Integrin-mediated cell attachment induces a PAK4-dependent feedback loop regulating cell adhesion through modified integrin αvβ5 clustering and turnover

Molecular Biology of the Cell

Volumn 21, Issue 19, 2010, Pages 3317-3329

  Li, Zhilun ^a   Lock, John G ^a   Olofsson, Helene ^a   Kowalewski, Jacob M ^b   Teller, Steffen ^a,c   Liu, Yajuan ^a   Zhang, Hongquan ^a,d   Strömblad, Staffan ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b ROYAL INSTITUTE OF TECHNOLOGY   (Sweden)

^c UNIVERSITY OF GREIFSWALD   (Germany)

^d PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

Author keywords

[No Author keywords available]

Indexed keywords

F ACTIN; P21 ACTIVATED KINASE 4; VITRONECTIN; VITRONECTIN RECEPTOR;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL MOTILITY; CELL SPREADING; CONTROLLED STUDY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; NEGATIVE FEEDBACK; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN METABOLISM;

ACTINS; ANIMALS; CELL ADHESION; CELL LINE, TUMOR; CELL MOVEMENT; CERCOPITHECUS AETHIOPS; COS CELLS; ENZYME ACTIVATION; EXTRACELLULAR MATRIX; FEEDBACK, PHYSIOLOGICAL; GENE KNOCKDOWN TECHNIQUES; HUMANS; P21-ACTIVATED KINASES; RECEPTORS, VITRONECTIN; VITRONECTIN;

EID: 77958031728     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E10-03-0245     Document Type: Article

References (50)

