Self-organization of protrusions and polarity during eukaryotic chemotaxis

Current Opinion in Cell Biology

Volumn 30, Issue 1, 2014, Pages 60-67

  Graziano, Brian R ^a   Weiner, Orion D ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN FILAMENT; ACTIN POLYMERIZATION; CELL ADHESION; CELL FUNCTION; CELL MEMBRANE; CELL MIGRATION; CELL MOTILITY; CELL MOTION; CELL POLARITY; CHEMOTAXIS; DENDRITIC CELL; EUKARYOTIC CELL; FORCE; LAMELLIPODIUM; MORPHOLOGY; NEGATIVE FEEDBACK; NONHUMAN; OSCILLATION; PHENOTYPE; POSITIVE FEEDBACK; PRIORITY JOURNAL; QUALITATIVE ANALYSIS; REVIEW; CELL COUNT; IN VITRO STUDY; MEMBRANE BINDING; SIGNAL TRANSDUCTION; ANIMAL; CYTOLOGY; HUMAN; METABOLISM; PHYSIOLOGY; PSEUDOPODIUM;

ACTIN BINDING PROTEIN; ACTIN;

EUKARYOTA;

ACTINS; ANIMALS; CELL POLARITY; CHEMOTAXIS; EUKARYOTIC CELLS; HUMANS; PSEUDOPODIA; SIGNAL TRANSDUCTION;

EID: 84903773322     PISSN: 09550674     EISSN: 18790410     Source Type: Journal    
DOI: 10.1016/j.ceb.2014.06.007     Document Type: Review

References (87)

