Inhibition of calpain stabilises podosomes and impairs dendritic cell motility

Journal of Cell Science

Volumn 119, Issue 11, 2006, Pages 2375-2385

  Calle, Yolanda ^a   Carragher, Neil O ^b   Thrasher, Adrian J ^c   Jones, Gareth E ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b Advanced Science and Technology Laboratory   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Calpain; Cell adhesion; Cell motility; Dendritic cell; Leukocyte; Podosome

Indexed keywords

BETA2 INTEGRIN; CALPAIN; FOCAL ADHESION KINASE 2; NEURAL WISKOTT ALDRICH SYNDROME PROTEIN; PAXILLIN; TALIN; VINCULIN;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; BONE MARROW CELL; CELL ADHESION; CELL COMPOSITION; CELL LINEAGE; CELL MIGRATION; CELL MOTILITY; CELL STRUCTURE; CELL TYPE; CONTROLLED STUDY; DENDRITIC CELL; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; MONOLAYER CULTURE; MOUSE; NONHUMAN; PODOSOME; PRIORITY JOURNAL; REGULATORY MECHANISM; VELOCITY;

ANIMALS; CALCIUM-BINDING PROTEINS; CALPAIN; CELL ADHESION; CELL LINE; CELL MEMBRANE STRUCTURES; CELL MOVEMENT; CELLS, CULTURED; DENDRITIC CELLS; ENZYME ACTIVATION; FOCAL ADHESION KINASE 2; GLYCOPROTEINS; MICE; MICE, INBRED STRAINS; MICROFILAMENTS; OLIGOPEPTIDES; PEPTIDE FRAGMENTS; STRUCTURE-ACTIVITY RELATIONSHIP; TALIN; WISKOTT-ALDRICH SYNDROME PROTEIN;

EID: 33745482350     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.02939     Document Type: Article

References (56)