1. Abo, A., Qu, J., Cammarano, M. S., Dan, C., Fritsch, A., Baud, V., Belisle, B., and Minden, A. (1998). PAK4, a novel effector for Cdc42Hs, is implicated in the reorganization of the actin cytoskeleton and in the formation of filopodia. EMBO J. 17, 6527-6540.
2. Ahmed, T., Shea, K., Masters, J. R., Jones, G. E., and Wells, C. M. (2008). A PAK4-LIMK1 pathway drives prostate cancer cell migration downstream of HGF. Cell. Signal. 20, 1320-1328.
3. Albiges-Rizo, C., Destaing, O., Fourcade, B., Planus, E., and Block, M. R. (2009). Actin machinery and mechanosensitivity in invadopodia, podosomes and focal adhesions. J. Cell Sci. 122, 3037-3049.
4. Anthis, N. J., Haling, J. R., Oxley, C. L., Memo, M., Wegener, K. L., Lim, C. J., Ginsberg, M. H., and Campbell, I. D. (2009). Beta integrin tyrosine phosphorylation is a conserved mechanism for regulating talin-induced integrin activation. J. Biol. Chem. 284, 36700-36710.
5. Ballestrem, C., Hinz, B., Imhof, B. A., and Wehrle-Haller, B. (2001). Marching at the front and dragging behind: differential alphaVbeta3-integrin turnover regulates focal adhesion behavior. J. Cell Biol. 155, 1319-1332.
6. Bao, W., Thullberg, M., Zhang, H., Onischenko, A., and Strömblad, S. (2002). Cell attachment to the extracellular matrix induces proteasomal degradation of p21(CIP1) via Cdc42/Rac1 signaling. Mol. Cell. Biol. 22, 4587-4597.
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. Berrier, A. L., and Yamada, K. M. (2007). Cell-matrix adhesion. J. Cell. Physiol. 213, 565-573.
9. Bouvard, D., Vignoud, L., Dupe-Manet, S., Abed, N., Fournier, H. N., Vincent-Monegat, C., Retta, S. F., Fassler, R., and Block, M. R. (2003). Disruption of focal adhesions by integrin cytoplasmic domain-associated protein-1 alpha. J. Biol. Chem. 278, 6567-6574.
10. Callow, M. G., Clairvoyant, F., Zhu, S., Schryver, B., Whyte, D. B., Bischoff, J. R., Jallal, B., and Smeal, T. (2002). Requirement for PAK4 in the anchorage-independent growth of human cancer cell lines. J. Biol. Chem. 277, 550-558.
11. Callow, M. G., Zozulya, S., Gishizky, M. L., Jallal, B., and Smeal, T. (2005). PAK4 mediates morphological changes through the regulation of GEF-H1. J. Cell Sci. 118, 1861-1872.
12. Carman, C. V., and Springer, T. A. (2003). Integrin avidity regulation: are changes in affinity and conformation underemphasized? Curr. Opin. Cell Biol. 15, 547-556.
13. Caswell, P. T., and Norman, J. C. (2006). Integrin trafficking and the control of cell migration. Traffic 7, 14-21.
14. Chrzanowska-Wodnicka, M., and Burridge, K. (1996). Rho-stimulated contractility drives the formation of stress fibers and focal adhesions. J. Cell Biol. 133, 1403-1415.
15. Coniglio, S. J., Zavarella, S., and Symons, M. H. (2008). Pak1 and Pak2 mediate tumor cell invasion through distinct signaling mechanisms. Mol. Cell. Biol. 28, 4162-4172.
16. Dan, C., Kelly, A., Bernard, O., and Minden, A. (2001). Cytoskeletal changes regulated by the PAK4 serine/threonine kinase are mediated by LIM kinase 1 and cofilin. J. Biol. Chem. 276, 32115-32121.
17. 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.
18. Hynes, R. O. (2002). Integrins: bidirectional, allosteric signaling machines. Cell 110, 673-687.
19. 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.
20. Kiosses, W. B., Daniels, R. H., Otey, C., Bokoch, G. M., and Schwartz, M. A. (1999). A role for p21-activated kinase in endothelial cell migration. J. Cell Biol. 147, 831-844.
21. Lauffenburger, D. A., and Horwitz, A. F. (1996). Cell migration: a physically integrated molecular process. Cell 84, 359-369.
22. Lee, J., and Jacobson, K. (1997). The composition and dynamics of cell-substratum adhesions in locomoting fish keratocytes. J. Cell Sci. 110, 2833-2844.
23. Li, Z., Zhang, H., Lundin, L., Thullberg, M., Liu, Y., Wang, Y., Claesson-Welsh, L., and Strömblad, S. (2010). p21-activated kinase 4 phosphorylation of integrin β5 Ser 759 and Ser 762 regulates cell migration. J. Biol. Chem. 285, 23699-23710.
24. Liu, Y., Xiao, H., Tian, Y., Nekrasova, T., Hao, X., Lee, H.J., Suh, N., Yang, C. S., and Minden, A. (2008). The pak4 protein kinase plays a key role in cell survival and tumorigenesis in athymic mice. Mol Cancer Res. 6, 1215-1224.
25. Lock, J. G., and Strömblad, S. Systems microscopy: an emerging strategy for the life sciences. Exp. Cell Res. 316, 1438-1444.
26. Lock, J. G., Wehrle-Haller, B., and Strömblad, S. (2008). Cell-matrix adhesion complexes: Master control machinery of cell migration. Semin. Cancer Biol. 18, 65-76.
27. Manser, E., Huang, H. Y., Loo, T. H., Chen, X. Q., Dong, J. M., Leung, T., and Lim, L. (1997). Expression of constitutively active alpha-PAK reveals effects of the kinase on actin and focal complexes. Mol. Cell. Biol. 17, 1129-1143.
