A crucial role for β2 integrins in podosome formation, dynamics and Toll-like-receptor-signaled disassembly in dendritic cells

Journal of Cell Science

Volumn 127, Issue 19, 2014, Pages 4213-4224

  Gawden Bone, Christian ^a,c   West, Michele A ^a   Morrison, Vicky L ^b,d   Edgar, Alexander J ^a   McMillan, Sarah J ^a   Dill, Brian D ^a   Trost, Matthias ^a   Prescott, Alan ^a   Fagerholm, Susanna C ^b,d   Watts, Colin ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Dendritic cells; Integrins; Podosomes

Indexed keywords

AMINO ACID; CD18 ANTIGEN; CD86 ANTIGEN; FIBRINOGEN; FIBRONECTIN; GELATIN; INTERCELLULAR ADHESION MOLECULE 1; LAMININ; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PROGRAMMED DEATH 1 LIGAND 1; THREONINE; TOLL LIKE RECEPTOR;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL MEMBRANE; CONTROLLED STUDY; DENDRITIC CELL; FOCAL ADHESION; MOUSE; NONHUMAN; PODOSOME; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; ANIMAL; C57BL MOUSE; CELL MOTION; CYTOLOGY; FEMALE; MEMBRANE STRUCTURE; METABOLISM; PHYSIOLOGY; PREGNANCY;

ANIMALS; ANTIGENS, CD18; CELL MEMBRANE STRUCTURES; CELL MOVEMENT; DENDRITIC CELLS; FEMALE; MICE; MICE, INBRED C57BL; PREGNANCY; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS;

EID: 84913612531     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.151167     Document Type: Article

References (45)

