Podosomes of dendritic cells facilitate antigen sampling

Journal of Cell Science

Volumn 127, Issue 5, 2014, Pages 1052-1064

  Baranov, Maksim V ^a   Beest, Ter Martinter ^a   Reinieren Beeren, Inge ^a   Cambi, Alessandra ^a   Figdor, Carl G ^a   Den Bogaart, Geert Van ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Antigen presentation; Dendritic cell; Podosome; Receptor mediated endocytosis

Indexed keywords

ANTIGEN; F ACTIN; GELATIN; GLYCOPROTEIN GP 120; INTEGRIN; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; QUANTUM DOT;

ANIMAL CELL; ANTIGEN PRESENTATION; ANTIGEN RECOGNITION; ARTICLE; CELL MEMBRANE; CELL MIGRATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DENDRITIC CELL; ENDOCYTOSIS; ENDOTHELIUM CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; EPITHELIUM CELL; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; MEGAKARYOCYTE; MEMBRANE FILTER; MICROTUBULE; MONOCYTE; MOUSE; NONHUMAN; PHYSICAL RESISTANCE; PODOSOME; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION; TRANSMISSION ELECTRON MICROSCOPY;

ANTIGEN PRESENTATION; DENDRITIC CELL; PODOSOME; RECEPTOR-MEDIATED ENDOCYTOSIS;

ANTIGEN PRESENTATION; CELL SURFACE EXTENSIONS; CELLS, CULTURED; DENDRITIC CELLS; ENDOCYTOSIS; HUMANS; MATRIX METALLOPROTEINASE 14; TUBULIN;

EID: 84896900563     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.141226     Document Type: Article

References (64)

