Caveolin limits membrane microdomain mobility and integrin-mediated uptake of fibronectin-binding pathogens

Journal of Cell Science

Volumn 123, Issue 24, 2010, Pages 4280-4291

  Hoffmann, Christine ^a   Berking, Anne ^a   Agerer, Franziska ^b,d   Buntru, Alexander ^a   Neske, Florian ^b,e   Chhatwal, G Singh ^c   Ohlsen, Knut ^b   Hauck, Christof R ^a  

^a UNIVERSITY OF KONSTANZ   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^d Nexigen GmbH   (Germany)

^e PAUL EHRLICH INSTITUT   (Germany)

Author keywords

Caveolin; Endocytosis; Fibronectin; Integrin; Lipid rafts; Staphylococci

Indexed keywords

ACTIN; BETA1 INTEGRIN; CAVEOLIN; CAVEOLIN 1; FIBRONECTIN; FLOTILLIN 1; FLOTILLIN 2; GANGLIOSIDE GM1; GLYCOSYLPHOSPHATIDYLINOSITOL; INTEGRIN; STOMATIN;

ARTICLE; CELL MEMBRANE; CYTOSKELETON; ENDOCYTOSIS; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GENE EXPRESSION; INFECTION; INTERNALIZATION; NONHUMAN; PHAGOCYTE; POINT MUTATION; PRIORITY JOURNAL; STAPHYLOCOCCUS AUREUS; STIMULATION;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, CD29; BACTERIAL ADHESION; BACTERIAL PROTEINS; BLOOD PROTEINS; CATTLE; CAVEOLIN 1; ENDOCYTOSIS; FIBROBLASTS; FIBRONECTINS; HEK293 CELLS; HUMANS; MEMBRANE MICRODOMAINS; MEMBRANE PROTEINS; MICE; MOLECULAR SEQUENCE DATA; PROTEIN TRANSPORT; SRC-FAMILY KINASES; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS;

BACTERIA (MICROORGANISMS); STAPHYLOCOCCUS; STAPHYLOCOCCUS AUREUS;

EID: 78649738478     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.064006     Document Type: Article

References (73)

