MRNA encoding WAVE-Arp2/3-Associated proteins is co-localized with foci of active protein synthesis at the leading edge of MRC5 fibroblasts during cell migration

Biochemical Journal

Volumn 452, Issue 1, 2013, Pages 45-55

  Willett, Mark ^a   Brocard, Michele ^a   Pollard, Hilary J ^a   Morley, Simon J ^a  

^a UNIVERSITY OF SUSSEX   (United Kingdom)

Author keywords

Cell division cycle 42 (Cdc42); Focal adhesion; MRNA; Rac1; RhoA; Translation

Indexed keywords

ACTIN RELATED PROTEIN 2-3 COMPLEX; RAC1 PROTEIN; WISKOTT ALDRICH SYNDROME PROTEIN;

ARTICLE; CELL SPREADING; CONTROLLED STUDY; FIBROBLAST; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; RNA STRUCTURE;

ACTIN-RELATED PROTEIN 2-3 COMPLEX; CELL LINE, TRANSFORMED; CELL MOVEMENT; FIBROBLASTS; HUMANS; MOLECULAR DYNAMICS SIMULATION; PROTEIN BIOSYNTHESIS; RNA, MESSENGER; WISKOTT-ALDRICH SYNDROME PROTEIN FAMILY;

MAMMALIA;

EID: 84876902911     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20121803     Document Type: Article

References (57)