1. Banchereau, J. and Steinman, R. M. (1998). Dendritic cells and the control of immunity. Nature 392, 245-252.
2. Brakebusch, C. and Fässler, R. (2003). The integrin-actin connection, an eternal love affair. EMBO J. 22, 2324-2333.
3. Bravo-Cordero, J. J., Hodgson, L. and Condeelis, J. (2012). Directed cell invasion and migration during metastasis. Curr. Opin. Cell Biol. 24, 277-283.
4. Buccione, R., Orth, J. D. and McNiven, M. A. (2004). Foot and mouth: podosomes, invadopodia and circular dorsal ruffles. Nat. Rev. Mol. Cell Biol. 5, 647-657.
5. Burgdorf, S., Lukacs-Kornek, V. and Kurts, C. (2006). The mannose receptor mediates uptake of soluble but not of cell-associated antigen for crosspresentation. J. Immunol. 176, 6770-6776.
6. Burns, S., Thrasher, A. J., Blundell, M. P., Machesky, L. and Jones, G. E. (2001). Configuration of human dendritic cell cytoskeleton by Rho GTPases, the WAS protein, and differentiation. Blood 98, 1142-1149.
7. Calle, Y., Carragher, N. O., Thrasher, A. J. and Jones, G. E. (2006). Inhibition of calpain stabilises podosomes and impairs dendritic cell motility. J. Cell Sci. 119, 2375-2385.
8. Cambi, A., Lidke, D. S., Arndt-Jovin, D. J., Figdor, C. G. and Jovin, T. M. (2007). Ligand-conjugated quantum dotsmonitor antigen uptake and processing by dendritic cells. Nano Lett. 7, 970-977.
9. Carman, C. V., Sage, P. T., Sciuto, T. E., de la Fuente, M. A., Geha, R. S., Ochs, H. D., Dvorak, H. F., Dvorak, A. M. and Springer, T. A. (2007). Transcellular diapedesis is initiated by invasive podosomes. Immunity 26, 784-797.
10. Chieppa, M., Rescigno, M., Huang, A. Y. and Germain, R. N. (2006). Dynamic imaging of dendritic cell extension into the small bowel lumen in response to epithelial cell TLR engagement. J. Exp. Med. 203, 2841-2852.
11. Collin, O., Na, S., Chowdhury, F., Hong, M., Shin, M. E., Wang, F. and Wang, N. (2008). Self-organized podosomes are dynamic mechanosensors. Curr. Biol. 18, 1288-1294.
12. Cornfine, S., Himmel, M., Kopp, P., El Azzouzi, K., Wiesner, C., Krüger, M., Rudel, T. and Linder, S. (2011). The kinesin KIF9 and reggie/flotillin proteins regulate matrix degradation by macrophage podosomes. Mol. Biol. Cell 22, 202-215.
13. Cox, S., Rosten, E., Monypenny, J., Jovanovic-Talisman, T., Burnette, D. T., Lippincott-Schwartz, J., Jones, G. E. and Heintzmann, R. (2011). Bayesian localization microscopy reveals nanoscale podosome dynamics. Nat. Methods 9, 195-200.
14. de Vries, I. J., Eggert, A. A., Scharenborg, N. M., Vissers, J. L., Lesterhuis, W. J., Boerman, O. C., Punt, C. J., Adema, G. J. and Figdor, C. G. (2002). Phenotypical and functional characterization of clinical grade dendritic cells. J. Immunother. 25, 429-438.
15. Dovas, A., Gevrey, J. C., Grossi, A., Park, H., Abou-Kheir, W. and Cox, D. (2009). Regulation of podosome dynamics by WASp phosphorylation: implication in matrix degradation and chemotaxis in macrophages. J. Cell Sci. 122, 3873-3882.
16. Dutta, D., Williamson, C. D., Cole, N. B. and Donaldson, J. G. (2012). Pitstop 2 is a potent inhibitor of clathrin-independent endocytosis. PLoS ONE 7, e45799.
17. Farache, J., Koren, I., Milo, I., Gurevich, I., Kim, K. W., Zigmond, E., Furtado, G. C., Lira, S. A. and Shakhar, G. (2013). Luminal bacteria recruit CD103+dendritic cells into the intestinal epithelium to sample bacterial antigens for presentation. Immunity 38, 581-595.
18. Gawden-Bone, C., Zhou, Z., King, E., Prescott, A., Watts, C. and Lucocq, J. (2010). Dendritic cell podosomes are protrusive and invade the extracellular matrix using metalloproteinase MMP-14. J. Cell Sci. 123, 1427-1437.
19. Geijtenbeek, T. B., Kwon, D. S., Torensma, R., van Vliet, S. J., van Duijnhoven, G. C., Middel, J., Cornelissen, I. L., Nottet, H. S., KewalRamani, V. N., Littman, D. R. et al. (2000). DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell 100, 587-597.
20. Gimona, M., Buccione, R., Courtneidge, S. A. and Linder, S. (2008). Assembly and biological role of podosomes and invadopodia. Curr. Opin. Cell Biol. 20, 235-241.
21. Jones, G. E., Zicha, D., Dunn, G. A., Blundell, M. and Thrasher, A. (2002). Restoration of podosomes and chemotaxis in Wiskott-Aldrich syndrome macrophages following induced expression of WASp. Int. J. Biochem. Cell Biol. 34, 806-815.
22. Kaparakis, M., Philpott, D. J. and Ferrero, R. L. (2007). Mammalian NLR proteins; discriminating foe from friend. Immunol. Cell Biol. 85, 495-502.
23. Labernadie, A., Thibault, C., Vieu, C., Maridonneau-Parini, I. and Charrière, G. M. (2010). Dynamics of podosome stiffness revealed by atomic force microscopy. Proc. Natl. Acad. Sci. USA 107, 21016-21021.
