Feedback regulation between plasma membrane tension and membrane-bending proteins organizes cell polarity during leading edge formation

Nature Cell Biology

Volumn 17, Issue 6, 2015, Pages 749-758

  Tsujita, Kazuya ^a   Takenawa, Tadaomi ^b   Itoh, Toshiki ^a  

^a KOBE UNIVERSITY   (Japan)

^b KOBE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ACTIN RELATED PROTEIN 2-3 COMPLEX; CLATHRIN; FBP17 PROTEIN; MEMBRANE PROTEIN; NEURAL WISKOTT ALDRICH SYNDROME PROTEIN; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; UNCLASSIFIED DRUG; WISKOTT ALDRICH SYNDROME PROTEIN; CARRIER PROTEIN; FNBP1 PROTEIN, HUMAN; FNBP1L PROTEIN, HUMAN; LIPOSOME; MICROTUBULE ASSOCIATED PROTEIN; SMALL INTERFERING RNA; TRIP10 PROTEIN, HUMAN;

ACTIN POLYMERIZATION; ARTICLE; BINDING AFFINITY; CELL MIGRATION; CELL POLARITY; CELL STRUCTURE; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FEEDBACK SYSTEM; IN VITRO STUDY; MEMBRANE BINDING; MEMBRANE BIOLOGY; PLASMA MEMBRANE TENSION; POLARIZATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; 3T3 CELL LINE; ANIMAL; CELL LINE; CELL MEMBRANE; CELL MOTION; CHLOROCEBUS AETHIOPS; COS 1 CELL LINE; ENZYME ACTIVATION; GENETICS; HUMAN; MECHANICAL STRESS; METABOLISM; MOUSE; PHYSIOLOGICAL STRESS; PHYSIOLOGY; RNA INTERFERENCE;

3T3 CELLS; ACTINS; ANIMALS; CARRIER PROTEINS; CELL LINE; CELL MEMBRANE; CELL MOVEMENT; CELL POLARITY; CERCOPITHECUS AETHIOPS; COS CELLS; ENZYME ACTIVATION; HUMANS; LIPOSOMES; MEMBRANE PROTEINS; MICE; MICROTUBULE-ASSOCIATED PROTEINS; RNA INTERFERENCE; RNA, SMALL INTERFERING; STRESS, MECHANICAL; STRESS, PHYSIOLOGICAL; WISKOTT-ALDRICH SYNDROME PROTEIN, NEURONAL;

EID: 84930178562     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb3162     Document Type: Article

References (52)