1. Agerer, F., Michel, A., Ohlsen, K. and Hauck, C. R. (2003). Integrin-mediated invasion of Staphylococcus aureus into human cells requires Src family protein tyrosine kinases. J. Biol. Chem. 278, 42524-42531.
2. Agerer, F., Waeckerle, S. and Hauck, C. R. (2004). Microscopic quantification of bacterial invasion by a novel antibody-independent staining method. J. Microbiol. Methods 59, 23-32.
3. Agerer, F., Lux, S., Michel, A., Rohde, M., Ohlsen, K. and Hauck, C. R. (2005). Cellular invasion by Staphylococcus aureus reveals a functional link between focal adhesion kinase and cortactin in integrin-mediated internalisation. J. Cell Sci. 118, 2189-2200.
4. Alrutz, M. A. and Isberg, R. R. (1998). Involvement of focal adhesion kinase in invasin-mediated uptake. Proc. Natl. Acad. Sci. USA 95, 13658-13663.
5. Axelrod, D., Koppel, D. E., Schlessinger, J., Elson, E. and Webb, W. W. (1976). Mobility measurement by analysis of fluorescence photobleaching recovery kinetics. Biophys. J. 16, 1055-1069.
6. Bonazzi, M., Veiga, E., Pizarro-Cerda, J. and Cossart, P. (2008). Successive post-translational modifications of E-cadherin are required for InlA-mediated internalization of Listeria monocytogenes. Cell. Microbiol. 10, 2208-2222.
7. Boyle, E. C. and Finlay, B. B. (2003). Bacterial pathogenesis: exploiting cellular adherence. Curr. Opin. Cell Biol. 15, 633-639.
8. Bretscher, M. S. (1989). Endocytosis and recycling of the fibronectin receptor in CHO cells. EMBO J. 8, 1341-1348.
9. Browman, D. T., Hoegg, M. B. and Robbins, S. M. (2007). The SPFH domain-containing proteins: more than lipid raft markers. Trends Cell Biol. 17, 394-402.
10. Caswell, P. and Norman, J. (2008). Endocytic transport of integrins during cell migration and invasion. Trends Cell Biol. 18, 257-263.
11. Couet, J., Li, S., Okamoto, T., Ikezu, T. and Lisanti, M. P. (1997). Identification of peptide and protein ligands for the caveolin-scaffolding domain. Implications for the interaction of caveolin with caveolae-associated proteins. J. Biol. Chem. 272, 6525-6533.
12. Damm, E. M., Pelkmans, L., Kartenbeck, J., Mezzacasa, A., Kurzchalia, T. and Helenius, A. (2005). Clathrin- and caveolin-1-independent endocytosis: entry of simian virus 40 into cells devoid of caveolae. J. Cell Biol. 168, 477-488. (Pubitemid 40205069)
13. del Pozo, M. A., Alderson, N. B., Kiosses, W. B., Chiang, H. H., Anderson, R. G. and Schwartz, M. A. (2004). Integrins regulate Rac targeting by internalization of membrane domains. Science 303, 839-842.
14. del Pozo, M. A., Balasubramanian, N., Alderson, N. B., Kiosses, W. B., Grande-Garcia, A., Anderson, R. G. and Schwartz, M. A. (2005). Phospho-caveolin-1 mediates integrin-regulated membrane domain internalization. Nat. Cell Biol. 7, 901-908.
15. Dersch, P. and Isberg, R. R. (1999). A region of the Yersinia pseudotuberculosis invasin protein enhances integrin-mediated uptake into mammalian cells and promotes self-association. EMBO J. 18, 1199-1213.
16. Drab, M., Verkade, P., Elger, M., Kasper, M., Lohn, M., Lauterbach, B., Menne, J., Lindschau, C., Mende, F., Luft, F. C. et al. (2001). Loss of caveolae, vascular dysfunction, and pulmonary defects in caveolin-1 gene-disrupted mice. Science 293, 2449-2452.
17. Dupuy, A. G. and Caron, E. (2008). Integrin-dependent phagocytosis: spreading from microadhesion to new concepts. J. Cell Sci. 121, 1773-1783.
18. Fowler, T., Wann, E. R., Joh, D., Johansson, S., Foster, T. J. and Hook, M. (2000). Cellular invasion by Staphylococcus aureus involves a fibronectin bridge between the bacterial fibronectin-binding MSCRAMMs and host cell beta1 integrins. Eur. J. Cell Biol. 79, 672-679.
