Molecular mechanisms of cellular mechanosensing

Nature Materials

Volumn 12, Issue 11, 2013, Pages 1064-1071

  Luo, Tianzhi ^a   Mohan, Krithika ^b   Iglesias, Pablo A ^b   Robinson, Douglas N ^a,b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Johns Hopkins University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CONTRACTION; CORTICAL CYTOSKELETON; CYTOSKELETAL PROTEINS; INHIBITORY EFFECT; MECHANICAL LOADS; MOLECULAR MECHANISM; MULTI-SCALE MODELLING; PROTEIN ACCUMULATION;

CELLS; CYTOLOGY;

PROTEINS;

MYOSIN II; PROTOZOAL PROTEIN;

ARTICLE; BIOMECHANICS; CYTOLOGY; CYTOSKELETON; DICTYOSTELIUM; MECHANICS; METABOLISM;

BIOMECHANICAL PHENOMENA; CYTOSKELETON; DICTYOSTELIUM; MECHANICAL PROCESSES; MYOSIN TYPE II; PROTOZOAN PROTEINS;

EID: 84886286196     PISSN: 14761122     EISSN: 14764660     Source Type: Journal    
DOI: 10.1038/nmat3772     Document Type: Article

References (54)

1. LeDuc, P. R. & Robinson, D. N. Using lessons from cellular and molecular structures for future materials. Adv. Mater. 19, 3761-3770 (2007).
2. Grashoff, C. et al. Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics. Nature 466, 263-266 (2010).
3. Geiger, B., Spatz, J. P. & Bershadsky, A. D. Environmental sensing through focal adhesions. Nature Rev. Mol. Cell Biol. 10, 21-33 (2009).
4. Tamada, M., Sheetz, M. P. & Sawada, Y. Activation of signaling cascade by cytoskeleton stretch. Dev. Cell 7, 709-718 (2004).
5. Chowdhury, F. et al. Material properties of the cell dictate stress-induced spreading and differentiation in embryonic stem cells. Nature Mater. 9, 82-88 (2010).
6. 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).
7. Effler, J. C. et al. Mitosis-specific mechanosensing and contractile protein redistribution control cell shape. Curr. Biol. 16, 1962-1967 (2006).
8. Kee, Y-S. et al. A mechanosensory system governs myosin II accumulation in dividing cells. Mol. Biol. Cell 23, 1510-1523 (2012).
9. Johnson, C. P., Tang, H-Y., Carag, C., Speicher, D. W. & Discher, D. E. Forced unfolding of proteins within cells. Science 317, 663-666 (2007).
10. DuFort, C. C., Paszek, M. J. & Weaver, V. M. Balancing forces: Architectural control of mechanotransduction. Nature Rev. Mol. Cell Biol. 12, 308-319 (2011).
11. Engler, A. J., Sen, S., Sweeney, H. L. & Discher, D. E. Matrix elasticity directs stem cell lineage specification. Cell 126, 677-689 (2006).
12. Raab, M. et al. Crawling from soft to stiff matrix polarizes the cytoskeleton and phosphoregulates myosin-II heavy chain. J. Cell Biol. 199, 669-683 (2012).
13. Köhler, S., Schaller, V. & Bausch, A. R. Structure formation in active networks. Nature Mater. 10, 462-468 (2011).
14. Del Rio, A. et al. Stretching single talin rod molecules activates vinculin binding. Science 323, 638-641 (2009).
15. Gardel, M. L. et al. Elastic behavior of cross-linked and bundled actin networks. Science 304, 1301-1305 (2004).
16. Shin, J. H., Gardel, M. L., Mahadevan, L., Matsudaira, P. & Weitz, D. A. Relating microstructure to rheology of a bundled and cross-linked F-actin network in vitro. Proc. Natl Acad. Sci. USA 101, 9636-9641 (2004).
17. Chaudhuri, O., Parekh, S. H. & Fletcher, D. A. Reversible stress softening of actin networks. Nature 445, 295-298 (2007).
18. Koenderink, G. H. et al. An active biopolymer network controlled by molecular motors. Proc. Natl Acad. Sci. USA 106, 15192-15197 (2009).
19. Wagner, B., Tharmann, R., Haase, I., Fischer, M. & Bausch, A. R. Cytoskeletal polymer networks: The molecular structure of cross-linkers determines macroscopic properties. Proc. Natl Acad. Sci. USA 103, 13974-13978 (2006).
20. Schmoller, K. M., Lieleg, O. & Bausch, A. R. Cross-linking molecules modify composite actin networks independently. Phys. Rev. Lett. 101, 118102 (2008).
21. Murrell, M. et al. Spreading dynamics of biomimetic actin cortices. Biophys. J. 100, 1400-1409 (2011).
22. He, L., Wang, X., Tang, H. L. & Montell, D. J. Tissue elongation requires oscillating contractions of a basal actomyosin network. Nature Cell. Biol. 12, 1133-1142 (2010).
23. Solon, J., Kaya-Çopur, A., Colombelli, J. & Brunner, D. Pulsed forces timed by a ratchet-like mechanism drive directed tissue movement during dorsal closure. Cell 137, 1331-1342 (2009).
24. Bao, G. & Suresh, S. Cell and molecular mechanics of biological materials. Nature Mater. 2, 715-725 (2003).
25. Luo, T. et al. Understanding the cooperative interaction between myosin II and actin cross-linkers mediated by actin filaments during mechanosensation. Biophys. J. 102, 238-247 (2012).
