Documentation and localization of force-mediated filamin A domain perturbations in moving cells

Nature Communications

Volumn 5, Issue , 2014, Pages

  Nakamura, Fumihiko ^a   Song, Mia ^a   Hartwig, John H ^a   Stossel, Thomas P ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FILAMIN A; ACTIN; FILAMIN;

CYTOLOGY; PHOTOCHEMISTRY; PROTEIN; SIGNAL;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; BINDING SITE; CELL CULTURE; CELL MOTION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DOCUMENTATION; DYNAMICS; FLUORESCENCE RESONANCE ENERGY TRANSFER; IN VITRO STUDY; INSECT CELL; INTRACELLULAR SIGNALING; MECHANOTRANSDUCTION; NONHUMAN; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN CROSS LINKING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN UNFOLDING; ANIMAL; BIOMECHANICS; CHEMISTRY; CHLOROCEBUS AETHIOPS; COS CELL LINE; CYTOLOGY; KIDNEY; OPTICS; PHYSIOLOGY; PROCEDURES;

ACTINS; ANIMALS; BIOMECHANICAL PHENOMENA; CELL MOVEMENT; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; COS CELLS; FILAMINS; FLUORESCENCE RESONANCE ENERGY TRANSFER; IN VITRO TECHNIQUES; KIDNEY; MECHANOTRANSDUCTION, CELLULAR; OPTICS AND PHOTONICS;

EID: 84907348365     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms5656     Document Type: Article

References (60)