19. Fowler, T., Johansson, S., Wary, K. K. and Hook, M. (2003). Src kinase has a central role in in vitro cellular internalization of Staphylococcus aureus. Cell. Microbiol. 5, 417-426.
20. Frick, M., Bright, N. A., Riento, K., Bray, A., Merrified, C. and Nichols, B. J. (2007). Coassembly of flotillins induces formation of membrane microdomains, membrane curvature, and vesicle budding. Curr. Biol. 17, 1151-1156.
21. Garner, M. J., Hayward, R. D. and Koronakis, V. (2002). The Salmonella pathogenicity island 1 secretion system directs cellular cholesterol redistribution during mammalian cell entry and intracellular trafficking. Cell. Microbiol. 4, 153-165.
22. Gaus, K., Le Lay, S., Balasubramanian, N. and Schwartz, M. A. (2006). Integrin-mediated adhesion regulates membrane order. J. Cell Biol. 174, 725-734.
23. Ghosh, P. K., Vasanji, A., Murugesan, G., Eppell, S. J., Graham, L. M. and Fox, P. L. (2002). Membrane microviscosity regulates endothelial cell motility. Nat. Cell Biol. 4, 894-900.
24. Greene, C., McDevitt, D., Francois, P., Vaudaux, P. E., Lew, D. P. and Foster, T. J. (1995). Adhesion properties of mutants of Staphylococcus aureus defective in fibronectin-binding proteins and studies on the expression of fnb genes. Mol. Microbiol. 17, 1143-1152.
25. Gulbins, E., Dreschers, S., Wilker, B. and Grassme, H. (2004). Ceramide, membrane rafts and infections. J. Mol. Med. 82, 357-363.
26. Hauck, C. R. and Ohlsen, K. (2006). Sticky connections: extracellular matrix protein recognition and integrin-mediated cellular invasion by Staphylococcus aureus. Curr. Opin. Microbiol. 9, 5-11.
27. Hauck, C. R., Hsia, D. A., Puente, X. S., Cheresh, D. A. and Schlaepfer, D. D. (2002). FRNK blocks v-Src-stimulated invasion and experimental metastases without effects on cell motility or growth. EMBO J. 21, 6289-6302.
28. Hauck, C. R., Agerer, F., Muenzner, P. and Schmitter, T. (2006). Cellular adhesion molecules as targets for bacterial infection. Eur. J. Cell Biol. 85, 235-242.
29. Hernandez-Deviez, D. J., Howes, M. T., Laval, S. H., Bushby, K., Hancock, J. F. and Parton, R. G. (2008). Caveolin regulates endocytosis of the muscle repair protein, dysferlin. J. Biol. Chem. 283, 6476-6488.
30. Hynes, R. O. (2002). Integrins: bidirectional, allosteric signaling machines. Cell 110, 673-687.
31. Kinoshita, T., Fujita, M. and Maeda, Y. (2008). Biosynthesis, remodelling and functions of mammalian GPI-anchored proteins: recent progress. J. Biochem. 144, 287-294.
32. Kirkham, M. and Parton, R. G. (2005). Clathrin-independent endocytosis: new insights into caveolae and non-caveolar lipid raft carriers. Biochim. Biophys. Acta 1745, 273-286.
33. Kupsch, E. M., Knepper, B., Kuroki, T., Heuer, I. and Meyer, T. F. (1993). Variable opacity (Opa) outer membrane proteins account for the cell tropisms displayed by Neisseria gonorrhoeae for human leukocytes and epithelial cells. EMBO J. 12, 641-650.
34. Lafont, F. and van der Goot, F. G. (2005). Bacterial invasion via lipid rafts. Cell. Microbiol. 7, 613-620.
35. Lafont, F., Tran Van Nhieu, G., Hanada, K., Sansonetti, P. and van der Goot, F. G. (2002). Initial steps of Shigella infection depend on the cholesterol/sphingolipid raft-mediated CD44-IpaB interaction. EMBO J. 21, 4449-4457.
36. Lajoie, P., Goetz, J. G., Dennis, J. W. and Nabi, I. R. (2009a). Lattices, rafts, and scaffolds: domain regulation of receptor signaling at the plasma membrane. J. Cell Biol. 185, 381-385.
37. Lajoie, P., Kojic, L. D., Nim, S., Li, L., Dennis, J. W. and Nabi, I. R. (2009b). Caveolin-1 regulation of dynamin-dependent, raft-mediated endocytosis of cholera toxin b-subunit occurs independently of caveolae. J. Cell. Mol. Med. 13, 3218-3225.