1. De Bruyn P.P. The amoeboid movement of the mammalian leukocyte in tissue culture. Anat Rec 1946, 95:177-191.
2. Hartman R.S., Lau K., Chou W., Coates T.D. The fundamental motor of the human neutrophil is not random: evidence for local non-Markov movement in neutrophils. Biophys J 1994, 67:2535-2545.
3. Killich T., Plath P.J., Wei X., Bultmann H., Rensing L., Vicker M.G. The locomotion, shape and pseudopodial dynamics of unstimulated Dictyostelium cells are not random. J Cell Sci 1993, 106(Pt 4):1005-1013.
4. Vicker M.G. Reaction-diffusion waves of actin filament polymerization/depolymerization in Dictyostelium pseudopodium extension and cell locomotion. Biophys Chem 2000, 84:87-98.
5. Vicker M.G. Eukaryotic cell locomotion depends on the propagation of self-organized reaction-diffusion waves and oscillations of actin filament assembly. Exp Cell Res 2002, 275:54-66.
6. Bretschneider T., Diez S., Anderson K., Heuser J., Clarke M., Muller-Taubenberger A., Kohler J., Gerisch G. Dynamic actin patterns and Arp2/3 assembly at the substrate-attached surface of motile cells. Curr Biol 2004, 14:1-10.
7. Gerisch G., Bretschneider T., Muller-Taubenberger A., Simmeth E., Ecke M., Diez S., Anderson K. Mobile actin clusters and traveling waves in cells recovering from actin depolymerization. Biophys J 2004, 87:3493-3503.
8. Xiong Y., Huang C.H., Iglesias P.A., Devreotes P.N. Cells navigate with a local-excitation, global-inhibition-biased excitable network. Proc Natl Acad Sci U S A 2010, 107:17079-17086.
9. 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 2012, 198:501-508.
10. 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 2013, 15:1307-1316.
11. 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 2007, 5:e221.
12. Millius A., Dandekar S.N., Houk A.R., Weiner O.D. Neutrophils establish rapid and robust WAVE complex polarity in an actin-dependent fashion. Curr Biol 2009, 19:253-259.
13. Dobereiner H.G., Dubin-Thaler B.J., Hofman J.M., Xenias H.S., Sims T.N., Giannone G., Dustin M.L., Wiggins C.H., Sheetz M.P. Lateral membrane waves constitute a universal dynamic pattern of motile cells. Phys Rev Lett 2006, 97:038102.
14. Case L.B., Waterman C.M. Adhesive F-actin waves: a novel integrin-mediated adhesion complex coupled to ventral actin polymerization. PLoS ONE 2011, 6:e26631.
15. Lam Hui K., Kwak S.I., Upadhyaya A. Adhesion-dependent modulation of actin dynamics in Jurkat T cells. Cytoskeleton (Hoboken) 2014, 71:119-135.
16. Cross M.C., Hohenberg P.C. Pattern-formation outside of equilibrium. Rev Mod Phys 1993, 65:851-1112.
17. Neilson M.P., Veltman D.M., van Haastert P.J., Webb S.D., Mackenzie J.A., Insall R.H. Chemotaxis: a feedback-based computational model robustly predicts multiple aspects of real cell behaviour. PLoS Biol 2011, 9:e1000618.
18. Shibata T., Nishikawa M., Matsuoka S., Ueda M. Intracellular encoding of spatiotemporal guidance cues in a self-organizing signaling system for chemotaxis in Dictyostelium cells. Biophys J 2013, 105:2199-2209.
19. Nishikawa M., Horning M., Ueda M., Shibata T. Excitable signal transduction induces both spontaneous and directional cell asymmetries in the phosphatidylinositol lipid signaling system for eukaryotic chemotaxis. Biophys J 2014, 106:723-734.
20. Weiner O.D., Rentel M.C., Ott A., Brown G.E., Jedrychowski M., Yaffe M.B., Gygi S.P., Cantley L.C., Bourne H.R., Kirschner M.W. Hem-1 complexes are essential for Rac activation, actin polymerization, and myosin regulation during neutrophil chemotaxis. PLoS Biol 2006, 4:e38.
21. Allard J., Mogilner A. Traveling waves in actin dynamics and cell motility. Curr Opin Cell Biol 2013, 25:107-115.
22. Arai Y., Shibata T., Matsuoka S., Sato M.J., Yanagida T., Ueda M. Self-organization of the phosphatidylinositol lipids signaling system for random cell migration. Proc Natl Acad Sci U S A 2010, 107:12399-12404.
23. Millius A., Watanabe N., Weiner O.D. Diffusion, capture and recycling of SCAR/WAVE and Arp2/3 complexes observed in cells by single-molecule imaging. J Cell Sci 2012, 125:1165-1176.