1. Brown, A. E. &Discher, D. E. Conformational changes and signaling in cell and matrix physics. Curr. Biol. 19, R781-R789 (2009).
2. Moore, S. W., Roca-Cusachs, P. &Sheetz, M. P. Stretchy proteins on stretchy substrates: the important elements of integrin-mediated rigidity sensing. Dev. Cell 19, 194-206 (2010).
3. Schwartz, M. A. Integrins and extracellular matrix in mechanotransduction. Cold Spring Harb. Perspect. Biol. 2, a005066 (2010).
4. Heisenberg, C. P. &Bellaiche, Y. Forces in tissue morphogenesis and patterning. Cell 153, 948-962 (2013).
5. Guillot, C. &Lecuit, T. Mechanics of epithelial tissue homeostasis and morphogenesis. Science 340, 1185-1189 (2013).
6. Grashoff, C. et al. Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics. Nature 466, 263-266 (2010).
7. Kyndt, F. et al. Mutations in the gene encoding filamin A as a cause for familial cardiac valvular dystrophy. Circulation 115, 40-49 (2007). (Pubitemid 46058610)
8. Ehrlicher, A. J., Nakamura, F., Hartwig, J. H., Weitz, D. A. &Stossel, T. P. Mechanical strain in actin networks regulates FilGAP and integrin binding to filamin A. Nature 478, 260-263 (2011).
9. Razinia, Z., Makela, T., Ylanne, J. &Calderwood, D. A. Filamins in mechanosensing and signaling. Annu. Rev. Biophys. 41, 227-246 (2012).
10. Kainulainen, T. et al. Cell death and mechanoprotection by filamin a in connective tissues after challenge by applied tensile forces. J. Biol. Chem. 277, 21998-22009 (2002). (Pubitemid 34952354)
11. Sharif-Naeini, R. et al. Polycystin-1 and-2 dosage regulates pressure sensing. Cell 139, 587-596 (2009).
12. Luo, W. et al. Analysis of the local organization and dynamics of cellular actin networks. J. Cell Biol. 202, 1057-1073 (2013).
13. Stossel, T. P. et al. Filamins as integrators of cell mechanics and signalling. Nat. Rev. Mol. Cell Biol. 2, 138-145 (2001). (Pubitemid 33674042)
14. Gorlin, J. B. et al. Human endothelial actin-binding protein (ABP-280, nonmuscle filamin): a molecular leaf spring. J. Cell Biol. 111, 1089-1105 (1990).
15. Nakamura, F., Stossel, T. P. &Hartwig, J. H. The filamins: Organizers of cell structure and function. Cell Adh. Migr. 5, 160-169 (2011).
16. Nakamura, F., Osborn, T. M., Hartemink, C. A., Hartwig, J. H. &Stossel, T. P. Structural basis of filamin A functions. J. Cell Biol. 179, 1011-1025 (2007). (Pubitemid 350223495)
17. Lad, Y. et al. Structure of three tandem filamin domains reveals auto-inhibition of ligand binding. EMBO J. 26, 3993-4004 (2007). (Pubitemid 47367495)
18. Heikkinen, O. K. et al. Atomic structures of two novel immunoglobulin-like domain pairs in the actin cross-linking protein filamin. J. Biol. Chem. 284, 25450-25458 (2009).
19. Ruskamo, S. et al. The C-terminal rod 2 fragment of filamin A forms a compact structure that can be extended. Biochem. J. 446, 261-269 (2012).
20. Tossavainen, H. et al. Model of a six immunoglobulin-like domain fragment of filamin A (16-21) built using residual dipolar couplings. J. Am. Chem. Soc. 134, 6660-6672 (2012).
21. Rognoni, L., Stigler, J., Pelz, B., Ylanne, J. &Rief, M. Dynamic force sensing of filamin revealed in single-molecule experiments. Proc. Natl Acad. Sci. USA 109, 19679-19684 (2012).
22. Ganesan, S., Ameer-Beg, S. M., Ng, T. T., Vojnovic, B. &Wouters, F. S. A dark yellow fluorescent protein (YFP)-based Resonance Energy-Accepting Chromoprotein (REACh) for Forster resonance energy transfer with GFP. Proc. Natl Acad. Sci. USA 103, 4089-4094 (2006).
23. Murakoshi, H., Lee, S. J. &Yasuda, R. Highly sensitive and quantitative FRETFLIM imaging in single dendritic spines using improved non-radiative YFP. Brain Cell Biol. 36, 31-42 (2008).
24. Wang, Y., Shyy, J. Y. &Chien, S. Fluorescence proteins, live-cell imaging, and mechanobiology: seeing is believing. Annu. Rev. Biomed. Eng. 10, 1-38 (2008).
25. Mochizuki, N. et al. Spatio-temporal images of growth-factor-induced activation of Ras and Rap1. Nature 411, 1065-1068 (2001). (Pubitemid 32612332)
26. Wang, Y. et al. Visualizing the mechanical activation of Src. Nature 434, 1040-1045 (2005). (Pubitemid 40586054)
27. Koenderink, G. H. et al. An active biopolymer network controlled by molecular motors. Proc. Natl Acad. Sci. USA 106, 15192-15197 (2009).
28. Bond, L. M., Tumbarello, D. A., Kendrick-Jones, J. &Buss, F. Small-molecule inhibitors of myosin proteins. Future Med. Chem. 5, 41-52 (2013).
29. Dantzig, J. A., Walker, J. W., Trentham, D. R. &Goldman, Y. E. Relaxation of muscle fibers with adenosine 50-[gamma-thio]triphosphate (ATP[gamma S]) and by laser photolysis of caged ATP[gamma S]: evidence for Ca2dependent affinity of rapidly detaching zero-force cross-bridges. Proc. Natl Acad. Sci. USA 85, 6716-6720 (1988).
30. Ithychanda, S. S. et al. Identification and characterization of multiple similar ligand-binding repeats in filamin: implication on filamin-mediated receptor clustering and cross-talk. J. Biol. Chem. 284, 35113-35121 (2009).
31. Ylilauri, M. &Pentikainen, O. T. MMGBSA as a tool to understand the binding affinities of filamin-peptide interactions. J. Chem. Inf. Model. 53, 2626-2633 (2013).
