Phosphorylation facilitates the integrin binding of filamin under force

Biophysical Journal

Volumn 97, Issue 12, 2009, Pages 3095-3104

  Chen, Harvey S ^a   Kolahi, Kevin S ^a   Mofrad, Mohammad R K ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 73449113921     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2009.08.059     Document Type: Article

References (49)

1. Feng, Y., and C. A. Walsh. 2004. The many faces of filamin: a versatile molecular scaffold for cell motility and signaling. Nat. Cell Biol. 6:1034-1038.
2. Popowicz, G., M. Schleicher, A. Noegel, and T. Holak. 2006. Filamins: promiscuous organizers of the cytoskeleton. Trends Biochem. Sci. 31:411-419.
3. Ingber, D. E. 2006. Cellular mechanotransduction: putting all the pieces together again. FASEB J. 20:811-827.
4. Janmey, P. A., and C. McCulloch. 2007. Cell mechanics: integrating cell responses to mechanical stimuli. Annu. Rev. Biomed. Eng. 9:1-34.
5. Kaazempur Mofrad, M. R., N. A. Abdul-Rahim, H. Karcher, P. J. Mack, B. Yap, et al. 2005. Exploring the molecular basis for mechanosensation, signal transduction, and cytoskeletal remodeling. Acta Biomater. 1:281-293.
6. Mofrad, M. R. K., and R. D. Kamm. 2009. Cellular Mechanotransduction. Cambridge University Press, New York.
7. Stossel, T. P., J. Condeelis, L. Cooley, J. H. Hartwig, A. Noegel, et al. 2001. Filamins as integrators of cell mechanics and signaling. Nat. Rev. Mol. Cell Biol. 2:138-145.
8. Campbell, I. 2008. Studies of focal adhesion assembly. Biochem. Soc. Trans. 36:263-266.
9. Pudas, R., T. R. Kiema, P. J. Butler, M. Stewart, and J. Ylänne. 2005. Structural basis for vertebrate filamin dimerization. Structure. 13:111-119.
10. Uribe, R., and D. Jay. 2009. A review of actin binding proteins: new perspectives. Mol. Biol. Rep. 36:121-125.
11. van der Flier, A., and A. Sonnenberg. 2001. Structural and functional aspects of filamins. Biochim. Biophys. Acta. 1538:99-117.
12. Fox, J. W., E. D. Lamperti, Y. Z. Ekşioǧlu, S. E. Hong, Y. Feng, et al. 1998. Mutations in filamin 1 prevent migration of cerebral cortical neurons in human periventricular heterotopia. Neuron. 21:1315-1325.
13. Kyndt, F., J. P. Gueffet, V. Probst, P. Jaafar, A. Legendre, et al. 2007. Mutations in the gene encoding filamin A as a cause for familial cardiac valvular dystrophy. Circulation. 115:40-49.
14. Lad, Y., T. Kiema, P. Jiang, O. Pentikäinen, C. Coles, et al. 2007. Structure of three tandem filamin domains reveals auto-inhibition of ligand binding. EMBO J. 26:3993-4004.
15. Gorlin, J. B., R. Yamin, S. Egan, M. Stewart, T. P. Stossel, et al. 1990. Human endothelial actin-binding protein (ABP-280, nonmuscle filamin): a molecular leaf spring. J. Cell Biol. 111:1089-1105.
16. Nakamura, F., T. Osborn, C. Hartemink, J. Hartwig, and T. Stossel. 2007. Structural basis of filamin A functions. J. Cell Biol. 179:1011-1025.
17. Hartwig, J. H., and T. P. Stossel. 1981. Structure of macrophage actin-binding protein molecules in solution and interacting with actin filaments. J. Mol. Biol. 145:563-581.
18. Sutoh, K., M. Iwane, F. Matsuzaki, M. Kikuchi, and A. Ikai. 1984. Isolation and characterization of a high molecular weight actin-binding protein from Physarum polycephalum plasmodia. J. Cell Biol. 98:1611-1618.
19. Jay, D., E. J. García, J. E. Lara, M. A. Medina, and M. de la Luz Ibarra. 2000. Determination of a cAMP-dependent protein kinase phosphorylation site in the C-terminal region of human endothelial actin-binding protein. Arch. Biochem. Biophys. 377:80-84.
20. Vadlamudi, R. K., F. Li, L. Adam, D. Nguyen, Y. Ohta, et al. 2002. Filamin is essential in actin cytoskeletal assembly mediated by p21-activated kinase 1. Nat. Cell Biol. 4:681-690.
21. Woo, M. S., Y. Ohta, I. Rabinovitz, T. P. Stossel, and J. Blenis. 2004. Ribosomal S6 kinase (RSK) regulates phosphorylation of filamin A on an important regulatory site. Mol. Cell. Biol. 24:3025-3035.
22. Kim, H., A. Sengupta, M. Glogauer, and C. Mcculloch. 2008. Filamin A regulates cell spreading and survival via β1 integrins. Exp. Cell Res. 314:834-846.
23. Shifrin, Y., P. D. Arora, Y. Ohta, D. A. Calderwood, and C. A. McCulloch. 2009. The role of FilGAP-filamin A interactions in mechanoprotection. Mol. Biol. Cell. 20:1269-1279.
24. Glogauer, M., P. Arora, D. Chou, P. A. Janmey, G. P. Downey, et al. 1998. The role of actin-binding protein 280 in integrin-dependent mechanoprotection. J. Biol. Chem. 273:1689-1698.