1. Jilkine, A. & Edelstein-Keshet, L. A comparison of mathematical models for polarization of single eukaryotic cells in response to guided cues. PLoS Comput. Biol. 7, e1001121 (2011)
2. Neilson, M. P. et al. Chemotaxis: a feedback-based computational model robustly predicts multiple aspects of real cell behaviour. PLoS Biol. 9, e1000618 (2011)
3. Graziano, B. R. & Weiner, O. D. Self-organization of protrusions and polarity during eukaryotic chemotaxis. Curr. Opin. Cell Biol. 30, 60-67 (2014)
4. Weiner, O. D., Marganski, W. A., Wu, L. F., Altschuler, S. J. & Kirschner, M. W. An actin-based wave generator organizes cell motility. PLoS Biol. 5, e221 (2007)
5. Veltman, D. M., King, J. S., Machesky, L. M. & Insall, R. H. SCAR knockouts in Dictyostelium: WASP assumes SCAR's position and upstream regulators in pseudopods. J. Cell Biol. 198, 501-508 (2012)
6. Huang, C. H., Tang, M., Shi, C., Iglesias, P. A. & Devreotes, P. N. An excitable signal integrator couples to an idling cytoskeletal oscillator to drive cell migration. Nat. Cell Biol. 15, 1307-1316 (2013)
7. Allard, J. & Mogilner, A. Traveling waves in actin dynamics and cell motility. Curr. Opin. Cell Biol. 25, 107-115 (2012)
8. Iglesias, P. A. & Devreotes, P. N. Biased excitable networks: how cells direct motion in response to gradients. Curr. Opin. Cell Biol. 24, 245-253 (2012)
9. Houk, A. R. et al. Membrane tension maintains cell polarity by confining signals to the leading edge during neutrophil migration. Cell 148, 175-188 (2012)
10. Gauthier, N. C., Masters, T. A. & Sheetz, M. P. Mechanical feedback between membrane tension and dynamics. Trends Cell Biol. 22, 527-535 (2012)
11. Diz-Munoz, A., Fletcher, D. A. & Weiner, O. D. Use the force: membrane tension as an organizer of cell shape and motility. Trends Cell Biol. 23, 47-53 (2013)
12. Lieber, A. D., Yehudai-Resheff, S., Barnhart, E. L., Theriot, J. A. & Keren, K. Membrane tension in rapidly moving cells is determined by cytoskeletal forces. Curr. Biol. 23, 1409-1417 (2013)
13. Ho, H. Y. et al. Toca-1 mediates Cdc42-dependent actin nucleation by activating the N-WASP-WIP complex. Cell 118, 203-216 (2004)
14. Hu, J., Mukhopadhyay, A. & Craig, A. W. Transducer of Cdc42-dependent actin assembly promotes epidermal growth factor-induced cell motility and invasiveness. J. Biol. Chem. 286, 2261-2272 (2011)
15. Malet-Engra, G. et al. CIP4 controls CCL19-driven cell steering and chemotaxis in chronic lymphocytic leukemia. Cancer Res. 73, 3412-3424 (2013)
16. Chander, H., Truesdell, P., Meens, J. & Craig, A. W. Transducer of Cdc42-dependent actin assembly promotes breast cancer invasion and metastasis. Oncogene 32, 3080-3090 (2013)
17. Rolland, Y. et al. The CDC42-interacting protein 4 controls epithelial cell cohesion and tumor dissemination. Dev. Cell 30, 553-568 (2014)
18. Truesdell, P. et al. CIP4 promotes lung adenocarcinoma metastasis and is associated with poor prognosis. Oncogene http://dx.doi.org/10.1038/onc.2014.280 (2014)
19. Shimada, A. et al. Curved EFC/F-BAR-domain dimers are joined end to end into a filament for membrane invagination in endocytosis. Cell 129, 761-772 (2007)
20. Frost, A. et al. Structural basis of membrane invagination by F-BAR domains. Cell 132, 807-817 (2008)
21. Liu, J., Sun, Y., Drubin, D. G. & Oster, G. F. The mechanochemistry of endocytosis. PLoS Biol. 7, e1000204 (2009)
22. Takano, K., Toyooka, K. & Suetsugu, S. EFC/F-BAR proteins and the N-WASP-WIP complex induce membrane curvature-dependent actin polymerization. EMBO J. 27, 2817-2828 (2008)
23. Padrick, S. B. et al. Hierarchical regulation of WASP/WAVE proteins. Mol. Cell 32, 426-438 (2008)
24. Wu, M., Wu, X. & DeCamilli, P. Calcium oscillations-coupled conversion of actin travelling waves to standing oscillations. Proc. Natl Acad. Sci. USA 110, 1339-1344 (2013)
25. Wu, M. et al. Coupling between clathrin-dependent endocytic budding and F-BARdependent tubulation in a cell-free system. Nat. Cell Biol. 12, 902-908 (2010)
26. Raucher, D. & Sheetz, M. P. Cell spreading and lamellipodial extension rate is regulated by membrane tension. J. Cell Biol. 148, 127-136 (2000)
27. Sheetz, M. P. Cell control by membrane-cytoskeleton adhesion. Nat. Rev. Mol. Cell Biol. 2, 392-396 (2001)