24. Inoue T., Meyer T. Synthetic activation of endogenous PI3K and Rac identifies an AND-gate switch for cell polarization and migration. PLoS ONE 2008, 3:e3068.
25. Servant G., Weiner O.D., Herzmark P., Balla T., Sedat J.W., Bourne H.R. Polarization of chemoattractant receptor signaling during neutrophil chemotaxis. Science 2000, 287:1037-1040.
26. Weiner O.D., Neilsen P.O., Prestwich G.D., Kirschner M.W., Cantley L.C., Bourne H.R. A PtdInsP(3)- and Rho GTPase-mediated positive feedback loop regulates neutrophil polarity. Nat Cell Biol 2002, 4:509-513.
27. Kunida K., Matsuda M., Aoki K. FRET imaging and statistical signal processing reveal positive and negative feedback loops regulating the morphology of randomly migrating HT-1080 cells. J Cell Sci 2012, 125:2381-2392.
28. Cross M.C., Hohenberg P.C. Spatiotemporal chaos. Science 1994, 263:1569-1570.
29. Blagg S.L., Stewart M., Sambles C., Insall R.H. PIR121 regulates pseudopod dynamics and SCAR activity in Dictyostelium. Curr Biol 2003, 13:1480-1487.
30. Kunda P., Craig G., Dominguez V., Baum B. Abi Sra1, and Kette control the stability and localization of SCAR/WAVE to regulate the formation of actin-based protrusions. Curr Biol 2003, 13:1867-1875.
31. Yamazaki D., Suetsugu S., Miki H., Kataoka Y., Nishikawa S., Fujiwara T., Yoshida N., Takenawa T. WAVE2 is required for directed cell migration and cardiovascular development. Nature 2003, 424:452-456.
32. Yan C., Martinez-Quiles N., Eden S., Shibata T., Takeshima F., Shinkura R., Fujiwara Y., Bronson R., Snapper S.B., Kirschner M.W., et al. WAVE2 deficiency reveals distinct roles in embryogenesis and Rac-mediated actin-based motility. EMBO J 2003, 22:3602-3612.
33. Innocenti M., Gerboth S., Rottner K., Lai F.P., Hertzog M., Stradal T.E., Frittoli E., Didry D., Polo S., Disanza A., et al. Abi1 regulates the activity of N-WASP and WAVE in distinct actin-based processes. Nat Cell Biol 2005, 7:969-976.
34. Nicholson-Dykstra S.M., Higgs H.N. Arp2 depletion inhibits sheet-like protrusions but not linear protrusions of fibroblasts and lymphocytes. Cell Motil Cytoskeleton 2008, 65:904-922.
35. Steffen A., Faix J., Resch G.P., Linkner J., Wehland J., Small J.V., Rottner K., Stradal T.E. Filopodia formation in the absence of functional WAVE- and Arp2/3-complexes. Mol Biol Cell 2006, 17:2581-2591.
36. Suraneni P., Rubinstein B., Unruh J.R., Durnin M., Hanein D., Li R. The Arp2/3 complex is required for lamellipodia extension and directional fibroblast cell migration. J Cell Biol 2012, 197:239-251.
37. Langridge P.D., Kay R.R. Mutants in the Dictyostelium Arp2/3 complex and chemoattractant-induced actin polymerization. Exp Cell Res 2007, 313:2563-2574.
38. Wu C., Asokan S.B., Berginski M.E., Haynes E.M., Sharpless N.E., Griffith J.D., Gomez S.M., Bear J.E. Arp2/3 is critical for lamellipodia and response to extracellular matrix cues but is dispensable for chemotaxis. Cell 2012, 148:973-987.
39. Di Nardo A., Cicchetti G., Falet H., Hartwig J.H., Stossel T.P., Kwiatkowski D.J. Arp2/3 complex-deficient mouse fibroblasts are viable and have normal leading-edge actin structure and function. Proc Natl Acad Sci U S A 2005, 102:16263-16268.
40. Machesky L.M., Mullins R.D., Higgs H.N., Kaiser D.A., Blanchoin L., May R.C., Hall M.E., Pollard T.D. Scar, a WASp-related protein, activates nucleation of actin filaments by the Arp2/3 complex. Proc Natl Acad Sci U S A 1999, 96:3739-3744.
41. Co C., Wong D.T., Gierke S., Chang V., Taunton J. Mechanism of actin network attachment to moving membranes: barbed end capture by N-WASP WH2 domains. Cell 2007, 128:901-913.
42. Hu X., Kuhn J.R. Actin filament attachments for sustained motility in vitro are maintained by filament bundling. PLOS ONE 2012, 7:e31385.
43. Montaville P., Jegou A., Pernier J., Compper C., Guichard B., Mogessie B., Schuh M., Romet-Lemonne G., Carlier M.F. Spire and formin 2 synergize and antagonize in regulating actin assembly in meiosis by a ping-pong mechanism. PLoS Biol 2014, 12:e1001795.
44. Gohl C., Banovic D., Grevelhorster A., Bogdan S. WAVE forms hetero- and homo-oligomeric complexes at integrin junctions in Drosophila visualized by bimolecular fluorescence complementation. J Biol Chem 2010, 285:40171-40179.
