator inhibitor type-1 mediates cell adhesion and spreading. J Cell Sci 110(Pt 9): 1091-1098.
15. Chazaud B, Ricoux R, Christov C, Plonquet A, Gherardi RK, et al. (2002) Promigratory effect of plasminogen activator inhibitor-1 on invasive breast cancer cell populations. Am J Pathol 160: 237-246.
16. 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.
17. Wang Z, Sosne G, Kurpakus-Wheater M, (2005) Plasminogen activator inhibitor-1 (PAI-1) stimulates human corneal epithelial cell adhesion and migration in vitro. Exp Eye Res 80: 1-8.
18. 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.
19. Stefansson S, Lawrence DA, (1996) The serpin PAI-1 inhibits cell migration by blocking integrin alpha V beta 3 binding to vitronectin. Nature 383: 441-443.
20. Stefansson S, Muhammad S, Cheng XF, Battey FD, Strickland DK, et al. (1998) Plasminogen activator inhibitor-1 contains a cryptic high affinity binding site for the low density lipoprotein receptor-related protein. J Biol Chem 273: 6358-6366.
21. Jo M, Thomas KS, Somlyo AV, Somlyo AP, Gonias SL, (2002) Cooperativity between the Ras-ERK and Rho-Rho kinase pathways in urokinase-type plasminogen activator-stimulated cell migration. J Biol Chem 277: 12479-12485.
22. Nguyen DH, Catling AD, Webb DJ, Sankovic M, Walker LA, et al. (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.
23. Aguirre Ghiso JA, (2002) Inhibition of FAK signaling activated by urokinase receptor induces dormancy in human carcinoma cells in vivo. Oncogene 21: 2513-2524.
24. Kjoller L, Hall A, (2001) Rac mediates cytoskeletal rearrangements and increased cell motility induced by urokinase-type plasminogen activator receptor binding to vitronectin. J Cell Biol 152: 1145-1157.
25. Liu D, Aguirre Ghiso J, Estrada Y, Ossowski L, (2002) EGFR is a transducer of the urokinase receptor initiated signal that is required for in vivo growth of a human carcinoma. Cancer Cell 1: 445-457.
26. Vial E, Sahai E, Marshall CJ, (2003) ERK-MAPK signaling coordinately regulates activity of Rac1 and RhoA for tumor cell motility. Cancer Cell 4: 67-79.
27. Smith HW, Marshall CJ, (2010) Regulation of cell signalling by uPAR. Nat Rev Mol Cell Biol 11: 23-36.
28. Malo M, Cartier-Michaud A, Fabre-Guillevin E, Hutzler G, Delaplace F, et al. (2010) When a collective outcome triggers a rare individual event: a mode of metastatic process in a cell population. Mathematical Population Studies 17: 136-165.
29. Charras GT, Hu CK, Coughlin M, Mitchison TJ, (2006) Reassembly of contractile actin cortex in cell blebs. J Cell Biol 175: 477-490.
30. Fackler OT, Grosse R, (2008) Cell motility through plasma membrane blebbing. J Cell Biol 181: 879-884.
31. Leverrier Y, Ridley AJ, (2001) Apoptosis: caspases orchestrate the ROCK 'n' bleb. Nat Cell Biol 3: E91-93.
32. Wang N, Planus E, Pouchelet M, Fredberg JJ, Barlovatz-Meimon G, (1995) Urokinase receptor mediates mechanical force transfer across the cell surface. Am J Physiol 268: C1062-1066.
33. Samarakoon R, Higgins CE, Higgins SP, Kutz SM, Higgins PJ, (2005) Plasminogen activator inhibitor type-1 gene expression and induced migration in TGF-beta1-stimulated smooth muscle cells is pp60(c-src)/MEK-dependent. J Cell Physiol 204: 236-246.
34. Huang Y, Haraguchi M, Lawrence DA, Border WA, Yu L, et al. (2003) A mutant, noninhibitory plasminogen activator inhibitor type 1 decreases matrix accumulation in experimental glomerulonephritis. J Clin Invest 112: 379-388.
35. Nykjaer A, Conese M, Christensen EI, Olson D, Cremona O, et al. (1997) Recycling of the urokinase receptor upon internalization of the uPA:serpin complexes. Embo J 16: 2610-2620.
36. Stefansson S, Lawrence DA, Argraves WS, (1996) Plasminogen activator inhibitor-1 and vitronectin promote the cellular clearance of thrombin by low density lipoprotein receptor-related proteins 1 and 2. J Biol Chem 271: 8215-8220.