1. Kalluri, R. and Zeisberg, M. (2006) Fibroblasts in cancer. Nat. Rev. Cancer 6, 392-401
2. 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
3. Ridley, A. (2009) Roles of Rho GTPases in cell adhesion and migration. FEBS J. 276, 49-49
4. Abercrombie, M., Heaysman, J. E. and Pegrum, S. M. (1970) The locomotion of fibroblasts in culture. Exp. Cell Res. 62, 389-398
5. Pollard, T. D. and Borisy, G. G. (2003) Cellular motility driven by assembly and disassembly of actin filaments. Cell 112, 453-465
6. Bugyi, B. and Carlier, M. F. (2010) Control of actin filament treadmilling in cell motility. Annu. Rev. Biophys. 39, 449-470
7. Suraneni, P., Rubinstein, B., Unruh, J. R., Durnin, M., Hanein, D. and Li, R. (2012) The Arp2/3 complex is required for lamellipodia extension and directional fibroblast cell migration. J. Cell Biol. 197, 239-251
8. Eden, S., Rohatgi, R., Podtelejnikov, A. V., Mann, M. and Kirschner, M. W. (2002) Mechanism of regulation of WAVE1-induced actin nucleation by Rac1 and Nck. Nature 418, 790-793
9. Derivery, E. and Gautreau, A. (2010) Generation of branched actin networks: assembly and regulation of the N-WASP and WAVE molecular machines. BioEssays 32, 119-131
10. Rodal, A. A., Sokolova, O., Robins, D. B., Daugherty, K. M., Hippenmeyer, S., Riezman, H., Grigorieff, N. and Goode, B. L. (2005) Conformational changes in the Arp2/3 complex leading to actin nucleation. Nat. Struct. Mol. Biol. 12, 26-31
11. Machesky, L. M., Mullins, R. D., Higgs, H. N., Kaiser, D. A., Blanchoin, L., May, R. C., Hall, M. E. and Pollard, T. D. (1999) Scar, a WASP-related protein, activates nucleation of actin filaments by the Arp2/3 complex. Proc. Natl. Acad. Sci. U.S.A. 96, 3739-3744
12. Pollitt, A. Y. and Insall, R. H. (2009) WASP and SCAR/WAVE proteins: the drivers of actin assembly. J. Cell Sci. 122, 2575-2578
13. 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
14. Martin, K. C. and Ephrussi, A. (2009) mRNA localization: gene expression in the spatial dimension. Cell 136, 719-730
15. Chao, J. A., Patskovsky, Y., Patel, V., Levy, M., Almo, S. C. and Singer, R. H. (2010) ZBP1 recognition of β-Actin zipcode induces RNA looping. Genes Dev. 24, 148-158
16. Oleynikov, Y. and Singer, R. H. (2003) Real-time visualization of ZBP1 association with β-Actin mRNA during transcription and localization. Curr. Biol. 13, 199-207
17. Eom, T., Antar, L. N., Singer, R. H. and Bassell, G. J. (2003) Localization of a β-Actin messenger ribonucleoprotein complex with zipcode-binding protein modulates the density of dendritic filopodia and filopodial synapses. J. Neurosci. 23, 10433-10444
18. Mingle, L. A., Okuhama, N. N., Shi, J., Singer, R. H., Condeelis, J. and Liu, G. (2005) Localization of all seven messenger RNAs for the actin-polymerization nucleator Arp2/3 complex in the protrusions of fibroblasts. J. Cell Sci. 118, 2425-2433
19. Sonenberg, N. and Hinnebusch, A. G. (2009) Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 136, 731-745
20. Morley, S. J., Coldwell, M. J. and Clemens, M. J. (2005) Initiation factor modifications in the preapoptotic phase. Cell Death Differ. 12, 571-584
21. Proud, C. G. (2011) mTOR signalling in health and disease. Biochem. Soc. Trans. 39, 431-436
22. Jackson, R. J., Hellen, C. U. T. and Pestova, T. V. (2010) The mechanism of eukaryotic translation initiation and principles of its regulation. Nat. Rev. Mol. Cell Biol. 11, 113-127
23. Laplante, M. and Sabatini, D. M. (2012) mTOR signaling in growth control and disease. Cell 149, 274-293
24. Ma, X. M. and Blenis, J. (2009) Molecular mechanisms of mTOR-mediated translational control. Mol. Cell. Biol. 10, 307-318
25. Sakakibara, K., Liu, B., Hollenbeck, S. and Kent, K. C. (2005) Rapamycin inhibits fibronectin-induced migration of the human arterial smooth muscle line (E47) through the mammalian target of rapamycin. Am. J. Physiol. Heart Circ. Physiol. 288, H2861- H2868
26. Liu, L. and Parent, C. A. (2011) Review series: TOR kinase complexes and cell migration. J. Cell Biol. 194, 815-824
27. Willett, M., Brocard, M., Davide, A. and Morley, S. J. (2011) Translation initiation factors and active sites of protein synthesis co-localize at the leading edge of migrating fibroblasts. Biochem. J. 438, 217-227
28. Willett, M., Pollard, H. J., Vlasak, M. and Morley, S. J. (2009) Localisation of translation initiation factors to talin/β3-integrin- enriched adhesion complexes in spreading and migrating mammalian cells. Biol. Cell 102, 265-276
29. Cowan, J. L. and Morley, S. J. (2004) The proteasome inhibitor, MG132, promotes the reprogramming of translation in C2C12 myoblasts and facilitates the association of hsp25 with the eIF4F complex. Eur. J. Biochem. 271, 3596-3611
30. Chaumeil, J., Okamoto, I. and Heard, E. (2004) X-chromosome inactivation in mouse embryonic stem cells: analysis of histone modifications and transcriptional activity using immunofluorescence and FISH. Methods Enzymol. 376, 405-419
31. Li, L., Okura, M. and Imamoto, A. (2002) Focal adhesions require catalytic activity of Src family kinases to mediate integrin-matrix adhesion. Mol. Cell. Biol. 22, 1203-1217