24. Lelouard, H., Fallet, M., de Bovis, B., Méresse, S. and Gorvel, J. P. (2012). Peyer's patch dendritic cells sample antigens by extending dendrites through M cell-specific transcellular pores. Gastroenterology 142, 592-601, e3.
25. Linder, S. (2007). The matrix corroded: podosomes and invadopodia in extracellular matrix degradation. Trends Cell Biol. 17, 107-117.
26. Linder, S., Nelson, D., Weiss, M. and Aepfelbacher, M. (1999). Wiskott-Aldrich syndrome protein regulates podosomes in primary human macrophages. Proc. Natl. Acad. Sci. USA 96, 9648-9653.
27. Linder, S., Wiesner, C. and Himmel, M. (2011). Degrading devices: invadosomes in proteolytic cell invasion. Annu. Rev. Cell Dev. Biol. 27, 185-211.
28. Lipscomb, M. F. and Masten, B. J. (2002). Dendritic cells: immune regulators in health and disease. Physiol. Rev. 82, 97-130.
29. Matías-Román, S., Gálvez, B. G., Genís, L., Yáñez-Mó , M., de la Rosa, G., Sánchez-Mateos, P., Sánchez-Madrid, F. and Arroyo, A. G. (2005). Membrane type 1-matrix metalloproteinase is involved in migration of human monocytes and is regulated through their interaction with fibronectin or endothelium. Blood 105, 3956-3964.
30. McGreal, E. P., Miller, J. L. and Gordon, S. (2005). Ligand recognition by antigen-presenting cell C-type lectin receptors. Curr. Opin. Immunol. 17, 18-24.
31. Muller, W. A. (2011). Mechanisms of leukocyte transendothelial migration. Annu. Rev. Pathol. 6, 323-344.
32. Murphy, D. A. and Courtneidge, S. A. (2011). The 'ins' and 'outs' of podosomes and invadopodia: characteristics, formation and function. Nat. Rev. Mol. Cell Biol. 12, 413-426.
33. Niess, J. H., Brand, S., Gu, X., Landsman, L., Jung, S., McCormick, B. A., Vyas, J. M., Boes, M., Ploegh, H. L., Fox, J. G. et al. (2005). CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance. Science 307, 254-258.
34. Peterson, J. R., Bickford, L. C., Morgan, D., Kim, A. S., Ouerfelli, O., Kirschner, M. W. and Rosen, M. K. (2004). Chemical inhibition of N-WASP by stabilization of a native autoinhibited conformation. Nat. Struct. Mol. Biol. 11, 747-755.
35. Prehoda, K. E., Scott, J. A., Mullins, R. D. and Lim, W. A. (2000). Integration of multiple signals through cooperative regulation of the N-WASP-Arp2/3 complex. Science 290, 801-806.
36. Proszynski, T. J., Gingras, J., Valdez, G., Krzewski, K. and Sanes, J. R. (2009). Podosomes are present in a postsynaptic apparatus and participate in its maturation. Proc. Natl. Acad. Sci. USA 106, 18373-18378.
37. Quaranta, V., Walker, L. E., Pellegrino, M. A. and Ferrone, S. (1980). Purification of immunologically functional subsets of human Ia-like antigens on a monoclonal antibody (Q5/13) immunoadsorbent. J. Immunol. 125, 1421-1425.
38. Rescigno, M., Urbano, M., Valzasina, B., Francolini, M., Rotta, G., Bonasio, R., Granucci, F., Kraehenbuhl, J. P. and Ricciardi-Castagnoli, P. (2001). Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat. Immunol. 2, 361-367.
39. Sabeh, F., Ota, I., Holmbeck, K., Birkedal-Hansen, H., Soloway, P., Balbin, M., Lopez-Otin, C., Shapiro, S., Inada, M., Krane, S. et al. (2004). Tumor cell traffic through the extracellular matrix is controlled by the membrane-anchored collagenase MT1-MMP. J. Cell Biol. 167, 769-781.
40. Sage, P. T., Varghese, L. M., Martinelli, R., Sciuto, T. E., Kamei, M., Dvorak, A. M., Springer, T. A., Sharpe, A. H. and Carman, C. V. (2012). Antigen recognition is facilitated by invadosome-like protrusions formed by memory/ effector T cells. J. Immunol. 188, 3686-3699.
41. Schachtner, H., Calaminus, S. D., Sinclair, A., Monypenny, J., Blundell, M. P., Leon, C., Holyoake, T. L., Thrasher, A. J., Michie, A. M., Vukovic, M. et al. (2013a). Megakaryocytes assemble podosomes that degrade matrix and protrude through basement membrane. Blood 121, 2542-2552.
42. Schachtner, H., Calaminus, S. D., Thomas, S. G. and Machesky, L. M. (2013b). Podosomes in adhesion, migration, mechanosensing and matrix remodeling. Cytoskeleton (Hoboken) 70, 572-589.
43. Schmidt, S., Nakchbandi, I., Ruppert, R., Kawelke, N., Hess, M. W., Pfaller, K., Jurdic, P., Fässler, R. and Moser, M. (2011). Kindlin-3-mediated signaling from multiple integrin classes is required for osteoclast-mediated bone resorption. J. Cell Biol. 192, 883-897.
44. Schoumacher, M., Goldman, R. D., Louvard, D. and Vignjevic, D. M. (2010). Actin, microtubules, and vimentin intermediate filaments cooperate for elongation of invadopodia. J. Cell Biol. 189, 541-556.