37. Strickland DK, Gonias SL, Argraves WS, (2002) Diverse roles for the LDL receptor family. Trends Endocrinol Metab 13: 66-74.
38. Providence KM, Higgins SP, Mullen A, Battista A, Samarakoon R, et al. (2008) SERPINE1 (PAI-1) is deposited into keratinocyte migration "trails" and required for optimal monolayer wound repair. Arch Dermatol Res 300: 303-310.
39. Rougier JP, Guia S, Hagege J, Nguyen G, Ronco PM, (1998) PAI-1 secretion and matrix deposition in human peritoneal mesothelial cell cultures: transcriptional regulation by TGF-beta 1. Kidney Int 54: 87-98.
40. 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 ECM migration tracks. Exp Cell Res 203: 504-507.
41. Maxwell CA, McCarthy J, Turley E, (2008) Cell-surface and mitotic-spindle RHAMM: moonlighting or dual oncogenic functions? J Cell Sci 121: 925-932.
42. Lee TH, D'Asti E, Magnus N, Al-Nedawi K, Meehan B, et al. (2011) Microvesicles as mediators of intercellular communication in cancer-the emerging science of cellular 'debris'. Semin Immunopathol 33 (5): 455-467.
43. Diehl HC, Stuhler K, Klein-Scory S, Volmer MW, Schoneck A, et al. (2007) A catalogue of proteins released by colorectal cancer cells in vitro as an alternative source for biomarker discovery. Proteomics Clin Appl 1: 47-61.
44. van Niel G, Raposo G, Candalh C, Boussac M, Hershberg R, et al. (2001) Intestinal epithelial cells secrete exosome-like vesicles. Gastroenterology 121: 337-349.
45. Maquerlot F, Galiacy S, Malo M, Guignabert C, Lawrence DA, et al. (2006) Dual role for plasminogen activator inhibitor type 1 as soluble and as matricellular regulator of epithelial alveolar cell wound healing. Am J Pathol 169: 1624-1632.
46. Tomasini-Johansson BR, Sundberg C, Lindmark G, Gailit JO, Rubin K, (1994) Vitronectin in colorectal adenocarcinoma-synthesis by stromal cells in culture. Exp Cell Res 214: 303-312.
47. Minor KH, Peterson CB, (2002) Plasminogen activator inhibitor type 1 promotes the self-association of vitronectin into complexes exhibiting altered incorporation into the extracellular matrix. J Biol Chem 277: 10337-10345.
48. 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.
49. Aaboe M, Offersen BV, Christensen A, Andreasen PA, (2003) Vitronectin in human breast carcinomas. Biochim Biophys Acta 1638: 72-82.
50. Thiery JP, (2002) Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer 2: 442-454.
51. Friedl P, Wolf K, (2009) Proteolytic interstitial cell migration: a five-step process. Cancer Metastasis Rev 28: 129-135.
52. Vinot S, Anguille C, de Toledo M, Gadea G, Roux P, (2008) Analysis of cell migration and its regulation by Rho GTPases and p53 in a three-dimensional environment. Methods Enzymol 439: 413-424.
53. Dass K, Ahmad A, Azmi AS, Sarkar SH, Sarkar FH, (2008) Evolving role of uPA/uPAR system in human cancers. Cancer Treat Rev 34: 122-136.
54. Heegaard CW, Simonsen AC, Oka K, Kjoller L, Christensen A, et al. (1995) Very low density lipoprotein receptor binds and mediates endocytosis of urokinase-type plasminogen activator-type-1 plasminogen activator inhibitor complex. J Biol Chem 270: 20855-20861.
55. Cubellis MV, Wun TC, Blasi F, (1990) Receptor-mediated internalization and degradation of urokinase is caused by its specific inhibitor PAI-1. Embo J 9: 1079-1085.
56. Czekay RP, Kuemmel TA, Orlando RA, Farquhar MG, (2001) Direct binding of occupied urokinase receptor (uPAR) to LDL receptor-related protein is required for endocytosis of uPAR and regulation of cell surface urokinase activity. Mol Biol Cell 12: 1467-1479.
57. Estreicher A, Muhlhauser J, Carpentier JL, Orci L, Vassalli JD, (1990) The receptor for urokinase type plasminogen activator polarizes expression of the protease to the leading edge of migrating monocytes and promotes degradation of enzyme inhibitor complexes. J Cell Biol 111: 783-792.