1. Abram, C. L, Seals, D. F, Pass, I, Salinsky, D, Maurer, L, Roth, T. and Courtneidge, S. A. (2003). The adaptor protein fish associates with members of the ADAMs family and localizes to podosomes of Src-transformed cells. J. Biol. Chem. 278, 16844-16851.
2. Adams, J. C. (2002). Regulation of protrusive and contracti[e cell-matrix contacts. J. Cell Sci. 115, 257-265.
3. Bhatt, A, Kaverina, I., Otey, C. and Huttenlocher, A. (2002). Regulation of focal complex composition and disassembly by the calcium-dependent protease calpain. J. Cell Sci. 115, 3415-3425.
4. Bialkowska, K, Kulkarni, S., Du, X., Goll, D. E., Saido, T. C. and Fox, J. E. (2000). Evidence that beta3 integrin-induced Rac activation involves the calpain-dependent formation of integrin clusters that are distinct from the focal complexes and focal adhesions that form as Rac and RhoA become active. J. Cell Biol. 151, 685-696.
5. Binks M., Jones, G. E., Brickell, P. M., Kinnon, C, Katz, D. R. and Thrasher, A. J. (1998). Intrinsic dendritic cell abnormalities in Wiskott-Aldrich syndrome. Eur. J. Immunol. 28, 3259-3267.
6. Brunton, V. G., MacPherson, I. R. and Frame, M. C. (2004). Cell adhesion receptors, tyrosine kinases and actin modulators: a complex three-way circuitry. Biochim. Biophys. Acta 1692, 121-144.
7. 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.
8. 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.
9. Calle, Y., Chou, H. C., Thrasher, A. J. and Jones, G. E. (2004a). Wiskott-Aldrich syndrome protein and the cytoskeletal dynamics of dendritic cells. J. Pathol. 204, 460-469.
10. Calle, Y., Jones, G. E., Jagger, C., Fuller, K., Blundel], M. P., Chow, J., Chambers, T. and Thrasher, A. I (2004b). WASp deficiency in mice results in failure to form osteoclast sealing zones and defects in bone resorption. Blood 103, 3552-3561.
11. Calle, Y., Burns, S., Thrasher, A. and Jones, G. E. (2006). The leukocyte podosome. Eur J. Cell Biol. 85, 151-157.
12. Carragher, N. O. and Frame, M. C. (2002). Calpain: a role in cell transformation and migration. Int. J. Biochem. Cell Biol. 34, 1539-1543.
13. Carragher, N. O., Fincham, V. J., Riley, D. and Frame, M. C. (2001). Cleavage of focal adhesion kinase by different proteases; during SRC-regulated transformation and apoptosis. Distinct roles for calpain and caspases. J. Biol. Chem. 276, 4270-4275.
14. Critchley, D. R. (2004). Cytoskeletal proteins talin and vincutin in integrin-mediated adhesion. Biochem. Soc. Trans. 32, 831-836.
15. Curtis, A. S. (1964). The mechanism of adhesion of cells to glass. A study by interference reflection microscopy. J. Cell Biol. 20, 199-215.
16. DeMali K. A., Barlow, C_ A. and Burridge, K. (2002). Recruitment of the Arp2/3 complex to vinculin: coupling membrane protrusion to matrix adhesion. J. Cell Biol. 159, 881-891.
17. Destaing, O., Saltel, F., Geminard, 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.
18. Dunn, G. A. and Jones, G. E. (2004). Cell motility under the microscope: vorsprung durch technik. Nat. Rev. Mol. Cell Biol. 5, 667-672.
19. Evans, J. G, Correia, L, 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.
20. Franco, S. J. and Huttenlocher, A. (2005). Regulating cell migration: calpains make the cut. J. Cell Sci. 118, 3829-3838.
21. Franco, S. J., Rodgers, M. A., Perrin, B. J., Han, J., Bennin, D. A., Critchley, D. R. and Huttenlocher, A. (2004). Calpain-mediated proteolysis of talin regulates adhesion dynamics. Nat. Cell Biol. 6, 977-983.
22. Gaidano, G., Bergui, L., Schena, M., Gaboli M., Cremona, O., Marchisio, P. C. and Caligaris-Cappio, F. (1990). Integrin distribution and cytoskeleton organization in normal and malignant monocytes. Leukemia 4, 682-687.
23. Glading, A, Lauffenburger, D. A. and Wells, A. (2002). Cutting to the chase: calpain proteases in cell motility. Trends Cell Biol. 12, 46-54.
24. Goll, D. E, Dayton, W. R, Singh, I. and Robson, R. M. (1991). Studies of the alpha-actinin/actin interaction in the Z-disk by using calpain. J. Biol. Chem. 266, 8501-8510.
25. Goto, T, Maeda, H. and Tanaka, T. (2002). A selective inhibitor of matrix metalloproteinases inhibits the migration of isolated osteoclasts by increasing the life span of podosomes. J. Bone Miner Metab. 20, 98-105.
26. Higgs, H. N. and Pollard, T. D. (2001). Regulation of actin filament network formation through ARP213 complex: activation by a diverse array of proteins. Annu. Rev. Biochem. 70, 649-676.
27. Imhof, B. A. and Aurrand-Lions, M. (2004). Adhesion mechanisms regulating the migration of monocytes. Nat. Rev. Immunol. 4, 432-444.
28. Jones, G. E, Zicha, D, Dunn, G. A., Blundell, M. and Thrasher, A. (2002). Restoration of pordosomes and chemotaxis in Wiskott-Aldrich syndrome macrophages following induced expression of WASp. Int. J. Biochem. Cell Biol. 34, 806-815.
29. Kanehisa, J, Yamanaka, T., Doi, S., Turksen, K., Heersche, J. N., Aubin, J.E. and Takeuchi, H. (1990). A band of F-actin containing podosomes is involved in bone resorption by osteoclasts. Bone 11, 287-293.
30. Kaverina, I., Stradal, T. E. and Gimona, M. (2003). Podosome formation in cultured A7r5 vascular smooth muscle cells requires Arp26-dependent de-novo actin polymerization at discrete microdomains. J. Cell Sci. 116, 4915-4924.