28. Diz-Munoz, A. et al. Control of directed cell migration in vivo by membrane-to-cortex attachment. PLoS Biol. 8, e1000544 (2010)
29. Raucher, D. et al. Phosphatidylinositol 4,5-bisphosphate functions as a second messenger that regulates cytoskeleton-plasma membrane adhesion. Cell 100, 221-228 (2000)
30. Hao, J. J. et al. Phospholipase C-mediated hydrolysis of PIP2 releases ERM proteins from lymphocyte membrane. J. Cell Biol. 184, 451-462 (2009)
31. Ueno, T., Falkenburger, B. H., Pohlmeyer, C. & Inoue, T. Triggering actin comets versus membrane ruffles: distinctive effects of phosphoinositides on actin reorganization. Sci. Signal 4, ra87 (2011)
32. Varnai, P., Thyagarajan, B., Rohacs, T. & Balla, T. Rapidly inducible changes in phosphatidylinositol 4,5-bisphosphate levels influence multiple regulatory functions of the lipid in intact living cells. J. Cell Biol. 175, 377-382 (2006)
33. Itoh, T. et al. Dynamin and the actin cytoskeleton cooperatively regulate plasma membrane invagination by BAR and F-BAR proteins. Dev. Cell 9, 791-804 (2005)
34. Tsujita, K. et al. Coordination between the actin cytoskeleton and membrane deformation by a novel membrane tubulation domain of PCH proteins is involved in endocytosis. J. Cell Biol. 172, 269-279 (2006)
35. Giannone, G. et al. Periodic lamellipodial contractions correlate with rearward actin waves. Cell 116, 431-443 (2004)
36. Giannone, G. et al. Lamellipodial actin mechanically links myosin activity with adhesion-site formation. Cell 128, 561-575 (2007)
37. Nolen, B. J. et al. Characterization of two classes of small molecule inhibitors of Arp2/3 complex. Nature 460, 1031-1034 (2009)
38. Gauthier, N. C., Fardin, M. A., Roca-Cusachs, P. & Sheetz, M. P. Temporary increase in plasma membrane tension coordinates the activation of exocytosis and contraction during cell spreading. Proc. Natl Acad. Sci. USA 108, 14467-14472 (2011)
39. Batchelder, E. L. et al. Membrane tension regulates motility by controlling lamellipodium organization. Proc. Natl Acad. Sci. USA 108, 11429-11434 (2011)
40. Fujita, H., Katoh, H., Ishikawa, Y., Mori, K. & Negishi, M. Rapostlin is a novel effector of Rnd2 GTPase inducing neurite branching. J. Biol. Chem. 277, 45428-45434 (2002)
41. Itoh, T. & DeCamilli, P. BAR, F-BAR (EFC) and ENTH/ANTH domains in the regulation of membrane-cytosol interfaces and membrane curvature. Biochim. Biophys. Acta 1761, 897-912 (2006)
42. Soderling, S. H. et al. The WRP component of the WAVE-1 complex attenuates Racmediated signalling. Nat. Cell Biol. 4, 970-975 (2002)
43. Guerrier, S. et al. The F-BAR domain of srGAP2 induces membrane protrusions required for neuronal migration and morphogenesis. Cell 138, 990-1004 (2009)
44. Yamazaki, D., Itoh, T., Miki, H. & Takenawa, T. srGAP1 regulates lamellipodial dynamics and cell migratory behavior by modulating Rac1 activity. Mol. Biol. Cell 24, 3393-3405 (2013)
45. Itoh, T., Hasegawa, J., Tsujita, K., Kanaho, Y. & Takenawa, T. The tyrosine kinase Fer is a downstream target of the PLD-PA pathway that regulates cell migration. Sci. Signal. 2, ra52 (2009)
46. Itoh, T. et al. Dynamin and the actin cytoskeleton cooperatively regulate plasma membrane invagination by BAR and F-BAR proteins. Dev. Cell 9, 791-804 (2005)
47. Tsujita, K. et al. Coordination between the actin cytoskeleton and membrane deformation by a novel membrane tubulation domain of PCH proteins is involved in endocytosis. J. Cell Biol. 172, 269-279 (2006)
48. Tsujita, K. et al. Antagonistic regulation of F-BAR protein assemblies controls actin polymerization during podosome formation. J. Cell Sci. 126, 2267-2278 (2013)
49. Shimada, A. et al. Curved EFC/F-BAR-domain dimers are joined end to end into a filament for membrane invagination in endocytosis. Cell 129, 761-772 (2007)
50. Sheetz, M. P. Cell control by membrane-cytoskeleton adhesion. Nat. Rev. Mol. Cell Biol. 2, 392-396 (2001)
51. Morlot, S. et al. Membrane shape at the edge of the dynamin helix sets location and duration of the fission reaction. Cell 151, 619-629 (2012)
52. Bhatia, V. K. et al. Amphipathic motifs in BAR domains are essential for membrane curvature sensing. EMBO J. 28, 3303-3314 (2009).