38. Le, P. U., Guay, G., Altschuler, Y. and Nabi, I. R. (2002). Caveolin-1 is a negative regulator of caveolae-mediated endocytosis to the endoplasmic reticulum. J. Biol. Chem. 277, 3371-3379.
39. Lee, W., Sodek, J. and McCulloch, C. A. (1996). Role of integrins in regulation of collagen phagocytosis by human fibroblasts. J. Cell Physiol. 168, 695-704.
40. Leitinger, B. and Hogg, N. (2002). The involvement of lipid rafts in the regulation of integrin function. J. Cell Sci. 115, 963-972. (Pubitemid 34257381)
41. Manninen, A., Verkade, P., Le Lay, S., Torkko, J., Kasper, M., Fullekrug, J. and Simons, K. (2005). Caveolin-1 is not essential for biosynthetic apical membrane transport. Mol. Cell. Biol. 25, 10087-10096.
42. McNally, E. M., de Sa Moreira, E., Duggan, D. J., Bonnemann, C. G., Lisanti, M. P., Lidov, H. G., Vainzof, M., Passos-Bueno, M. R., Hoffman, E. P., Zatz, M. et al. (1998). Caveolin-3 in muscular dystrophy. Hum. Mol. Genet. 7, 871-877.
43. Memmo, L. M. and McKeown-Longo, P. (1998). The alphavbeta5 integrin functions as an endocytic receptor for vitronectin. J. Cell Sci. 111, 425-433.
44. Muenzner, P., Bachmann, V., Kuespert, K. and Hauck, C. R. (2008). The CEACAM1 transmembrane domain, but not the cytoplasmic domain, directs internalization of human pathogens via membrane-microdomains. Cell. Microbiol. 10, 1074-1092.
45. Neet, K. and Hunter, T. (1995). The nonreceptor protein-tyrosine kinase CSK complexes directly with the GTPase-activating protein-associated p62 protein in cells expressing v-Src or activated c-Src. Mol. Cell. Biol. 15, 4908-4920.
46. Neumann-Giesen, C., Falkenbach, B., Beicht, P., Claasen, S., Luers, G., Stuermer, C. A., Herzog, V. and Tikkanen, R. (2004). Membrane and raft association of reggie-1/flotillin-2: role of myristoylation, palmitoylation and oligomerization and induction of filopodia by overexpression. Biochem. J. 378, 509-518. (Pubitemid 38367240)
47. Oggioni, M. R. and Pozzi, G. (1996). A host-vector system for heterologous gene expression in Streptococcus gordonii. Gene 169, 85-90.
48. Ozeri, V., Rosenshine, I., Ben-Ze'Ev, A., Bokoch, G. M., Jou, T. S. and Hanski, E. (2001). De novo formation of focal complex-like structures in host cells by invading Streptococci. Mol. Microbiol. 41, 561-573.
49. Pelkmans, L., Kartenbeck, J. and Helenius, A. (2001). Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER. Nat. Cell Biol. 3, 473-483.
50. Pils, S., Schmitter, T., Neske, F. and Hauck, C. R. (2006). Quantification of bacterial invasion into adherent cells by flow cytometry. J. Microbiol. Methods 65, 301-310.
51. Pizarro-Cerda, J. and Cossart, P. (2006). Bacterial adhesion and entry into host cells. Cell 124, 715-727.
52. Riethmuller, J., Riehle, A., Grassme, H. and Gulbins, E. (2006). Membrane rafts in host-pathogen interactions. Biochim. Biophys. Acta 1758, 2139-2147.
53. Rizzo, M. A., Springer, G. H., Granada, B. and Piston, D. W. (2004). An improved cyan fluorescent protein variant useful for FRET. Nat. Biotechnol. 22, 445-449.
54. Rohde, M., Muller, E., Chhatwal, G. S. and Talay, S. R. (2003). Host cell caveolae act as an entry-port for group A streptococci. Cell. Microbiol. 5, 323-342.
55. Salzer, U. and Prohaska, R. (2001). Stomatin, flotillin-1, and flotillin-2 are major integral proteins of erythrocyte lipid rafts. Blood 97, 1141-1143. (Pubitemid 32154306)
56. Sandvig, K., Garred, O., Holm, P. K. and van Deurs, B. (1993). Endocytosis and intracellular transport of protein toxins. Biochem. Soc. Trans. 21, 707-711.
57. Sargiacomo, M., Scherer, P. E., Tang, Z., Kubler, E., Song, K. S., Sanders, M. C. and Lisanti, M. P. (1995). Oligomeric structure of caveolin: implications for caveolae membrane organization. Proc. Natl. Acad. Sci. USA 92, 9407-9411.
