Syndecan-1 controls cell migration by activating rap1 to regulate focal adhesion disassembly

Journal of Cell Science

Volumn 125, Issue 21, 2012, Pages 5188-5195

  Altemeier, William A ^a   Schlesinger, Saundra Y ^a   Buell, Catherine A ^a   Parks, William C ^a   Chen, Peter ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Focal adhesion; Migration; Syndecan 1

Indexed keywords

FOCAL ADHESION KINASE; PAXILLIN; RAP1 PROTEIN; SYNDECAN 1;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL MIGRATION; CONTROLLED STUDY; LUNG ALVEOLUS EPITHELIUM; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN METABOLISM;

CELL LINE; CELL MOVEMENT; ENZYME ACTIVATION; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; FOCAL ADHESIONS; HUMANS; KINETICS; MICROTUBULES; NOCODAZOLE; PAXILLIN; PROTEIN MULTIMERIZATION; RAP1 GTP-BINDING PROTEINS; SYNDECAN-1; TIME-LAPSE IMAGING; TUBULIN MODULATORS;

EID: 84867411149     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.109884     Document Type: Article

References (60)

1. Alexandrova, A. Y., Arnold, K., Schaub, S., Vasiliev, J. M., Meister, J.-J., Bershadsky, A. D. and Verkhovsky, A. B. (2008). Comparative dynamics of retrograde actin flow and focal adhesions: formation of nascent adhesions triggers transition from fast to slow flow. PLoS ONE 3, e3234.
2. Bass, M. D., Morgan, M. R. and Humphries, M. J. (2009). Syndecans shed their reputation as inert molecules. Sci. Signal. 2, pe18.
3. Beauvais, D. M. and Rapraeger, A. C. (2003). Syndecan-1-mediated cell spreading requires signaling by alphavbeta3 integrins in human breast carcinoma cells. Exp. Cell Res. 286, 219-232.
4. Beauvais, D. M. and Rapraeger, A. C. (2010). Syndecan-1 couples the insulin-like growth factor-1 receptor to inside-out integrin activation. J. Cell Sci. 123, 3796-3807.
5. Beauvais, D. M., Burbach, B. J. and Rapraeger, A. C. (2004). The syndecan-1 ectodomain regulates alphavbeta3 integrin activity in human mammary carcinoma cells. J. Cell Biol. 167, 171-181.
6. Beauvais, D. M., Ell, B. J., McWhorter, A. R. and Rapraeger, A. C. (2009). Syndecan-1 regulates alphavbeta3 and alphavbeta5 integrin activation during angiogenesis and is blocked by synstatin, a novel peptide inhibitor. J. Exp. Med. 206, 691-705.
7. Beningo, K. A., Dembo, M., Kaverina, I., Small, J. V. and Wang, Y. L. (2001). Nascent focal adhesions are responsible for the generation of strong propulsive forces in migrating fibroblasts. J. Cell Biol. 153, 881-888.
8. Bhatt, A., Kaverina, I., Otey, C. and Huttenlocher, A. (2002). Regulation of focalcomplex composition and disassembly by the calcium-dependent protease calpain.J. Cell Sci. 115, 3415-3425.
9. Boettner, B. and Van Aelst, L. (2009). Control of cell adhesion dynamics by Rap1 signaling. Curr. Opin. Cell Biol. 21, 684-693.
10. Broussard, J. A., Webb, D. J. and Kaverina, I. (2008). Asymmetric focal adhesion disassembly in motile cells. Curr. Opin. Cell Biol. 20, 85-90.
11. Carmona, G., Göttig, S., Orlandi, A., Scheele, J., Bäuerle, T., Jugold, M., Kiessling, F., Henschler, R., Zeiher, A. M., Dimmeler, S. et al. (2009). Role of the small GTPase Rap1 for integrin activity regulation in endothelial cells and angiogenesis. Blood 113, 488-497.
12. Chen, P., Abacherli, L. E., Nadler, S. T., Wang, Y., Li, Q. and Parks, W. C. (2009). MMP7 shedding of syndecan-1 facilitates re-epithelialization by affecting alpha(2)-beta(1) integrin activation. PLoS ONE 4, e6565.
13. Choi, C. K., Vicente-Manzanares, M., Zareno, J., Whitmore, L. A., Mogilner, A. and Horwitz, A. R. (2008). Actin and alpha-actinin orchestrate the assembly and maturation of nascent adhesions in a myosin II motor-independent manner. Nat. Cell Biol. 10, 1039-1050.
14. Couchman, J. R. (2003). Syndecans: proteoglycan regulators of cell-surface microdomains? Nat. Rev. Mol. Cell Biol. 4, 926-938.
15. Crosby, L. M. and Waters, C. M. (2010). Epithelial repair mechanisms in the lung. Am. J. Physiol. Lung Cell Mol. Physiol. 298, L715-L731.