1. Badowski, C., Pawlak, G., Grichine, A., Chabadel, A., Oddou, C., Jurdic, P., Pfaff, M., Albigès-Rizo, C. and Block, M. R. (2008). Paxillin phosphorylation controls invadopodia/podosomes spatiotemporal organization. Mol. Biol. Cell 19, 633-645.
2. Burns, S., Hardy, S. J., Buddle, J., Yong, K. L., Jones, G. E. and Thrasher, A. J. (2004). Maturation of DC is associated with changes in motile characteristics and adherence. Cell Motil. Cytoskeleton 57, 118-132.
3. Cairo, C. W., Mirchev, R. and Golan, D. E. (2006). Cytoskeletal regulation couples LFA-1 conformational changes to receptor lateral mobility and clustering. Immunity 25, 297-308.
4. Chabadel, A., Bañon-Rodríguez, I., Cluet, D., Rudkin, B. B., Wehrle-Haller, B., Génot, E., Jurdic, P., Antón, I. M. and Saltel, F. (2007). CD44 and beta3 integrin organize two functionally distinct actin-based domains in osteoclasts. Mol. Biol. Cell 18, 4899-4910.
5. Chou, H.-C., Antón, I. M., Holt, M. R., Curcio, C., Lanzardo, S., Worth, A., Burns, S., Thrasher, A. J., Jones, G. E. and Calle, Y. (2006). WIP regulates the stability and localization of WASP to podosomes in migrating dendritic cells. Curr. Biol. 16, 2337-2344.
6. 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.
7. Destaing, O., Saltel, F., Géminard, J.-C., Jurdic, P. and Bard, F. (2003). Podosomes display actin turnover and dynamic self-organization in osteoclasts expressing actin-green fluorescent protein. Mol. Biol. Cell 14, 407-416.
8. Destaing, O., Planus, E., Bouvard, D., Oddou, C., Badowski, C., Bossy, V., Raducanu, A., Fourcade, B., Albiges-Rizo, C. and Block, M. R. (2010). β1A integrin is a master regulator of invadosome organization and function. Mol. Biol. Cell 21, 4108-4119.
9. Dovas, A. and Cox, D. (2011). Signaling networks regulating leukocyte podosome dynamics and function. Cell. Signal. 23, 1225-1234.
10. Evans, J. G., Correia, I., Krasavina, O., Watson, N. and Matsudaira, P. (2003). Macrophage podosomes assemble at the leading lamella by growth and fragmentation. J. Cell Biol. 161, 697-705.
11. Fagerholm, S., Morrice, N., Gahmberg, C. G. and Cohen, P. (2002). Phosphorylation of the cytoplasmic domain of the integrin CD18 chain by protein kinase C isoforms in leukocytes. J. Biol. Chem. 277, 1728-1738.
12. Fagerholm, S. C., Hilden, T. J., Nurmi, S. M. and Gahmberg, C. G. (2005). Specific integrin alpha and beta chain phosphorylations regulate LFA-1 activation through affinity-dependent and-independent mechanisms. J. Cell Biol. 171, 705-715.
13. Gahmberg, C. G., Fagerholm, S. C., Nurmi, S. M., Chavakis, T., Marchesan, S. and Grönholm, M. (2009). Regulation of integrin activity and signalling. Biochim. Biophys. Acta 1790, 431-444.
14. 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.
15. 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.
16. Harlow, E. and Lane, D. (1988). Antibodies: a Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
17. 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.
18. Law, D. A., DeGuzman, F. R., Heiser, P., Ministri-Madrid, K., Killeen, N. and Phillips, D. R. (1999). Integrin cytoplasmic tyrosine motif is required for outsidein alphaIIbbeta3 signalling and platelet function. Nature 401, 808-811.
19. Legate, K. R. and Fässler, R. (2009). Mechanisms that regulate adaptor binding to beta-integrin cytoplasmic tails. J. Cell Sci. 122, 187-198.
20. Lim, J., Hotchin, N. A. and Caron, E. (2011). Ser756 of β2 integrin controls Rap1 activity during inside-out activation of αMβ2. Biochem. J. 437, 461-467.
21. Linder, S. (2007). The matrix corroded: podosomes and invadopodia in extracellular matrix degradation. Trends Cell Biol. 17, 107-117.
22. Linder, S. (2009). Invadosomes at a glance. J. Cell Sci. 122, 3009-3013.
23. Liu, J., He, X., Qi, Y., Tian, X., Monkley, S. J., Critchley, D. R., Corbett, S. A., Lowry, S. F., Graham, A. M. and Li, S. (2011). Talin1 regulates integrin turnover to promote embryonic epithelial morphogenesis. Mol. Cell. Biol. 31, 3366-3377.
24. Luxenburg, C., Geblinger, D., Klein, E., Anderson, K., Hanein, D., Geiger, B. and Addadi, L. (2007). The architecture of the adhesive apparatus of cultured osteoclasts: from podosome formation to sealing zone assembly. PLoS ONE 2, e179.