25. Lee, S. E., S. Chunsrivirot, R. D. Kamm, and M. R. Mofrad. 2008. Molecular dynamics study of talin-vinculin binding. Biophys. J. 95:2027-2036.
26. Kiema, T., Y. Lad, P. Jiang, C. L. Oxley, M. Baldassarre, et al. 2006. The molecular basis of filamin binding to integrins and competition with talin. Mol. Cell. 21:337-347.
27. Calderwood, D. A., A. Huttenlocher, W. B. Kiosses, D. M. Rose, D. G. Woodside, et al. 2001. Increased filamin binding to beta-integrin cytoplasmic domains inhibits cell migration. Nat. Cell Biol. 3:1060-1068.
28. Golji, J., R. Collins, and M. R. Mofrad. 2009. Molecular mechanics of the alpha-actinin rod domain: bending, torsional, and extensional behavior. PLOS Comput. Biol. 5:e1000389.
29. Linke, W. A., and A. Grützner. 2008. Pulling single molecules of titin by AFM - recent advances and physiological implications. Pflugers Arch. 456:101-115.
30. van der Flier, A., I. Kuikman, D. Kramer, D. Geerts, M. Kreft, et al. 2002. Different splice variants of filamin-B affect myogenesis, subcellular distribution, and determine binding to integrin [beta] subunits. J. Cell Biol. 156:361-376.
31. Humphrey, W., A. Dalke, and K. Schulten. 1996. VMD: visual molecular dynamics. J. Mol. Graph. 14:33-38, 27-38.
32. Peitsch, M. C. 1996. ProMod and Swiss-Model: Internet-based tools for automated comparative protein modelling. Biochem. Soc. Trans. 24:274-279.
33. Peitsch, M. C., T. Schwede, and N. Guex. 2000. Automated protein modeling - the proteome in 3D. Pharmacogenomics. 1:257-266.
34. Schwede, T., J. Kopp, N. Guex, and M. C. Peitsch. 2003. SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res. 31:3381-3385.
35. Brooks, B., and M. Karplus. 1983. Harmonic dynamics of proteins: normal modes and fluctuations in bovine pancreatic trypsin inhibitor. Proc. Natl. Acad. Sci. USA. 80:6571-6575.
36. MacKerell, A. D., M. S. Sommer, and M. Karplus. 1995. pH dependence of binding reactions from free energy simulations and macroscopic continuum electrostatic calculations: application to 2′GMP/3′GMP binding to ribonuclease T1 and implications for catalysis. J. Mol. Biol. 247:774-807.
37. Kolahi, K. S., and M. R. Mofrad. 2008. Molecular mechanics of filamin's rod domain. Biophys. J. 94:1075-1083.
38. Schaefer, M., H. W. van Vlijmen, and M. Karplus. 1998. Electrostatic contributions to molecular free energies in solution. Adv. Protein Chem. 51:1-57.
39. Chen, J., C. L. Brooks, and J. Khandogin. 2008. Recent advances in implicit solvent-based methods for biomolecular simulations. Curr. Opin. Struct. Biol. 18:140-148.
40. Phillips, J. C., R. Braun, W. Wang, J. Gumbart, E. Tajkhorshid, et al. 2005. Scalable molecular dynamics with NAMD. J. Comput. Chem. 26:1781-1802.
41. Raiteri, P., A. Laio, and M. Parrinello. 2004. Correlations among hydrogen bonds in liquid water. Phys. Rev. Lett. 93:087801.
42. Travis, M. A., A. van der Flier, R. A. Kammerer, A. P. Mould, A. Sonnenberg, et al. 2004. Interaction of filamin A with the integrin beta 7 cytoplasmic domain: role of alternative splicing and phosphorylation. FEBS Lett. 569:185-190.
43. Freddolino, P. L., F. Liu, M. Gruebele, and K. Schulten. 2008. Ten-microsecond molecular dynamics simulation of a fast-folding WW domain. Biophys. J. 94:L75-L77.
44. Schwaiger, I., A. Kardinal, M. Schleicher, A. A. Noegel, and M. Rief. 2004. A mechanical unfolding intermediate in an actin-crosslinking protein. Nat. Struct. Mol. Biol. 11:81-85.
45. Schwaiger, I., M. Schleicher, A. A. Noegel, and M. Rief. 2005. The folding pathway of a fast-folding immunoglobulin domain revealed by single-molecule mechanical experiments. EMBO Rep. 6:46-51.
46. Monticelli, L., E. J. Sorin, D. P. Tieleman, and V. S. Pande. 2008. Molecular simulation of multistate peptide dynamics: a comparison between microsecond timescale. J. Comput. Chem. 29:1740-1752.
47. Heikkinen, O. K., S. Ruskamo, P. V. Konarev, D. I. Svergun, T. Iivanainen, et al. 2009. Atomic structures of two novel immunoglobulin-like domain-pairs in the actin cross-linking protein filamin. Biol. Chem. 284:25450-25458.
48. Bershadsky, A. D., N. Q. Balaban, and B. Geiger. 2003. Adhesion-dependent cell mechanosensitivity. Annu. Rev. Cell Dev. Biol. 19:677-695.
49. Nicolas, A., B. Geiger, and S. A. Safran. 2004. Cell mechanosensitivity controls the anisotropy of focal adhesions. Proc. Natl. Acad. Sci. USA. 101:12520-12525.