16. Deramaudt, T. B., Dujardin, D., Hamadi, A., Noulet, F., Kolli, K., De Mey, J., Takeda, K. and Rondé, P. (2011). FAK phosphorylation at Tyr-925 regulates crosstalk between focal adhesion turnover and cell protrusion. Mol. Biol. Cell 22, 964-975.
17. DiMilla, P. A., Stone, J. A., Quinn, J. A., Albelda, S. M. and Lauffenburger, D. A. (1993). Maximal migration of human smooth muscle cells on fibronectin and type IV collagen occurs at an intermediate attachment strength. J. Cell Biol. 122, 729-737.
18. Endo, K., Takino, T., Miyamori, H., Kinsen, H., Yoshizaki, T., Furukawa, M. and Sato, H. (2003). Cleavage of syndecan-1 by membrane type matrix metalloproteinase-1 stimulates cell migration. J. Biol. Chem. 278, 40764-40770.
19. Ezratty, E. J., Partridge, M. A. and Gundersen, G. G. (2005). Microtubule-induced focal adhesion disassembly is mediated by dynamin and focal adhesion kinase. Nat. Cell Biol. 7, 581-590.
20. Galbraith, C. G. and Sheetz, M. P. (1997). A micromachined device provides a new bend on fibroblast traction forces. Proc. Natl. Acad. Sci. USA 94, 9114-9118.
21. Galbraith, C. G., Yamada, K. M. and Sheetz, M. P. (2002). The relationship between force and focal complex development. J. Cell Biol. 159, 695-705.
22. García-Mata, R. and Burridge, K. (2007). Catching a GEF by its tail. Trends Cell Biol. 17, 36-43.
23. Gloerich, M. and Bos, J. L. (2011). Regulating Rap small G-proteins in time and space. Trends Cell Biol. 21, 615-623.
24. Gupton, S. L. and Waterman-Storer, C. M. (2006). Spatiotemporal feedback between actomyosin and focal-adhesion systems optimizes rapid cell migration. Cell 125, 1361-1374.
25. Hamadi, A., Bouali, M., Dontenwill, M., Stoeckel, H., Takeda, K. and Rondé, P. (2005). Regulation of focal adhesion dynamics and disassembly by phosphorylation of FAK at tyrosine 397. J. Cell Sci. 118, 4415-4425.
26. Han, J., Lim, C. J., Watanabe, N., Soriani, A., Ratnikov, B., Calderwood, D. A., Puzon-McLaughlin, W., Lafuente, E. M., Boussiotis, V. A., Shattil, S. J. et al. (2006). Reconstructing and deconstructing agonist-induced activation of integrin alphaIIbbeta3. Curr. Biol. 16, 1796-1806.
27. Hayashida, K., Stahl, P. D. and Park, P. W. (2008). Syndecan-1 ectodomain shedding is regulated by the small GTPase Rab5. J. Biol. Chem. 283, 35435-35444.
28. Hogan, C., Serpente, N., Cogram, P., Hosking, C. R., Bialucha, C. U., Feller, S. M., Braga, V. M. M., Birchmeier, W. and Fujita, Y. (2004). Rap1 regulates the formation of E-cadherin-based cell-cell contacts. Mol. Cell. Biol. 24, 6690-6700.
29. Huttenlocher, A. and Horwitz, A. R. (2011). Integrins in cell migration. Cold Spring Harb. Perspect. Biol. 3, a005074.
30. Jossin, Y. and Cooper, J. A. (2011). Reelin, Rap1 and N-cadherin orient the migration of multipolar neurons in the developing neocortex. Nat. Neurosci. 14, 697-703.
31. Katagiri, K., Maeda, A., Shimonaka, M. and Kinashi, T. (2003). RAPL, a Rap1- binding molecule that mediates Rap1-induced adhesion through spatial regulation of LFA-1. Nat. Immunol. 4, 741-748.
32. Kato, M., Saunders, S., Nguyen, H. and Bernfield, M. (1995). Loss of cell surface syndecan-1 causes epithelia to transform into anchorage-independent mesenchymelike cells. Mol. Biol. Cell 6, 559-576.
33. Kaverina, I., Rottner, K. and Small, J. V. (1998). Targeting, capture, and stabilization of microtubules at early focal adhesions. J. Cell Biol. 142, 181-190.
34. Kaverina, I., Krylyshkina, O. and Small, J. V. (1999). Microtubule targeting of substrate contacts promotes their relaxation and dissociation. J. Cell Biol. 146, 1033-1044.
35. Kaverina, I., Krylyshkina, O. and Small, J. V. (2002). Regulation of substrate adhesion dynamics during cell motility. Int. J. Biochem. Cell Biol. 34, 746-761.
36. Knox, A. L. and Brown, N. H. (2002). Rap1 GTPase regulation of adherens junction positioning and cell adhesion. Science 295, 1285-1288.
37. Kooistra, M. R. H., Dubé, N. and Bos, J. L. (2007). Rap1: a key regulator in cell-cell junction formation. J. Cell Sci. 120, 17-22.
