Palladin promotes assembly of non-contractile dorsal stress fibers through VASP recruitment

Journal of Cell Science

Volumn 127, Issue 9, 2014, Pages 1887-1898

  Gateva, Gergana ^a   Tojkander, Sari ^a   Koho, Sami ^b   Carpen, Olli ^c   Lappalainen, Pekka ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF TURKU   (Finland)

^c TURKU UNIVERSITY HOSPITAL   (Finland)

Author keywords

Actin; Focal adhesion; Palladin; Stress fiber; VASP

Indexed keywords

COLLAGEN; PALLADIN; PROTEIN; UNCLASSIFIED DRUG; VASODILATOR STIMULATED PHOSPHOPROTEIN; ACTIN; ACTIN BINDING PROTEIN; CELL ADHESION MOLECULE; CYTOSKELETON PROTEIN; PALLADIN PROTEIN, HUMAN; PHOSPHOPROTEIN; VASODILATOR-STIMULATED PHOSPHOPROTEIN;

ARTICLE; CELL ADHESION; CELL MIGRATION; CELL STRUCTURE; CONTROLLED STUDY; FOCAL ADHESION; HUMAN; HUMAN CELL; MORPHOGENESIS; OSTEOSARCOMA; OSTEOSARCOMA CELL; PRIORITY JOURNAL; PROTEIN LOCALIZATION; STRESS FIBER; FLUORESCENCE MICROSCOPY; IMMUNOPRECIPITATION; MECHANOTRANSDUCTION; METABOLISM; PHYSIOLOGY; TUMOR CELL LINE; WESTERN BLOTTING;

ACTINS; BLOTTING, WESTERN; CELL ADHESION MOLECULES; CELL LINE, TUMOR; CYTOSKELETAL PROTEINS; HUMANS; IMMUNOPRECIPITATION; MECHANOTRANSDUCTION, CELLULAR; MICROFILAMENT PROTEINS; MICROSCOPY, FLUORESCENCE; PHOSPHOPROTEINS; STRESS FIBERS;

EID: 84899734615     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.135780     Document Type: Article

References (52)

