Clathrin and LRP-1-independent constitutive endocytosis and recycling of uPAR

PLoS ONE

Volumn 3, Issue 11, 2008, Pages

  Cortese, Katia ^a   Sahores, Macarena ^b,c   Madsen, Chris D ^b,d   Tacchetti, Carlo ^a   Blasi, Francesco ^b  

^a UNIVERSITY OF GENOA   (Italy)

^b VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMILORIDE; CLATHRIN; EARLY ENDOSOME ANTIGEN 1; LIGAND; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN CDC42; RAC1 PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UROKINASE RECEPTOR; MONOMERIC GUANINE NUCLEOTIDE BINDING PROTEIN; PLASMINOGEN ACTIVATOR; PLASMINOGEN ACTIVATOR INHIBITOR 1;

ARTICLE; CELL MEMBRANE TRANSPORT; CELL SURFACE; CONTROLLED STUDY; DOWN REGULATION; ELECTRON MICROSCOPY; ENDOCYTOSIS; ENDOSOME; ENZYME ACTIVITY; HUMAN; HUMAN CELL; INTERNALIZATION; LIGAND BINDING; LYSOSOME; PINOCYTOSIS; PROTEIN TRANSPORT; RECEPTOR DOWN REGULATION; CELL COMPARTMENTALIZATION; CELL LINE; CELL MEMBRANE; DOSE RESPONSE; DRUG EFFECT; ENZYMOLOGY; METABOLISM; ULTRASTRUCTURE;

1-PHOSPHATIDYLINOSITOL 3-KINASE; AMILORIDE; CELL COMPARTMENTATION; CELL LINE; CLATHRIN; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOCYTOSIS; ENDOSOMES; HUMANS; LDL-RECEPTOR RELATED PROTEIN 1; LIGANDS; LYSOSOMES; MEMBRANE MICRODOMAINS; MONOMERIC GTP-BINDING PROTEINS; PLASMINOGEN ACTIVATOR INHIBITOR 1; PLASMINOGEN ACTIVATORS; RECEPTORS, UROKINASE PLASMINOGEN ACTIVATOR;

EID: 56649115742     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0003730     Document Type: Article

References (43)