28. Millon-Fremillon, A., Bouvard, D., Grichine, A., Manet-Dupe, 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.
29. Nayal, A., Webb, D. J., Brown, C. M., Schaefer, E. M., Vicente-Manzanares, M., and Horwitz, A.R. (2006). Paxillin phosphorylation at Ser273 localizes a GIT1-PIX-PAK complex and regulates adhesion and protrusion dynamics. J. Cell Biol. 173, 587-589.
30. Numakawa, T., Ishimoto, T., Suzuki, S., Numakawa, Y., Adachi, N., Matsumoto, T., Yokomaku, D., Koshimizu, H., Fujimori, K. E., Hashimoto, R., Taguchi, T., and Kunugi, H. (2004). Neuronal roles of the integrin-associated protein (IAP/CD47) in developing cortical neurons. J. Biol. Chem. 279, 43245-43253.
31. Oxley, C. L., Anthis, N. J., Lowe, E. D., Vakonakis, I., Campbell, I. D., and Wegener, K. L. (2008). An integrin phosphorylation switch: the effect of beta3 integrin tail phosphorylation on Dok1 and talin binding. J. Biol. Chem. 283, 5420-5426.
32. Pellinen, T., Arjonen, A., Vuoriluoto, K., Kallio, K., Fransen, J. A., and Ivaska, J. (2006). Small GTPase Rab21 regulates cell adhesion and controls endosomal traffic of beta1-integrins. J. Cell Biol. 173, 767-780.
33. Price, L. S., Leng, J., Schwartz, M. A., and Bokoch, G. M. (1998). Activation of Rac and Cdc42 by integrins mediates cell spreading. Mol. Biol. Cell 9, 1863-1871.
34. Qu, J., Cammarano, M. S., Shi, Q., Ha, K. C., de Lanerolle, P., and Minden, A. (2001). Activated PAK4 regulates cell adhesion and anchorage-independent growth. Mol. Cell. Biol. 21, 3523-3533.
35. Qu, J., Li, X., Novitch, B. G., Zheng, Y., Kohn, M., Xie, J.M., Kozinn, S., Bronson, R., Beg, A. A., and Minden, A. (2003). PAK4 kinase is essential for embryonic viability and for proper neuronal development. Mol. Cell. Biol. 23, 7122-7133.
36. Scott, L., Zelenin, S., Malmersjo, S., Kowalewski, J. M., Markus, E. Z., Nairn, A. C., Greengard, P., Brismar, H., and Aperia, A. (2006). Allosteric changes of the NMDA receptor trap diffusible dopamine 1 receptors in spines. Proc. Natl. Acad. Sci. USA 103, 762-767.
37. Shemesh, T., Geiger, B., Bershadsky, A. D., and Kozlov, M. M. (2005). Focal adhesions as mechanosensors: a physical mechanism. Proc. Natl. Acad. Sci. USA 102, 12383-12388.
38. Soosairajah, J., Maiti, S., Wiggan, O., Sarmiere, P., Moussi, N., Sarcevic, B., Sampath, R., Bamburg, J. R., and Bernard, O. (2005). Interplay between components of a novel LIM kinase-slingshot phosphatase complex regulates cofilin. EMBO J. 24, 473-486.
39. Stofega, M. R., Sanders, L. C., Gardiner, E. M., and Bokoch, G. M. (2004). Constitutive p21-activated kinase (PAK) activation in breast cancer cells as a result of mislocalization of PAK to focal adhesions. Mol. Biol. Cell 15, 2965-2977.
40. Tadokoro, S., Shattil, S. J., Eto, K., Tai, V., Liddington, R. C., de Pereda, J. M., Ginsberg, M. H., and Calderwood, D. A. (2003). Talin binding to integrin beta tails: a final common step in integrin activation. Science 302, 103-106.
41. 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, E97-100.
42. Wehrle-Haller, B. (2007). Analysis of integrin dynamics by fluorescence recovery after photobleaching. Methods Mol. Biol. 370, 173-202.
43. Wehrle-Haller, B., and Imhof, B. A. (2003). Actin, microtubules and focal adhesion dynamics during cell migration. Int. J. Biochem. Cell Biol. 35, 39-50.
44. Wells, C. M., Abo, A., and Ridley, A. J. (2002). PAK4 is activated via PI3K in HGF-stimulated epithelial cells. J. Cell Sci. 115, 3947-3956.
45. Xu, J., Wang, F., Van Keymeulen, A., Herzmark, P., Straight, A., Kelly, K., Takuwa, Y., Sugimoto, N., Mitchison, T., and Bourne, H. R. (2003). Divergent signals and cytoskeletal assemblies regulate self-organizing polarity in neutrophils. Cell 114, 201-214.
46. Yebra, M., Parry, G. C., Strömblad, S., Mackman, N., Rosenberg, S., Mueller, B. M., and Cheresh, D. A. (1996). Requirement of receptor-bound urokinasetype plasminogen activator for integrin alphavbeta5-directed cell migration. J. Biol. Chem. 271, 29393-29399.
47. Zamir, E., and Geiger, B. (2001). Molecular complexity and dynamics of cell-matrix adhesions. J. Cell Sci. 114, 3583-3590.
48. Zhang, H., Berg, J. S., Li, Z., Wang, Y., Lang, P., Sousa, A. D., Bhaskar, A., Cheney, R. E., and Strömblad, S. (2004). Myosin-X provides a motor-based link between integrins and the cytoskeleton. Nat. Cell Biol. 6, 523-531.
49. Zhang, H., Li, Z., Viklund, E. K., and Strömblad, S. (2002). P21-activated kinase 4 interacts with integrin alpha v beta 5 and regulates alpha v beta 5-mediated cell migration. J. Cell Biol. 158, 1287-1297.
50. Zhdankina, O., Strand, N. L., Redmond, J. M., and Boman, A. L. (2001). Yeast GGA proteins interact with GTP-bound Arf and facilitate transport through the Golgi. Yeast 18, 1-18.