1. 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.
2. Bershadsky, A., Kozlov, M. and Geiger, B. (2006). Adhesion-mediated mechanosensitivity: a time to experiment, and a time to theorize. Curr. Opin. Cell Biol. 18, 472-481.
3. Boukhelifa, M., Parast, M. M., Valtschanoff, J. G., LaMantia, A. S., Meeker, R. B. and Otey, C. A. (2001). A role for the cytoskeleton-associated protein palladin in neurite outgrowth. Mol. Biol. Cell 12, 2721-2729.
4. Boukhelifa, M., Hwang, S. J., Valtschanoff, J. G., Meeker, R. B., Rustioni, A. and Otey, C. A. (2003). A critical role for palladin in astrocyte morphology and response to injury. Mol. Cell. Neurosci. 23, 661-668.
5. Boukhelifa, M., Parast, M. M., Bear, J. E., Gertler, F. B. and Otey, C. A. (2004). Palladin is a novel binding partner for Ena/VASP family members. Cell Motil. Cytoskeleton 58, 17-29.
6. Boukhelifa, M., Moza, M., Johansson, T., Rachlin, A., Parast, M., Huttelmaier, S., Roy, P., Jockusch, B. M., Carpen, O., Karlsson, R. et al. (2006). The proline-rich protein palladin is a binding partner for profilin. FEBS J. 273, 26-33.
7. Breitsprecher, D., Kiesewetter, A. K., Linkner, J., Vinzenz, M., Stradal, T. E. B., Small, J. V., Curth, U., Dickinson, R. B. and Faix, J. (2011). Molecular mechanism of Ena/VASP-mediated actin-filament elongation. EMBO J. 30, 456-467.
8. Bugyi, B. and Carlier, M. F. (2010). Control of actin filament treadmilling in cell motility. In Annual Review of Biophysics, Vol. 39 (ed. D. C. Rees, K. A. Dill and J. R. Williamson), pp. 449-470. Palo Alto, CA: Annual Reviews.
9. Burnette, D. T., Manley, S., Sengupta, P., Sougrat, R., Davidson, M. W., Kachar, B. and Lippincott-Schwartz, J. (2011). A role for actin arcs in the leading-edge advance of migrating cells. Nat. Cell Biol. 13, 371-382.
10. Chin, Y. R. and Toker, A. (2010). The actin-bundling protein palladin is an Akt1-specific substrate that regulates breast cancer cell migration. Mol. Cell 38, 333-344.
11. Dixon, R. D. S., Arneman, D. K., Rachlin, A. S., Sundaresan, N. R., Costello, M. J., Campbell, S. L. and Otey, C. A. (2008). Palladin is an actin cross-linking protein that uses immunoglobulin-like domains to bind filamentous actin. J. Biol. Chem. 283, 6222-6231.
12. Fan, L., Pellegrin, S., Scott, A. and Mellor, H. (2010). The small GTPase Rif is an alternative trigger for the formation of actin stress fibers in epithelial cells. J. Cell Sci. 123, 1247-1252.
13. Fraley, S. I., Feng, Y., Krishnamurthy, R., Kim, D.-H., Celedon, A., Longmore, G. D. and Wirtz, D. (2010). A distinctive role for focal adhesion proteins in threedimensional cell motility. Nat. Cell Biol. 12, 598-604.
14. Goicoechea, S., Arneman, D., Disanza, A., Garcia-Mata, R., Scita, G. and Otey, C. A. (2006). Palladin binds to Eps8 and enhances the formation of dorsal ruffles and podosomes in vascular smooth muscle cells. J. Cell Sci. 119, 3316-3324.
15. Goicoechea, S. M., Arneman, D. and Otey, C. A. (2008). The role of palladin in actin organization and cell motility. Eur. J. Cell Biol. 87, 517-525.
16. Goicoechea, S. M., Bednarski, B., Garci{dotless}́a-Mata, R., Prentice-Dunn, H., Kim, H. J. and Otey, C. A. (2009). Palladin contributes to invasive motility in human breast cancer cells. Oncogene 28, 587-598.
17. Goicoechea, S. M., Bednarski, B., Stack, C., Cowan, D. W., Volmar, K., Thorne, L., Cukierman, E., Rustgi, A. K., Brentnall, T., Hwang, R. F. et al. (2010). Isoform-specific upregulation of palladin in human and murine pancreas tumors. PLoS ONE 5, e10347.
18. Goicoechea, S. M., Garci{dotless}́a-Mata, R., Staub, J., Valdivia, A., Sharek, L., McCulloch, C. G., Hwang, R. F., Urrutia, R., Yeh, J. J., Kim, H. J. et al. (2013). Palladin promotes invasion of pancreatic cancer cells by enhancing invadopodia formation in cancer-associated fibroblasts. Oncogene.
19. Haikarainen, T., Chen, W. Q., Lubec, G., Kursula, P. (2009). Structure, modifications and ligand-binding properties of rat profilin 2a. Acta Crystallogr. D Biol. Crystallogr. 65, 303-311.
20. Hansen, S. D. and Mullins, R. D. (2010). VASP is a processive actin polymerase that requires monomeric actin for barbed end association. J. Cell Biol. 191, 571-584.
21. Heath, J. P. (1983). Direct evidence for microfilament-mediated capping of surface receptors on crawling fibroblasts. Nature 302, 532-534.
22. Hoffman, L. M., Jensen, C. C., Kloeker, S., Wang, C.-L. A., Yoshigi, M. and Beckerle, M. C. (2006). Genetic ablation of zyxin causes Mena/VASP mislocalization, increased motility, and deficits in actin remodeling. J. Cell Biol. 172, 771-782.
23. Hoffman, L. M., Jensen, C. C., Chaturvedi, A., Yoshigi, M. and Beckerle, M. C. (2012). Stretch-induced actin remodeling requires targeting of zyxin to stress fibers and recruitment of actin regulators. Mol. Biol. Cell 23, 1846-1859.
24. Hotulainen, P. and Lappalainen, P. (2006). Stress fibers are generated by two distinct actin assembly mechanisms in motile cells. J. Cell Biol. 173, 383-394.
25. Jacinto, A., Wood, W., Woolner, S., Hiley, C., Turner, L., Wilson, C., Martinez-Arias, A. and Martin, P. (2002). Dynamic analysis of actin cable function during Drosophila dorsal closure. Curr. Biol. 12, 1245-1250.