25. McMillan, S. J., Bishop, B., Townsend, M. J., McKenzie, A. N. and Lloyd, C. M. (2002). The absence of interleukin 9 does not affect the development of allergen-induced pulmonary inflammation nor airway hyperreactivity. J. Exp. Med. 195, 51-57.
26. Morrison, V. L., MacPherson, M., Savinko, T., Lek, H. S., Prescott, A. and Fagerholm, S. C. (2013). The β2 integrin-kindlin-3 interaction is essential for Tcell homing but dispensable for T-cell activation in vivo. Blood 122, 1428-1436.
27. Moser, M., Bauer, M., Schmid, S., Ruppert, R., Schmidt, S., Sixt, M., Wang, H.-V., Sperandio, M. and Fässler, R. (2009a). Kindlin-3 is required for beta2 integrin-mediated leukocyte adhesion to endothelial cells. Nat. Med. 15, 300-305.
28. Moser, M., Legate, K. R., Zent, R. and Fässler, R. (2009b). The tail of integrins, talin, and kindlins. Science 324, 895-899.
29. Mulrooney, J. P., Hong, T. and Grabel, L. B. (2001). Serine 785 phosphorylation of the beta1 cytoplasmic domain modulates beta1A-integrin-dependent functions. J. Cell Sci. 114, 2525-2533.
30. 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.
31. Nurmi, S. M., Autero, M., Raunio, A. K., Gahmberg, C. G. and Fagerholm, S. C. (2007). Phosphorylation of the LFA-1 integrin beta2-chain on Thr-758 leads to adhesion, Rac-1/Cdc42 activation, and stimulation of CD69 expression in human T cells. J. Biol. Chem. 282, 968-975.
32. Perez, O. D., Mitchell, D., Jager, G. C., South, S., Murriel, C., McBride, J., Herzenberg, L. A., Kinoshita, S. and Nolan, G. P. (2003). Leukocyte functional antigen 1 lowers T cell activation thresholds and signaling through cytohesin-1 and Jun-activating binding protein 1. Nat. Immunol. 4, 1083-1092.
33. Riedl, J., Crevenna, A. H., Kessenbrock, K., Yu, J. H., Neukirchen, D., Bista, M., Bradke, F., Jenne, D., Holak, T. A., Werb, Z. et al. (2008). Lifeact: a versatile marker to visualize F-actin. Nat. Methods 5, 605-607.
34. Schachtner, H., Calaminus, S. D. J., Sinclair, A., Monypenny, J., Blundell, M. P., Leon, C., Holyoake, T. L., Thrasher, A. J., Michie, A. M., Vukovic, M. et al. (2013). Megakaryocytes assemble podosomes that degrade matrix and protrude through basement membrane. Blood 121, 2542-2552.
35. Scharffetter-Kochanek, K., Lu, H., Norman, K., van Nood, N., Munoz, F., Grabbe, S., McArthur, M., Lorenzo, I., Kaplan, S., Ley, K. et al. (1998). Spontaneous skin ulceration and defective T cell function in CD18 null mice. J. Exp. Med. 188, 119-131.
36. 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.
37. van den Dries, K., Meddens, M. B. M., de Keijzer, S., Shekhar, S., Subramaniam, V., Figdor, C. G. and Cambi, A. (2013a). Interplay between myosin IIA-mediated contractility and actin network integrity orchestrates podosome composition and oscillations. Nat. Commun. 4, 1412-1413.
38. van den Dries, K., Schwartz, S. L., Byars, J., Meddens, M. B. M., 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.
39. Van Goethem, E., Guiet, R., Balor, S., Charrière, G. M., Poincloux, R., Labrousse, A., Maridonneau-Parini, I. and Le Cabec, V. (2011). Macrophage podosomes go 3D. Eur. J. Cell Biol. 90, 224-236.
40. van Helden, S. F. G., Krooshoop, D. J. E. B., Broers, K. C. M., Raymakers,R. A. P., 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.
41. van Helden, S. F. G., Oud, M. M., Joosten, B., Peterse, N., Figdor, C. G. and van Leeuwen, F. N. (2008). PGE2-mediated podosome loss in dendritic cells is dependent on actomyosin contraction downstream of the RhoA-Rho-kinase axis. J. Cell Sci. 121, 1096-1106.
42. West, M. A., Antoniou, A. N., Prescott, A. R., Azuma, T., Kwiatkowski, D. J. and Watts, C. (1999). Membrane ruffling, macropinocytosis and antigen presentation in the absence of gelsolin in murine dendritic cells. Eur. J. Immunol. 29, 3450-3455.
43. West, M. A., Wallin, R. P. A., Matthews, S. P., Svensson, H. G., Zaru, R., Ljunggren, H.-G., Prescott, A. R. and Watts, C. (2004). Enhanced dendritic cell antigen capture via toll-like receptor-induced actin remodeling. Science 305, 1153-1157.
44. 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.
45. Yu, C.-H., Rafiq, N. B. M., Krishnasamy, A., Hartman, K. L., Jones, G. E., Bershadsky, A. D. and Sheetz, M. P. (2013). Integrin-matrix clusters form podosome-like adhesions in the absence of traction forces. Cell Reports 5, 1456-1468.