45. Li P., Banjade S., Cheng H.C., Kim S., Chen B., Guo L., Llaguno M., Hollingsworth J.V., King D.S., Banani S.F., et al. Phase transitions in the assembly of multivalent signalling proteins. Nature 2012, 483:336-340.
46. Suetsugu S., Kurisu S., Oikawa T., Yamazaki D., Oda A., Takenawa T. Optimization of WAVE2 complex-induced actin polymerization by membrane-bound IRSp53, PIP(3), and Rac. J Cell Biol 2006, 173:571-585.
47. Miki H., Yamaguchi H., Suetsugu S., Takenawa T. IRSp53 is an essential intermediate between Rac and WAVE in the regulation of membrane ruffling. Nature 2000, 408:732-735.
48. Weisswange I., Newsome T.P., Schleich S., Way M. The rate of N-WASP exchange limits the extent of ARP2/3-complex-dependent actin-based motility. Nature 2009, 458:87-91.
49. Ydenberg C.A., Smith B.A., Breitsprecher D., Gelles J., Goode B.L. Cease-fire at the leading edge: new perspectives on actin filament branching, debranching, and cross-linking. Cytoskeleton (Hoboken) 2011, 68:596-602.
50. Tang H., Li A., Bi J., Veltman D.M., Zech T., Spence H.J., Yu X., Timpson P., Insall R.H., Frame M.C., et al. Loss of Scar/WAVE complex promotes N-WASP- and FAK-dependent invasion. Curr Biol 2013, 23:107-117.
51. Wilson K., Lewalle A., Fritzsche M., Thorogate R., Duke T., Charras G. Mechanisms of leading edge protrusion in interstitial migration. Nat Commun 2013, 4:2896.
52. Renkawitz J., Schumann K., Weber M., Lammermann T., Pflicke H., Piel M., Polleux J., Spatz J.P., Sixt M. Adaptive force transmission in amoeboid cell migration. Nat Cell Biol 2009, 11:1438-1443.
53. Malawista S.E., de Boisfleury Chevance A., Boxer L.A. Random locomotion and chemotaxis of human blood polymorphonuclear leukocytes from a patient with leukocyte adhesion deficiency-1: normal displacement in close quarters via chimneying. Cell Motil Cytoskeleton 2000, 46:183-189.
54. Lammermann T., Bader B.L., Monkley S.J., Worbs T., Wedlich-Soldner R., Hirsch K., Keller M., Forster R., Critchley D.R., Fassler R., et al. Rapid leukocyte migration by integrin-independent flowing and squeezing. Nature 2008, 453:51-55.
55. Shi Y., Zhang J., Mullin M., Dong B., Alberts A.S., Siminovitch K.A. The mDial formin is required for neutrophil polarization, migration, and activation of the LARG/RhoA/ROCK signaling axis during chemotaxis. J Immunol 2009, 182:3837-3845.
56. Kitzing T.M., Wang Y., Pertz O., Copeland J.W., Grosse R. Formin-like 2 drives amoeboid invasive cell motility downstream of RhoC. Oncogene 2010, 29:2441-2448.
57. Block J., Breitsprecher D., Kuhn S., Winterhoff M., Kage F., Geffers R., Duwe P., Rohn J.L., Baum B., Brakebusch C., et al. FMNL2 drives actin-based protrusion and migration downstream of Cdc42. Curr Biol 2012, 22:1005-1012.
58. Bilancia C.G., Winkelman J.D., Tsygankov D., Nowotarski S.H., Sees J.A., Comber K., Evans I., Lakhani V., Wood W., Elston T.C., et al. Enabled negatively regulates diaphanous-driven actin dynamics in vitro and in vivo. Dev Cell 2014, 28:394-408.
59. Masters T.A., Pontes B., Viasnoff V., Li Y., Gauthier N.C. Plasma membrane tension orchestrates membrane trafficking, cytoskeletal remodeling, and biochemical signaling during phagocytosis. Proc Natl Acad Sci U S A 2013, 110:11875-11880.
60. 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 U S A 2011, 108:14467-14472.
61. Boulant S., Kural C., Zeeh J.C., Ubelmann F., Kirchhausen T. Actin dynamics counteract membrane tension during clathrin-mediated endocytosis. Nat Cell Biol 2011, 13:1124-1131.
62. Batchelder E.L., Hollopeter G., Campillo C., Mezanges X., Jorgensen E.M., Nassoy P., Sens P., Plastino J. Membrane tension regulates motility by controlling lamellipodium organization. Proc Natl Acad Sci U S A 2011, 108:11429-11434.
63. Keren K., Pincus Z., Allen G.M., Barnhart E.L., Marriott G., Mogilner A., Theriot J.A. Mechanism of shape determination in motile cells. Nature 2008, 453:475-480.
64. Dai J., Sheetz M.P. Regulation of endocytosis, exocytosis, and shape by membrane tension. Cold Spring Harb Symp Quant Biol 1995, 60:567-571.