26. Jin, L., Kern, M. J., Otey, C. A., Wamhoff, B. R. and Somlyo, A. V. (2007). Angiotensin II, focal adhesion kinase, and PRX1 enhance smooth muscle expression of lipoma preferred partner and its newly identified binding partner palladin to promote cell migration. Circ. Res. 100, 817-825.
27. Khatau, S. B., Hale, C. M., Stewart-Hutchinson, P. J., Patel, M. S., Stewart, C. L., Searson, P. C., Hodzic, D. and Wirtz, D. (2009). A perinuclear actin cap regulates nuclear shape. Proc. Natl. Acad. Sci. USA 106, 19017-19022.
28. Kovac, B., Teo, J. L., Mäkelä, T. P. and Vallenius, T. (2013). Assembly of noncontractile dorsal stress fibers requires a-actinin-1 and Rac1 in migrating and spreading cells. J. Cell Sci. 126, 263-273.
29. Kubow, K. E. and Horwitz, A. R. (2011). Reducing background fluorescence reveals adhesions in 3D matrices. Nat. Cell Biol. 13, 3-5, author reply 5-7.
30. Liu, X.-S., Luo, H.-J., Yang, H., Wang, L., Kong, H., Jin, Y.-E., Wang, F., Gu, M.-M., Chen, Z., Lu, Z.-Y. et al. (2007). Palladin regulates cell and extracellular matrix interaction through maintaining normal actin cytoskeleton architecture and stabilizing beta1-integrin. J. Cell. Biochem. 100, 1288-1300.
31. Maeda, M., Asano, E., Ito, D., Ito, S., Hasegawa, Y., Hamaguchi, M. and Senga, T. (2009). Characterization of interaction between CLP36 and palladin. FEBS J. 276, 2775-2785.
32. Millán, J., Cain, R. J., Reglero-Real, N., Bigarella, C., Marcos-Ramiro, B., Fernández-Marti{dotless}́n, L., Correas, I. and Ridley, A. J. (2010). Adherens junctions connect stress fibres between adjacent endothelial cells. BMC Biol. 8, 11.
33. Mykkänen, O.-M., Grönholm, M., Rönty, M., Lalowski, M., Salmikangas, P., Suila, H. and Carpén, O. (2001). Characterization of human palladin, a microfilament-associated protein. Mol. Biol. Cell 12, 3060-3073.
34. Oakes, P. W., Beckham, Y., Stricker, J. and Gardel, M. L. (2012). Tension is required but not sufficient for focal adhesion maturation without a stress fiber template. J. Cell Biol. 196, 363-374.
35. Otey, C. A., Rachlin, A., Moza, M., Arneman, D. and Carpen, O. (2005). The Palladin/Myotilin/Myopalladin family of actin-associated scaffolds. In International Review of Cytology (ed. W. J. Kwang), pp. 31-58. Academic Press.
36. Parast, M. M. and Otey, C. A. (2000). Characterization of palladin, a novel protein localized to stress fibers and cell adhesions. J. Cell Biol. 150, 643-656.
37. Pellegrin, S. and Mellor, H. (2007). Actin stress fibres. J. Cell Sci. 120, 3491-3499.
38. Petrie, R. J., Gavara, N., Chadwick, R. S. and Yamada, K. M. (2012). Nonpolarized signaling reveals two distinct modes of 3D cell migration. J. Cell Biol. 197, 439-455.
39. Pollard, T. D. and Cooper, J. A. (2009). Actin, a central player in cell shape and movement. Science 326, 1208-1212.
40. Rönty, M., Taivainen, A., Moza, M., Otey, C. A. and Carpén, O. (2004). Molecular analysis of the interaction between palladin and a-actinin. FEBS Lett. 566, 30-34.
41. Rönty, M. J., Leivonen, S.-K., Hinz, B., Rachlin, A., Otéy, C. A., Kähäri, V.-M. and Carpén, O. M. (2006). Isoform-specific regulation of the actin-organizing protein palladin during TGF-beta1-induced myofibroblast differentiation. J. Invest. Dermatol. 126, 2387-2396.
42. Rönty, M., Taivainen, A., Heiska, L., Otey, C., Ehler, E., Song, W. K. and Carpen, O. (2007). Palladin interacts with SH3 domains of SPIN90 and Src and is required for Src-induced cytoskeletal remodeling. Exp. Cell Res. 313, 2575-2585.
43. Sandbo, N. and Dulin, N. (2011). Actin cytoskeleton in myofibroblast differentiation: ultrastructure defining form and driving function. Transl. Res. 158, 181-196.
44. Sanger, J. W., Wang, J., Holloway, B., Du, A. and Sanger, J. M. (2009). Myofibrillogenesis in skeletal muscle cells in zebrafish. Cell Motil. Cytoskeleton 66, 556-566.
45. Sato, M. and Ohashi, T. (2005). Biorheological views of endothelial cell responses to mechanical stimuli. Biorheology 42, 421-441.
46. Schirenbeck, A., Arasada, R., Bretschneider, T., Stradal, T. E. B., Schleicher, M. and Faix, J. (2006). The bundling activity of vasodilator-stimulated phosphoprotein is required for filopodium formation. Proc. Natl. Acad. Sci. USA 103, 7694-7699.
47. Shemesh, T., Verkhovsky, A. B., Svitkina, T. M., Bershadsky, A. D. and Kozlov, M. M. (2009). Role of focal adhesions and mechanical stresses in the formation and progression of the lamellum interface [corrected]. Biophys. J. 97, 1254-1264.
48. Smith, M. A., Blankman, E., Gardel, M. L., Luettjohann, L., Waterman, C. M. and Beckerle, M. C. (2010). A zyxin-mediated mechanism for actin stress fiber maintenance and repair. Dev. Cell 19, 365-376.
49. Tojkander, S., Gateva, G., Schevzov, G., Hotulainen, P., Naumanen, P., Martin, C., Gunning, P. W. and Lappalainen, P. (2011). A molecular pathway for myosin II recruitment to stress fibers. Curr. Biol. 21, 539-550.
50. Tojkander, S., Gateva, G. and Lappalainen, P. (2012). Actin stress fibers - assembly, dynamics and biological roles. J. Cell Sci. 125, 1855-1864.
51. Wong, A. J., Pollard, T. D. and Herman, I. M. (1983). Actin filament stress fibers in vascular endothelial cells in vivo. Science 219, 867-869.
52. Yi, J., Wu, X. S., Crites, T. and Hammer, J. A., 3rd (2012). Actin retrograde flow and actomyosin II arc contraction drive receptor cluster dynamics at the immunological synapse in Jurkat T cells. Mol. Biol. Cell 23, 834-852.