58. Schmitter, T., Pils, S., Weibel, S., Agerer, F., Buntru, A., Kopp, K. and Hauck, C. R. (2007). Opa proteins of pathogenic Neisseriae initiate Src-kinase-dependent or lipid raft-mediated uptake via distinct human CEACAM isoforms. Infect. Immunol. 75, 4116-4126.
59. Schwarz-Linek, U., Werner, J. M., Pickford, A. R., Gurusiddappa, S., Kim, J. H., Pilka, E. S., Briggs, J. A., Gough, T. S., Hook, M., Campbell, I. D. et al. (2003). Pathogenic bacteria attach to human fibronectin through a tandem beta-zipper. Nature 423, 177-181. (Pubitemid 36569541)
60. Sergent, O., Pereira, M., Belhomme, C., Chevanne, M., Huc, L. and Lagadic-Gossmann, D. (2005). Role for membrane fluidity in ethanol-induced oxidative stress of primary rat hepatocytes. J. Pharmacol. Exp. Ther. 313, 104-111.
61. Seveau, S., Bierne, H., Giroux, S., Prevost, M. C. and Cossart, P. (2004). Role of lipid rafts in E-cadherin- and HGF-R/Met-mediated entry of Listeria monocytogenes into host cells. J. Cell Biol. 166, 743-753.
62. Shi, F. and Sottile, J. (2008). Caveolin-1-dependent {beta}1 integrin endocytosis is a critical regulator of fibronectin turnover. J. Cell Sci. 121, 2360-2371.
63. Sinha, B., Francois, P. P., Nusse, O., Foti, M., Hartford, O. M., Vaudaux, P., Foster, T. J., Lew, D. P., Herrmann, M. and Krause, K. H. (1999). Fibronectin-binding protein acts as Staphylococcus aureus invasin via fibronectin bridging to integrin alpha5beta1. Cell. Microbiol. 1, 101-117.
64. Solis, G. P., Hoegg, M., Munderloh, C., Schrock, Y., Malaga-Trillo, E., Rivera-Milla, E. and Stuermer, C. A. (2007). Reggie/flotillin proteins are organized into stable tetramers in membrane microdomains. Biochem. J. 403, 313-322.
65. Sotgia, F., Razani, B., Bonuccelli, G., Schubert, W., Battista, M., Lee, H., Capozza, F., Schubert, A. L., Minetti, C., Buckley, J. T. et al. (2002). Intracellular retention of glycosylphosphatidyl inositol-linked proteins in caveolin-deficient cells. Mol. Cell. Biol. 22, 3905-3926.
66. Sottile, J. and Chandler, J. (2005). Fibronectin matrix turnover occurs through a caveolin-1-dependent process. Mol. Biol. Cell 16, 757-768.
67. Talay, S. R., Zock, A., Rohde, M., Molinari, G., Oggioni, M., Pozzi, G., Guzman, C. A. and Chhatwal, G. S. (2000). Co-operative binding of human fibronectin to Sfbl protein triggers streptococcal invasion into respiratory epithelial cells. Cell. Microbiol. 2, 521-535.
68. Tsuda, K., Furuta, N., Inaba, H., Kawai, S., Hanada, K., Yoshimori, T. and Amano, A. (2008). Functional analysis of alpha5beta1 integrin and lipid rafts in invasion of epithelial cells by Porphyromonas gingivalis using fluorescent beads coated with bacterial membrane vesicles. Cell Struct. Funct. 33, 123-132.
69. van der Flier, A. and Sonnenberg, A. (2001). Function and interactions of integrins. Cell Tissue Res. 305, 285-298.
70. van Putten, J. P., Duensing, T. D. and Cole, R. L. (1998). Entry of OpaA+ gonococci into HEp-2 cells requires concerted action of glycosaminoglycans, fibronectin and integrin receptors. Mol. Microbiol. 29, 369-379.
71. van Zanten, T. S., Cambi, A., Koopman, M., Joosten, B., Figdor, C. G. and Garcia-Parajo, M. F. (2009). Hotspots of GPI-anchored proteins and integrin nanoclusters function as nucleation sites for cell adhesion. Proc. Natl. Acad. Sci. USA 106, 18557-18562.
72. Wakabayashi, M., Okada, T., Kozutsumi, Y. and Matsuzaki, K. (2005). GM1 ganglioside-mediated accumulation of amyloid beta-protein on cell membranes. Biochem. Biophys. Res. Commun. 328, 1019-1023.
73. Wary, K. K., Mariotti, A., Zurzolo, C. and Giancotti, F. G. (1998). A requirement for caveolin-1 and associated kinase Fyn in integrin signaling and anchorage-dependent cell growth. Cell 94, 625-634.