26. Ren, Y. et al. Mechanosensing through cooperative interactions between myosin II and the actin crosslinker cortexillin I. Curr. Biol. 19, 1421-1428 (2009).
27. Uyeda, T. Q. P., Iwadate, Y., Umeki, N., Nagasaki, A. & Yumura, S. Stretching actin filaments within cells enhances their affinity for the myosin II motor domain. PLoS ONE 6, e26200 (2011).
28. Fernandez-Gonzalez, R., Simoes Sde, M., Roper, J. C., Eaton, S. & Zallen, J. A. Myosin II dynamics are regulated by tension in intercalating cells. Dev. Cell 17, 736-743 (2009).
29. Discher, D. E. & Mohandas, N. Kinematics of red cell aspiration by fluorescence-imaged microdeformation. Biophys. J. 71, 1680-1694 (1996).
30. Evans, E. Probing the relation between force-life-time-and chemistry in single molecular bonds. Annu. Rev. Biophys. Biomol. Struct. 30, 105-128 (2001).
31. Bell, G. I. Models for the specific adhesion of cells to cells. Science 200, 618-627 (1978).
32. Veigel, C., Molloy, J. E., Schmitz, S. & Kendrick-Jones, J. Load-dependent kinetics of force production by smooth muscle myosin measured with optical tweezers. Nature Cell Biol. 5, 980-986 (2003).
33. Thomas, W. E., Vogel, V. & Sokurenko, E. Biophysics of catch bonds. Annu. Rev. Biophys. 37, 399-416 (2008).
34. Uyeda, T. Q., Abramson, P. D. & Spudich, J. A. The neck region of the myosin motor domain acts as a lever arm to generate movement. Proc. Natl Acad. Sci. USA 93, 4459-4464 (1996).
35. Robinson, D. N., Kee, Y. S., Luo, T. & Surcel, A. in Comprehensive Biophysics (ed. Edward, H. E.) 48-72 (Elsevier, 2012).
36. Seifert, U. Rupture of multiple parallel molecular bonds under dynamic loading. Phys. Rev. Lett. 84, 2750-2753 (2000).
37. Erdmann, T. & Schwarz, U. S. Stability of adhesion clusters under constant force. Phys. Rev. Lett. 92, 108102 (2004).
38. Girard, K. D., Chaney, C., Delannoy, M., Kuo, S. C. & Robinson, D. N. Dynacortin contributes to cortical viscoelasticity and helps define the shape changes of cytokinesis. EMBO J. 23, 1536-1546 (2004).
39. Gerisch, G. et al. Mobile actin clusters and traveling waves in cells recovering from actin depolymerization. Biophys. J. 87, 3493-3503 (2004).
40. Robinson, D. N. & Spudich, J. A. Dynacortin, a genetic link between equatorial contractility and global shape control discovered by library complementation of a Dictyostelium discoideum cytokinesis mutant. J. Cell Biol. 150, 823-838 (2000).
41. 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).
42. Meyer, R. K. & Aebi, U. Bundling of actin filaments by alpha-actinin depends on its molecular length. J. Cell Biol. 110, 2013-2024 (1990).
43. Hock, R. S. & Condeelis, J. S. Isolation of a 240-kilodalton actin-binding protein from Dictyostelium discoideum. J. Biol. Chem. 262, 394-400 (1987).
44. Ferrer, J. M. et al. Measuring molecular rupture forces between single actin filaments and actin-binding proteins. Proc. Natl Acad. Sci. USA 105, 9221-9226 (2008).
45. Guo, B. & Guilford, W. H. Mechanics of actomyosin bonds in different nucleotide states are tuned to muscle contraction. Proc. Natl Acad. Sci. USA. 103, 9844-9849 (2006).
46. Pereverzev, Y. V., Prezhdo, O. V., Forero, M., Sokurenko, E. V. & Thomas, W. E. The two-pathway model for the catch-slip transition in biological adhesion. Biophys. J. 89, 1446-1454 (2005).
47. Evans, E., Leung, A., Heinrich, V. & Zhu, C. Mechanical switching and coupling between two dissociation pathways in a P-selectin adhesion bond. Proc. Natl Acad. Sci. USA 101, 11282-11286 (2004).
48. Gimona, M., Djinovic-Carugo, K., Kranewitter, W. J. & Winder, S. J. Functional plasticity of CH domains. FEBS Lett. 513, 98-106 (2002).
49. Yao, N. Y. et al. Stress-enhanced gelation: A dynamic nonlinearity of elasticity. Phys. Rev. Lett. 110, 018103 (2013).
50. Maugis, B. et al. Dynamic instability of the intracellular pressure drives bleb-based motility. J. Cell Sci. 123, 3884-3892 (2010).
51. Hotulainen, P. & Lappalainen, P. Stress fibers are generated by two distinct actin assembly mechanisms in motile cells. J. Cell Biol. 173, 383-394 (2006).
52. Friedrich, B. M., Friedrich, E. F., Gov, N. S. & Safran, S. A. Sacromeric pattern formation by actin cluster coalescence. PLoS Comput. Biol. 8, e1002544 (2012).
53. Dickinson, D. J., Robinson, D. N., Nelson, W. J. & Weis, W. I. α-Catenin and IQGAP regulate myosin localization to control epithelial tube morphology in Dictyostelium morphogenesis. Dev. Cell 23, 533-546 (2012).
54. Chen, C-L., Wang, Y., Sesaki, H. & Iijima, M. Myosin I Links PIP3 signaling to remodeling of the actin cytoskeleton in chemotaxis. Sci. Signal. 5, ra10 (2012).