32. Jasaitis, A., Estevez, M., Heysch, J., Ladoux, B. and Dufour, S. (2012) E-cadherindependent stimulation of traction force at focal adhesions via the Src and PI3K signaling pathways. Biophys. J. 103, 175-184
33. Thoreen, C. C. and Sabatini, D. M. (2009) Rapamycin inhibits mTORC1, but not completely. Autophagy 5, 725-726
34. Willett, M., Cowan, J. L., Vlasak, M., Coldwell, M. J. and Morley, S. J. (2009) Inhibition of mammalian target of rapamycin (mTOR) signalling in C2C12 myoblasts prevents myogenic differentiation without affecting the hyperphosphorylation of 4E-BP1. Cell. Signalling 21, 1504-1512
35. Kim, J. E. and Chen, J. (2000) Cytoplasmic-nuclear shuttling of FKBP12-rapamycinassociated protein is involved in rapamycin-sensitive signaling and translation initiation. Proc. Natl. Acad. Sci. U.S.A. 97, 14340-14345
36. Ballou, L. M. and Lin, R. Z. (2008) Rapamycin and mTOR kinase inhibitors. J. Chem. Biol. 1, 27-36
37. Garcia-Martinez, J. M., Moran, J., Clarke, R. G., Gray, A., Cosulich, S. C., Chresta, C. M. and Alessi, D. R. (2009) Ku-0063794 is a specific inhibitor of the mammalian target of rapamycin (mTOR). Biochem. J. 421, 29-42
38. Chao, W. T., Daquinag, A. C., Ashcroft, F. and Kunz, J. (2010) Type I PIPK-α regulates directed cell migration by modulating Rac1 plasma membrane targeting and activation. J. Cell Biol. 190, 247-262
39. Abou-Kheir, W., Isaac, B., Yamaguchi, H. and Cox, D. (2008) Membrane targeting of WAVE2 is not sufficient for WAVE2-dependent actin polymerization: a role for IRSp53 in mediating the interaction between Rac and WAVE2. J. Cell Sci. 121, 379-390
40. Suetsugu, S., Kurisu, S., Oikawa, T., Yamazaki, D., Oda, A. and Takenawa, T. (2006) Optimization of WAVE2 complex-induced actin polymerization by membrane-bound IRSp53, PIP(3), and Rac. J. Cell Biol. 173, 571-585
41. Gautreau, A., Ho, H. Y., Li, J., Steen, H., Gygi, S. P. and Kirschner, M. W. (2004) Purification and architecture of the ubiquitous Wave complex. Proc. Natl. Acad. Sci. U.S.A. 101, 4379-4383
42. Derivery, E., Fink, J., Martin, D., Houdusse, A., Piel, M., Stradal, T. E., Louvard, D. and Gautreau, A. (2008) Free Brick1 is a trimeric precursor in the assembly of a functional wave complex. PLoS ONE 3, e2462
43. Goley, E. D. and Welch, M. D. (2006) The ARP2/3 complex: an actin nucleator comes of age. Nat. Rev. Mol. Cell Biol. 7, 713-726
44. Mullins, R. D., Heuser, J. A. and Pollard, T. D. (1998) The interaction of Arp2/3 complex with actin: nucleation, high affinity pointed end capping, and formation of branching networks of filaments. Proc. Natl. Acad. Sci. U.S.A. 95, 6181-6186
45. Chen, Z., Borek, D., Padrick, S. B., Gomez, T. S., Metlagel, Z., Ismail, A. M., Umetani, J., Billadeau, D. D., Otwinowsk, Z. and Rosen, M. K. (2010) Structure and regulation of the actin regulatory WAVE complex. Nature 468, 533-538
46. Kotula, L. (2012) Abi1, a critical molecule coordinating actin cytoskeleton reorganization with PI-3 kinase and growth signaling. FEBS J. 586, 2790-2794
47. Ismail, A. M., Padrick, S. B., Chen, B., Umetani, J. and Rosen, M. K. (2009) The WAVE regulatory complex is inhibited. Nat. Struct. Mol. Biol. 16, 561-563
48. Kunda, P., Craig, G., Dominguez, V. and Baum, B. (2003) Abi, Sra1, and Kette control the stability and localization of SCAR/WAVE to regulate the formation of actin-based protrusions. Curr. Biol. 13, 1867-1875
49. Pils, S., Kopp, K., Peterson, L., Delgado Tascon, J., Nyffenegger-Jann, N. J. and Hauck, C. R. (2012) The adaptor molecule Nck localizes the WAVE complex to promote actin polymerization during CEACAM3-mediated phagocytosis of bacteria. PLoS ONE 7, e32808
50. Gu, W., Katz, Z., Wu, B., Park, H. Y., Li, D., Lin, S., Wells, A. L. and Singer, R. H. (2012) Regulation of local expression of cell adhesion and motility-related mRNAs in breast cancer cells by IMP1/ZBP1. J. Cell Sci. 125, 81-91
51. Aslan, J. E. and McCarty, O. J. (2012) Regulation of the mTOR-Rac1 axis in platelet function. Small GTPases 3, 67-70
52. Castets, M., Schaeffer, C., Bechara, E., Schenck, A., Khandjian, E. W., Luche, S., Moine, H., Rabilloud, T., Mandel, J. L. and Bardoni, B. (2005) FMRP interferes with the Rac1 pathway and controls actin cytoskeleton dynamics in murine fibroblasts. Hum. Mol. Genet. 14, 835-844
53. Komar, A. A. and Hatzoglou, M. (2011) Cellular IRES-mediated translation: the war of ITAFs in pathophysiological states. Cell Cycle 10, 229-240
54. Morley, S. J. and Willett, M. (2008) Signaling pathways open the GAITway to translational control. Dev. Cell 15, 639-640
55. Morley, S. J. and Willett, M. (2009) Kinky binding and SECsy insertions. Mol. Cell 35, 396-398
56. Bubenik, J. L., Ladd, A. N., Gerber, C. A., Budiman, M. E. and Driscoll, D. M. (2009) Known turnover and translation regulatory RNA-binding proteins interact with the 3- UTR of SECIS-binding protein 2. RNA 6, 73-83
57. Napoli, I., Mercaldo, V., Boyl, P. P., Eleuteri, B., Zalfa, F., De Rubeis, S., Di Marino, D., Mohr, E., Massimi, M., Falconi, M. et al. (2008) The fragile X syndrome protein represses activity-dependent translation through CYFIP1, a new 4E-BP. Cell 134, 1042-1054