32. Kaneider, N. C., Djanani, A., Fischer-Colbrie, R. &Wiedermann, C. J. Sphingosine kinase-dependent directional migration of leukocytes in response to phorbol ester. Biochem. Biophys. Res. Commun. 297, 806-810 (2002). (Pubitemid 35230322)
33. Sumagin, R., Robin, A. Z., Nusrat, A. &Parkos, C. A. Activation of PKCbetaII by PMA facilitates enhanced epithelial wound repair through increased cell spreading and migration. PLoS ONE 8, e55775 (2013).
34. Fukata, Y., Amano, M. &Kaibuchi, K. Rho-Rho-kinase pathway in smooth muscle contraction and cytoskeletal reorganization of non-muscle cells. Trends Pharmacol. Sci. 22, 32-39 (2001). (Pubitemid 32126284)
35. Uehata, M. et al. Calcium sensitization of smooth muscle mediated by a Rhoassociated protein kinase in hypertension. Nature 389, 990-994 (1997). (Pubitemid 27485693)
36. Ingber, D. E. Mechanobiology and diseases of mechanotransduction. Ann. Med. 35, 564-577 (2003). (Pubitemid 38005314)
37. Discher, D. et al. Biomechanics: cell research and applications for the next decade. Ann. Biomed. Eng. 37, 847-859 (2009).
38. Hoffman, B. D., Grashoff, C. &Schwartz, M. A. Dynamic molecular processes mediate cellular mechanotransduction. Nature 475, 316-323 (2011).
39. Janmey, P. A., Wells, R. G., Assoian, R. K. &McCulloch, C. A. From tissue mechanics to transcription factors. Differentiation 86, 112-120 (2013).
40. Wang, Y. &Wang, N. FRET and mechanobiology. Integr. Biol. 1, 565-573 (2009).
41. del Rio, A. et al. Stretching single talin rod molecules activates vinculin binding. Science 323, 638-641 (2009).
42. Yonemura, S., Wada, Y., Watanabe, T., Nagafuchi, A. &Shibata, M. alpha-Catenin as a tension transducer that induces adherens junction development. Nat. Cell Biol. 12, 533-542 (2010).
43. Borghi, N. et al. E-cadherin is under constitutive actomyosin-generated tension that is increased at cell-cell contacts upon externally applied stretch. Proc. Natl Acad. Sci. USA 109, 12568-12573 (2012).
44. Meng, F., Suchyna, T. M. &Sachs, F. A fluorescence energy transfer-based mechanical stress sensor for specific proteins in situ. FEBS J. 275, 3072-3087 (2008). (Pubitemid 351743583)
45. Meng, F., Suchyna, T. M., Lazakovitch, E., Gronostajski, R. M. &Sachs, F. Real time FRET based detection of mechanical stress in cytoskeletal and extracellular matrix proteins. Cell. Mol. Bioeng. 4, 148-159 (2011).
46. Suphamungmee, W., Nakamura, F., Hartwig, J. H. &Lehman, W. Electron microscopy and 3D reconstruction reveals filamin Ig domain binding to F-actin. J. Mol. Biol. 424, 248-256 (2012).
47. Chen, H. et al. Differential mechanical stability of filamin A rod segments. Biophys. J. 101, 1231-1237 (2011).
48. Chen, H. et al. Mechanical perturbation of filamin A immunoglobulin repeats 20-21 reveals potential non-equilibrium mechanochemical partner binding function. Sci. Rep. 3, 1642 (2013).
49. Kiema, T. et al. The molecular basis of filamin binding to integrins and competition with talin. Mol. Cell 21, 337-347 (2006). (Pubitemid 43163529)
50. Das, M., Ithychanda, S. S., Qin, J. &Plow, E. F. Migfilin and filamin as regulators of integrin activation in endothelial cells and neutrophils. PLoS ONE 6, e26355 (2011).
51. Tu, Y., Wu, S., Shi, X., Chen, K. &Wu, C. Migfilin and Mig-2 link focal adhesions to filamin and the actin cytoskeleton and function in cell shape modulation. Cell 113, 37-47 (2003). (Pubitemid 36411958)
52. Takafuta, T., Saeki, M., Fujimoto, T. T., Fujimura, K. &Shapiro, S. S. A new member of the LIM protein family binds to filamin B and localizes at stress fibers. J. Biol. Chem. 278, 12175-12181 (2003). (Pubitemid 36800197)
53. Gardel, M. L. et al. Prestressed F-actin networks cross-linked by hinged filamins replicate mechanical properties of cells. Proc. Natl Acad. Sci. USA 103, 1762-1767 (2006). (Pubitemid 43228767)
54. Burridge, K. &Wittchen, E. S. The tension mounts: stress fibers as forcegenerating mechanotransducers. J. Cell Biol. 200, 9-19 (2013).
55. Hartwig, J. H. &Stossel, T. P. Structure of macrophage actin-binding protein molecules in solution and interacting with actin filaments. J. Mol. Biol. 145, 563-581 (1981). (Pubitemid 11143904)
56. Oster, G. Biophysics of the leading lamella. Cell Motil. Cytoskeleton 10, 164-171 (1988).
57. Pufall, M. A. &Graves, B. J. Autoinhibitory domains: modular effectors of cellular regulation. Annu. Rev. Cell Dev. Biol. 18, 421-462 (2002). (Pubitemid 35387357)
58. Nakamura, F. et al. Molecular basis of filamin A-FilGAP interaction and its impairment in congenital disorders associated with filamin A mutations. PLoS ONE 4, e4928 (2009).
59. Nakamura, F., Osborn, E., Janmey, P. A. &Stossel, T. P. Comparison of filamin A-induced cross-linking and Arp2/3 complex-mediated branching on the mechanics of actin filaments. J. Biol. Chem. 277, 9148-9154 (2002). (Pubitemid 34952992)
60. Kardash, E., Bandemer, J. &Raz, E. Imaging protein activity in live embryos using fluorescence resonance energy transfer biosensors. Nat. Protoc. 6, 1835-1846 (2011).