1. Blasi F, Carmeliet P (2002) uPAR: a versatile signalling orchestrator. Nat Rev Mol Cell Biol 3: 932-943.
2. Madsen CD, Ferraris GM, Andolfo A, Cunningham O, Sidenius N (2007) uPAR-induced cell adhesion and migration: vitronectin provides the key. J Cell Biol 177(5): 927-39.
3. Parton RG, Simons K (2007) The multiple faces of caveolae. Nat Rev Mol Cell Biol 3: 185-194.
4. Cunningham O, Andolfo A, Santovito ML, Iuzzolino L, Blasi F, et al. (2003) Dimerization controls the lipid raft partitioning of uPAR/CD87 and regulates its biological functions. EMBO J 22: 5994-6003.
5. Sahores M, Prinetti A, Chiabrando G, Blasi F, Sonnino S (2008) uPA binding increases UPAR localization to lipid rafts and modifies the receptor microdomain composition. Biochim Biophys Acta 1778: 250-9.
6. Caiolfa VR, Zamai M, Marengo G, Andolfo A, Madsen CD, et al. (2007) J Cell Biol 179: 1067-82.
7. Nykjaer A, Petersen CM, Møller B, Jensen PH, Moestrup SK, et al. (1992) Purified alpha 2-macroglobulin receptor/LDL receptor-related protein binds urokinase plasminogen activator inhibitor type-1 complex. Evidence that the alpha 2-macroglobulin receptor mediates cellular degradation of urokinase receptor-bound complexes. J Biol Chem 267: 14543-6.
8. Conese M, Nykjaer A, Petersen CM, Cremona O, Pardi R, et al. (1995) alpha-2 Macroglobulin receptor/Ldl receptor-related protein (LRP-1)-dependent internalization of the urokinase receptor. J Cell Biol 131: 1609-22.
9. Czekay RP, Kummel 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: 1467-79.
10. Mayor S, Pagano R (2007) Pathways of clathrin-independent endocytosis. Nat Rev Mol Cell Biol 8: 603-612.
11. Cubellis MV, Wun TC, Blasi F (1990) Receptor-mediated internalization and degradation of urokinase is caused by its specific inhibitor PAI-1. EMBO J. pp 1079-85.
12. Jones AT (2007) Macropinocytosis: searching for an endocytic identity and role in the uptake of cell penetrating peptides. J Cell Mol Med 11: 670-84.
13. Heuser J, Anderson RG (1989) Hypertonic media inhibit receptor-mediated endocytosis by blocking clathrin-coated pit formation. J Cell Biol 108: 389-400.
14. Roper K, Corbeil D, Huttner WB (2000) Retention of prominin in microvilli reveals distinct cholesterol-based microdomains in the apical plasma membrane. Nat Cell Biol 9: 582-592.
15. Bretscher MS, Thomson JN, Pearse BM (1980) Coated pits act as molecular filters. Proc Natl Acad Sci U S A 77: 4156-4159.
16. Parton RG, Joggerst B, Simons K (1994) Regulated internalization of caveolae. J Cell Biol 127: 1199-215.
17. Kirkham M, Fujita A, Chadda R, Nixon SJ, Kurzchalia TV, et al. (2005) Ultrastructural identification of uncoated caveolin-1 independent early endocytic carriers. J Cell Biol 168: 465-76.
18. Poussin C, Foti M, Carpentier JL, Pugin J (1998) CD14-dependent endotoxin internalization via a macropinocytic pathway. J Biol Chem 273(32): 20285-91.
19. Watarai M, Makino S, Fujii Y, Okamoto K, Shirahata T (2002) Modulation of Brucella-induced macropinocytosis by lipid rafts mediated intracellular replication. Cell Microbiol 6: 341-55.
20. Kjøller 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: 1145-57.
21. Degryse B, Resnati M, Rabbani SA, Villa A, Fazioli F, et al. (1999) Srcdependence and pertussis-toxin sensitivity of urokinase receptor-dependent chemotaxis and cytoskeleton reorganization in rat smooth muscle cells. Blood 94: 649-62.
22. West MA, Bretscher MS, Watts C (1989) Distinct endocytotic pathways in epidermal growth factor-stimulated human carcinoma A431 cells. J Cell Biol 109: 2731-9.
23. Mercer J, Helenius A (2008) Vaccinia virus uses macropinocytosis and apoptotic mimicry to enter host cells. Science 320: 531-535.
24. Ellis S, Mellor H (2000) Regulation of endocytic trafficking by Rho family GTPases. Trends Cell Biol 10: 85-88.
25. Ridley AJ, Paterson HF, Johnston CL, Diekman D, Hall A (1992) The small GTP-binding protein Rac regulates growth factor-induced ruffling. Cell 70: 401-410.
26. Lindmo K, Stenmark H (2006) Regulation of membrane traffic by phosphoinositide 3-kinases. J Cell Science 119: 605-614.
27. Lakadamyali M, Rust MJ, Zhuang X (2006) Ligands for clathrin-mediated endocytosis are differentially sorted into distinct populations of early endosomes. Cell 124: 997-1009.
28. Vilhardt F, Nielsen M, Sandvig K, van Deurs B (1999) Urokinase-type plasminogen activator receptor is internalized by different mechanisms in polarized and non polarized Madin-Darby canine kidney epithelial cells. Mol Biol Cell 10: 179-95.
29. Masilamani M, Narayanan S, Prieto M, Borrego F, Coligan JE (2008) Uncommon endocytic and trafficking pathway of the natural killer cell CD94/NKG2A inhibitory receptor. Traffic 6: 1019-34.
30. Cao H, Chen J, Awoniyi M, Henley JR, McNiven MA (2007) Dynamin 2 mediates fluid-phase micropinocytosis in epithelial cells. J Cell Science 120(Pt 23): 4167-77.
31. Bryant DM, Kerr MC, Hammond LA, Joseph SR, Mostov KE, et al. (2007) EGF induces macropinocytosis and SNX1-modulated recycling of E-cadherin. J Cell Science 120(Pt 10): 1818-28.
32. Frittoli E, Palamidessi A, Pizzigoni A, Lanzetti L, Garrè M, et al. (2008) The Primate-specific Protein TBC1D3 Is Required for Optimal Macropinocytosis in a Novel ARF6-dependent Pathway. Mol Biol Cell 19: 1304-1316.
33. Lanzetti L, Palamidessi A, Areces L, Scita G, Di Fiore PP (2004) Rab5 is a signalling GTPase involved in actin remodelling by receptor tyrosine kinases. Nature 429: 309-314.
34. Orth JD, McNiven M (2006) Get off my back! Rapid receptor internalization through circular dorsal ruffles. Cancer Res 66: 11094-11096.
35. Falcone S, Cocucci E, Podini P, Kirchhausen T, Clementi E, et al. (2006) Macropinocytosis: regulated coordination of endocytic and exocytic membrane traffic events. J Cell Science 119: 4758-69.
36. Hasegawa T (1993) Production of a unique antibody specific for membrane ruffles and its use to characterize the behavior of two distinct types of ruffles. J Cell Biol 120: 1439-1448.
37. Jo M, Thomas KS, O'Donnell DM, Gonias S (2003) Epidermal growth factor receptor-dependent and independent cell signalling pathways originating from the urokinase receptor. J Biol Chem 278: 1642-1646.
38. Geckle M, Drumm K, Mildenberger S, Freudinger R, Gassner B, et al. (1999) Inhibition of Na+/H+ exchange impairs receptor-mediated albumin endocytosis in renal proximal tubule-derived epithelial cells from opossum. J Physiol 520: 709-21.
39. Geckle M, Freudinger R, Mildenberger S (2001) Inhibition of Na+/H+ exchange-3 interferes with apical receptor-mediated endocytosis via vesicle fusion. J Physiol 560: 267-80.
40. Fretz MM, Penning NA, Taei SA, Futaki S, Takeuki T, et al. (2006) Effects of Na+/H+ exchanger inhibitors on subcellular localization of endocytic organelles and intracellular dynamics of protein transduction domains HIV-TAT peptide and octaarginine. J Control Release 116: 247-254.
41. Tokuyasu KT (1973) A technique for ultracryotomy of cell suspensions and tissues. J Cell Biol 57: 551-565.
42. Slot JW, Geuze HJ (2007) Cryosectioning and Immunolabeling. Nat Protoc 2: 2480-2491.
43. Cubellis MV, Andreasen P, Ragno P, Meyer M, Dano K, et al. (1989) Accessibility of receptor-bound urokinase to type-1 plasminogen activator inhibitor. Proc Natl Acad Sci 86: 4828-4832.