65. 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 2013, 23:1409-1417.
66. Houk A.R., Jilkine A., Mejean C.O., Boltyanskiy R., Dufresne E.R., Angenent S.B., Altschuler S.J., Wu L.F., Weiner O.D. Membrane tension maintains cell polarity by confining signals to the leading edge during neutrophil migration. Cell 2012, 148:175-188.
67. Yan S., Lv Z., Winterhoff M., Wenzl C., Zobel T., Faix J., Bogdan S., Grosshans J. The F-BAR protein Cip4/Toca-1 antagonizes the formin Diaphanous in membrane stabilization and compartmentalization. J Cell Sci 2013, 126:1796-1805.
68. Graziano B.R., Yu H.Y., Alioto S.L., Eskin J.A., Ydenberg C.A., Waterman D.P., Garabedian M., Goode B.L. The F-BAR protein Hof1 tunes formin activity to sculpt actin cables during polarized growth. Mol Biol Cell 2014, 25:1730-1743.
69. Ahmed S., Goh W.I., Bu W. I-BAR domains, IRSp53 and filopodium formation. Semin Cell Dev Biol 2010, 21:350-356.
70. Fricke R., Gohl C., Dharmalingam E., Grevelhorster A., Zahedi B., Harden N., Kessels M., Qualmann B., Bogdan S. Drosophila Cip4/Toca-1 integrates membrane trafficking and actin dynamics through WASP and SCAR/WAVE. Curr Biol 2009, 19:1429-1437.
71. Ho H.Y., Rohatgi R., Lebensohn A.M., Le M., Li J., Gygi S.P., Kirschner M.W. Toca-1 mediates Cdc42-dependent actin nucleation by activating the N-WASP-WIP complex. Cell 2004, 118:203-216.
72. Chaudhuri O., Parekh S.H., Fletcher D.A. Reversible stress softening of actin networks. Nature 2007, 445:295-298.
73. Loose M., Fischer-Friedrich E., Ries J., Kruse K., Schwille P. Spatial regulators for bacterial cell division self-organize into surface waves in vitro. Science 2008, 320:789-792.
74. Osawa M., Anderson D.E., Erickson H.P. Reconstitution of contractile FtsZ rings in liposomes. Science 2008, 320:792-794.
75. Lebensohn A.M., Kirschner M.W. Activation of the WAVE complex by coincident signals controls actin assembly. Mol Cell 2009, 36:512-524.
76. Koronakis V., Hume P.J., Humphreys D., Liu T., Horning O., Jensen O.N., McGhie E.J. WAVE regulatory complex activation by cooperating GTPases Arf and Rac1. Proc Natl Acad Sci U S A 2011, 108:14449-14454.
77. Krieg M., Helenius J., Heisenberg C.P., Muller D.J. A bond for a lifetime: employing membrane nanotubes from living cells to determine receptor-ligand kinetics. Angew Chem Int Ed Engl 2008, 47:9775-9777.
78. Diz-Munoz A., Krieg M., Bergert M., Ibarlucea-Benitez I., Muller D.J., Paluch E., Heisenberg C.P. Control of directed cell migration in vivo by membrane-to-cortex attachment. PLoS Biol 2010, 8:e1000544.
79. Levskaya A., Weiner O.D., Lim W.A., Voigt C.A. Spatiotemporal control of cell signalling using a light-switchable protein interaction. Nature 2009, 461:997-1001.
80. Yang X., Jost A.P., Weiner O.D., Tang C. A light-inducible organelle-targeting system for dynamically activating and inactivating signaling in budding yeast. Mol Biol Cell 2013, 24:2419-2430.
81. Wu Y.I., Frey D., Lungu O.I., Jaehrig A., Schlichting I., Kuhlman B., Hahn K.M. A genetically encoded photoactivatable Rac controls the motility of living cells. Nature 2009, 461:104-108.
82. Kennedy M.J., Hughes R.M., Peteya L.A., Schwartz J.W., Ehlers M.D., Tucker C.L. Rapid blue-light-mediated induction of protein interactions in living cells. Nat Methods 2010, 7:973-975.
83. Strickland D., Lin Y., Wagner E., Hope C.M., Zayner J., Antoniou C., Sosnick T.R., Weiss E.L., Glotzer M. TULIPs: tunable, light-controlled interacting protein tags for cell biology. Nat Methods 2012, 9:379-384.
84. Bugaj L.J., Choksi A.T., Mesuda C.K., Kane R.S., Schaffer D.V. Optogenetic protein clustering and signaling activation in mammalian cells. Nat Methods 2013, 10:249-252.
85. Zhou X.X., Chung H.K., Lam A.J., Lin M.Z. Optical control of protein activity by fluorescent protein domains. Science 2012, 338:810-814.
86. Charras G.T., Yarrow J.C., Horton M.A., Mahadevan L., Mitchison T.J. Non-equilibration of hydrostatic pressure in blebbing cells. Nature 2005, 435:365-369.
87. Spencer D.M., Wandless T.J., Schreiber S.L., Crabtree G.R. Controlling signal transduction with synthetic ligands. Science 1993, 262:1019-1024.