45. Shan, M., Gentile, M., Yeiser, J. R., Walland, A. C., Bornstein, V. U., Chen, K., He, B., Cassis, L., Bigas, A., Cols, M. et al. (2013). Mucus enhances gut homeostasis and oral tolerance by delivering immunoregulatory signals. Science 342, 447-453.
46. Shimonkevitz, R., Kappler, J., Marrack, P. and Grey, H. (1983). Antigen recognition by H-2-restricted Tcells. I. Cell-free antigen processing. J. Exp. Med. 158, 303-316.
47. Strisciuglio, C., Duijvestein, M., Verhaar, A. P., Vos, A. C., van den Brink, G. R., Hommes, D. W. and Wildenberg, M. E. (2013). Impaired autophagy leads to abnormal dendritic cell-epithelial cell interactions. J. Crohns Colitis 7, 534-541.
48. Takeda, K. and Akira, S. (2005). Toll-like receptors in innate immunity. Int. Immunol. 17, 1-14.
49. Thornton, E. E., Looney, M. R., Bose, O., Sen, D., Sheppard, D., Locksley, R., Huang, X. and Krummel, M. F. (2012). Spatiotemporally separated antigen uptake by alveolar dendritic cells and airway presentation to T cells in the lung. J. Exp. Med. 209, 1183-1199.
50. Tsujita, K., Kondo, A., Kurisu, S., Hasegawa, J., Itoh, T. and Takenawa, T. (2013). Antagonistic regulation of F-BAR protein assemblies controls actin polymerization during podosome formation. J. Cell Sci. 126, 2267-2278.
51. Vallon-Eberhard, A., Landsman, L., Yogev, N., Verrier, B. and Jung, S. (2006). Transepithelial pathogen uptake into the small intestinal lamina propria. J. Immunol. 176, 2465-2469.
52. Van Den Bogaart, G., Meyenberg, K., Risselada, H. J., Amin, H., Willig, K. I., Hubrich, B. E., Dier, M., Hell, S. W., Grubmüller, H., Diederichsen, U. et al. (2011). Membrane protein sequestering by ionic protein-lipid interactions. Nature 479, 552-555.
53. Van Den Dries, K., van Helden, S. F., te Riet, J., Diez-Ahedo, R., Manzo, C., Oud, M. M., van Leeuwen, F. N., Brock, R., Garcia-Parajo, M. F., Cambi, A. et al. (2012). Geometry sensing by dendritic cells dictates spatial organization and PGE(2)-induced dissolution of podosomes. Cell. Mol. Life Sci. 69, 1889-1901.
54. Van Den Dries, K., Meddens, M. B., de Keijzer, S., Shekhar, S., Subramaniam, V., Figdor, C. G. and Cambi, A. (2013a). Interplay between myosin IIAmediated contractility and actin network integrity orchestrates podosome composition and oscillations. Nat. Commun. 4, 1412.
55. Van Den Dries, K., Schwartz, S. L., Byars, J., Meddens, M. B., Bolomini-Vittori, M., Lidke, D. S., Figdor, C. G., Lidke, K. A. and Cambi, A. (2013b). Dual-color superresolution microscopy reveals nanoscale organization of mechanosensory podosomes. Mol. Biol. Cell 24, 2112-2123.
56. van Helden, S. F., Krooshoop, D. J., Broers, K. C., Raymakers, R. A., Figdor, C. G. and van Leeuwen, F. N. (2006). A critical role for prostaglandin E2 in podosome dissolution and induction of high-speed migration during dendritic cell maturation. J. Immunol. 177, 1567-1574.
57. Vestweber, D. (2012). Novel insights into leukocyte extravasation. Curr. Opin. Hematol. 19, 212-217.
58. von Kleist, L., Stahlschmidt, W., Bulut, H., Gromova, K., Puchkov, D., Robertson, M. J., MacGregor, K. A., Tomilin, N., Pechstein, A., Chau, N. et al. (2011). Role of the clathrin terminal domain in regulating coated pit dynamics revealed by small molecule inhibition. Cell 146, 471-484.
59. West, M. A., Prescott, A. R., Chan, K. M., Zhou, Z., Rose-John, S., Scheller, J. and Watts, C. (2008). TLR ligand-induced podosome disassembly in dendritic cells is ADAM17 dependent. J. Cell Biol. 182, 993-1005.
60. Wiesner, C., Faix, J., Himmel, M., Bentzien, F. and Linder, S. (2010). KIF5B and KIF3A/KIF3B kinesins drive MT1-MMP surface exposure, CD44 shedding, and extracellular matrix degradation in primary macrophages. Blood 116, 1559-1569.
61. Wolf, K. and Friedl, P. (2009). Mapping proteolytic cancer cell-extracellular matrix interfaces. Clin. Exp. Metastasis 26, 289-298.
62. Wolf, K., Te Lindert, M., Krause, M., Alexander, S., Te Riet, J., Willis, A. L., Hoffman, R. M., Figdor, C. G., Weiss, S. J. and Friedl, P. (2013). Physical limits of cell migration: control by ECM space and nuclear deformation and tuning by proteolysis and traction force. J. Cell Biol. 201, 1069-1084.
63. Yamaguchi, H., Yoshida, S., Muroi, E., Kawamura, M., Kouchi, Z., Nakamura, Y., Sakai, R. and Fukami, K. (2010). Phosphatidylinositol 4,5-bisphosphate and PIP5-kinase Ialpha are required for invadopodia formation in human breast cancer cells. Cancer Sci. 101, 1632-1638.
64. Zicha, D., Allen, W. E., Brickell, P. M., Kinnon, C., Dunn, G. A., Jones, G. E. and Thrasher, A. J. (1998). Chemotaxis of macrophages is abolished in the Wiskott-Aldrich syndrome. Br. J. Haematol. 101, 659-665.