38. Laukaitis, C. M., Webb, D. J., Donais, K. and Horwitz, A. F. (2001). Differential dynamics of alpha 5 integrin, paxillin, and alpha-actinin during formation and disassembly of adhesions in migrating cells. J. Cell Biol. 153, 1427-1440.
39. Lawson, C., Lim, S. T., Uryu, S., Chen, X. L., Calderwood, D. A. and Schlaepfer, D. D. (2012). FAK promotes recruitment of talin to nascent adhesions to control cell motility. J. Cell Biol. 196, 223-232.
40. Leppä, S., Vleminckx, K., Van Roy, F. and Jalkanen, M. (1996). Syndecan-1 expression in mammary epithelial tumor cells is E-cadherin-dependent. J. Cell Sci. 109, 1393-1403.
41. McQuade, K. J., Beauvais, D. M., Burbach, B. J. and Rapraeger, A. C. (2006). Syndecan-1 regulates alphavbeta5 integrin activity in B82L fibroblasts. J. Cell Sci. 119, 2445-2456.
42. Millon-Frémillon, A., Bouvard, D., Grichine, A., Manet-Dupé, S., Block, M. R. and Albiges-Rizo, C. (2008). Cell adaptive response to extracellular matrix density is controlled by ICAP-1-dependent beta1-integrin affinity. J. Cell Biol. 180, 427-441.
43. Montell, D. J. (2008). Morphogenetic cell movements: diversity from modular mechanical properties. Science 322, 1502-1505.
44. Morgan, M. R., Humphries, M. J. and Bass, M. D. (2007). Synergistic control of cell adhesion by integrins and syndecans. Nat. Rev. Mol. Cell Biol. 8, 957-969.
45. Nathan, C. and Ding, A. (2010). Nonresolving inflammation. Cell 140, 871-882.
46. Nourry, C., Grant, S. G. N. and Borg, J.-P. (2003). PDZ domain proteins: plug and play! Sci. STKE 2003, RE7.
47. Palecek, S. P., Loftus, J. C., Ginsberg, M. H., Lauffenburger, D. A. and Horwitz, A. F. (1997). Integrin-ligand binding properties govern cell migration speed through cell-substratum adhesiveness. Nature 385, 537-540.
48. Parsons, J. T., Horwitz, A. R. and Schwartz, M. A. (2010). Cell adhesion: integrating cytoskeletal dynamics and cellular tension. Nat. Rev. Mol. Cell Biol. 11, 633-643.
49. Price, L. S., Hajdo-Milasinovic, A., Zhao, J., Zwartkruis, F. J. T., Collard, J. G. and Bos, J. L. (2004). Rap1 regulates E-cadherin-mediated cell-cell adhesion. J. Biol. Chem. 279, 35127-35132.
50. Raftopoulou, M. and Hall, A. (2004). Cell migration: Rho GTPases lead the way. Dev. Biol. 265, 23-32.
51. 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.
52. Takahashi, M., Rikitake, Y., Nagamatsu, Y., Hara, T., Ikeda, W., Hirata, K.-I. and Takai, Y. (2008). Sequential activation of Rap1 and Rac1 small G proteins by PDGF locally at leading edges of NIH3T3 cells. Genes Cells 13, 549-569.
53. Vicente-Manzanares, M., Choi, C. K. and Horwitz, A. R. (2009). Integrins in cellmigration - the actin connection. J. Cell Sci. 122, 199-206.
54. von Wichert, G., Haimovich, B., Feng, G.-S. and Sheetz, M. P. (2003). Forcedependent integrin-cytoskeleton linkage formation requires downregulation of focal complex dynamics by Shp2. EMBO J. 22, 5023-5035.
55. Webb, D. J., Parsons, J. T. and Horwitz, A. F. (2002). Adhesion assembly,disassembly and turnover in migrating cells - over and over and over again. Nat. Cell Biol. 4, E97-E100.
56. Webb, D. J., Donais, K., Whitmore, L. A., Thomas, S. M., Turner, C. E., Parsons, J. T. and Horwitz, A. F. (2004). FAK-Src signalling through paxillin, ERK and MLCK regulates adhesion disassembly. Nat. Cell Biol. 6, 154-161.
57. Weber, G. F., Bjerke, M. A. and DeSimone, D. W. (2011). Integrins and cadherins join forces to form adhesive networks. J. Cell Sci. 124, 1183-1193.
58. Wehrle-Haller, B. (2012). Structure and function of focal adhesions. Curr. Opin. Cell Biol. 24, 116-124.
59. You, Y., Richer, E. J., Huang, T. and Brody, S. L. (2002). Growth and differentiation of mouse tracheal epithelial cells: selection of a proliferative population. Am. J. Physiol. Lung Cell Mol. Physiol. 283, L1315-L1321.
60. Zaidel-Bar, R., Milo, R., Kam, Z. and Geiger, B. (2007). A paxillin tyrosine phosphorylation switch regulates the assembly and form of cell-matrix adhesions. J. Cell Sci. 120, 137-148.