31. Krylyshkina, O., Anderson, K. I., Kaverina, I., Upmann I., Manstein, D. J,, Small, J. V. and Toomre, D. K. (2003). Nanometer targeting of microtubules to focal adhesions. J. Cell Biol. 161, 853-859.
32. Lakkakorpi, P. T. and Vaananen, H. K. (1991). Kinetics of the osteoclast cytoskeleton during the resorption cycle in vitro. J. Bone Miner. Res. 6, 817-826.
33. Linder, S. and Aepfelbacher, M. (2003). Podosomes: adhesion hot-spots of invasive cells. Trends Cell Biol. 13, 376-385.
34. Linder, S., Nelson, D., Weiss, M. and Aepfelbacher, M. (1999). Wiskott-Aldrich syndrome protein regulates pordosomes in primary human macrophages. Proc. Natl. Acad. Sci. USA 96, 9648-9653.
35. Machesky, L. M. and Insall, R. H. (1998). Scarl and the related Wiskott-Aldrich syndrome protein, WASP, regulate the actin cytoskeleton through the Arp2/3 complex. Curr. Biol. 8, 1347-1356.
36. Marchisio, P. C., Cirillo, D., Naldini, L., Primavera, M. V., Teti, A. and Zambonin-Zallone, A. (1984). Cell-substratum interaction of cultured avian osteoclasts is mediated by specific adhesion structures. J. Cell Biol. 99, 1696-1705.
37. Marchisio, P. C., Cirillo, D., Teti, A., Zambonin-Zallone, A. and Tarone, G. (1987). Rous sarcoma virus-transformed fibroblasts and cells of monocytic origin display a peculiar dot-like organization of cytoskeletal proteins involved in microfilament-membrane interactions. Exp. Cell Res. 169, 202-214.
38. Moreau, V., Tatin, F., Varon, C. and Genot, E. (2003). Actin can reorganize into podosomes in aortic endothelial cells, a process controlled by Cdc42 and RhoA. Mol. Cell Biol. 23, 6809-6822.
39. Mukhopadhyay, S., Ramars, A. S., Ochs, H. D. and Dash, D. (2001). Bruton's tyrosine kinase is a substrate of calpain in human platelets. FEBS Lett. 505, 37-41.
40. O'Connell, K. A. and Edidin, M. (1990). A mouse lymphoid endothelial cell line immortalized by simian virus 40 binds lymphocytes and retains functional characteristics of normal endothelial cells. J. Immunol. 144, 521-525.
41. Oda, A., Ochs, H. D., Druker, B. J., Ozaki, K., Watanabe C., Handa, M., Miyakawa, Y. and Ikeda, Y. (1998). Collagen induces tyrosine phosphorylation of Wiskott-Aldrich syndrome protein in human platelets. Blood 92, 1852-1858.
42. Oda, A., Ochs, H. D., Lasky, L. A., Spencer, S., Ozald, K., Fujihara, M., Handa, M., Ikebuchi, K. and Ikeda, H. (2001). CrkL is an adapter for Wiskott-Aldrich syndrome protein and Syk. Blood 97, 2633-2639.
43. Osiak, A. E., Zenner, G. and Linder, S. (2005). Subconfluent endothelial cells form podosomes downstream of cytokine and RhoGTPase signaling. Exp. Cell Res. 307, 342-353.
44. Ridley, A. J., Schwartz, M. A., Burridge, K., Firtel, R. A., Ginsberg, M. H., Borisy, G., Parsons, J. T. and Horwitz, A. R. (2003). Cell migration: integrating signals from front to back. Science 302, 1704-1709.
45. Rock, M. T., Dix, A. R., Brooks, W. H. and Roszman, T. L. (2000). Beta1 integrin-mediated T cell adhesion and cell spreading are regulated by calpain. Exp. Cell Res. 261, 260-270.
46. Selliah, N., Brooks, W. H. and Roszman, T. L. (1996). Proteolytic cleavage of alpha-actinin by calpain in T cells stimulated with anti-CD3 monoclonal antibody. J. Immunol. 156, 3215-3221.
47. Small, J. V., Geiger, B., Kaverina, I. and Bershadsky, A. (2002). How do microtubules guide migrating cells? Nat. Rev. Mol. Cell Biol. 3, 957-964.
48. Snapper, S. B., Rosen, F. S., Mizoguchi, E., Cohen, P., Kban, W., Liu, C. H,, Hagemann, T. L., Kwan, S. P., Ferrini, R., Davidson, L. et al. (1998). Wiskott-Aldrich syndrome protein-deficient mice reveal a role for WASP in T but not B cell activation. Immunity 9, 81-91.
49. Spinardi, L,. Rietdorf, J., Nitsch, L., Bono, M., Tacchetti, C., Way, M.and Marchisio, P. C. (2004). A dynamic podosome-like structure of epithelial cells. Exp. Cell Res. 295. 360-374.
50. Stewart, M. P., McDowall, A. and Hogg, N. (1998). LFA-1-mediated adhesion is regulated by cytoskeletal restraint and by a Ca2+-dependent protease, calpain. J. Cell Biol. 140, 699-707.
51. Thrasher, A. J. (2002). WASp in immune-system organization and function. Nat. Rev. Immunol. 2, 635-646.
52. West, M. A., Antonlou, A. N., Prescott, A. R., Azuma, T., Kwiatkowski, D. J. and Watts, C. (1999). Membrane ruffling, macroprinocytosis and antigen presentation in the absence of gelsolin in murrine dendritic cells. Eur. J. Immunol. 29, 3450-3455.
53. West, M. A., Wallin, R. P. A,, Matthews, S. P., Svensson, H. G,, Zara, R,, Ljunggren, H. G., Prescott, A. R. and Watts, C. (2004). Enhanced dendritic cell antigen capture via toll-Eke receptor-induced actin remodeling. Science 305, 1153-1157.
54. Yan, B, Calderwood, D. A., Yaspan, B. and Ginsberg, M. H. (2001). Calpain cleavage promotes talin binding to the beta 3 integrin cytoplasmic domain. J. Biol. Chem. 276, 28164-28170.
55. Zarnbonin-Zallone, A., Teti, A., Carano, A. and Marchisio, P. C. (1988). The distribution of pordosomes in osteoclasts cultured on bone laminae: effect of retinol. J. Bone Miner. Res. 3, 517-523.
56. Zufferey. R., Nagy, D., Mandel, R. J., Naldini, L. and Trono, D. (1997). Multiply attenuated lentiviral vector achieves efficient gene delivery in vivo. Nat. Biotechnol. 15, 871-875.