How to understand and outwit adaptation

Developmental Cell

Volumn 28, Issue 6, 2014, Pages 607-616

  Hoeller, Oliver ^a   Gong, Delquin ^a   Weiner, Orion D ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOATTRACTANT; CHEY PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN;

ADAPTATION; ADAPTIVE BEHAVIOR; CALCIUM HOMEOSTASIS; CHEMORECEPTOR; CHEMOTAXIS; CONFORMATIONAL TRANSITION; DICTYOSTELIUM; ESCHERICHIA COLI; EUKARYOTE; NEGATIVE FEEDBACK; NEUTROPHIL; NONHUMAN; OSMOREGULATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; REVIEW; SENSORY RECEPTOR; SIGNAL TRANSDUCTION; STEADY STATE; ANIMAL; BIOLOGICAL MODEL; CELL FUNCTION; EUKARYOTIC CELL; HUMAN; PHYSIOLOGY; CELL STIMULATION; EUKARYOTIC CHEMOTAXIS; GENE EXPRESSION; INTRACELLULAR SIGNALING; OPTOGENETICS; PHENOTYPE; PHOSPHORYLATION; PROTEIN ANALYSIS;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; CELL PHYSIOLOGICAL PHENOMENA; CHEMOTAXIS; EUKARYOTIC CELLS; HUMANS; MODELS, BIOLOGICAL; SIGNAL TRANSDUCTION;

EUKARYOTA;

EID: 84897090999     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2014.03.009     Document Type: Review

References (121)

1. Alon U., Surette M.G., Barkai N., Leibler S. Robustness in bacterial chemotaxis. Nature 1999, 397:168-171.
2. Arai H., Monteclaro F.S., Tsou C.L., Franci C., Charo I.F. Dissociation of chemotaxis from agonist-induced receptor internalization in a lymphocyte cell line transfected with CCR2B. Evidence that directed migration does not require rapid modulation of signaling at the receptor level. J.Biol. Chem. 1997, 272:25037-25042.
3. Arshavsky V.Y. Rhodopsin phosphorylation: from terminating single photon responses to photoreceptor dark adaptation. Trends Neurosci. 2002, 25:124-126.
4. Artemenko Y., Swaney K.F., Devreotes P.N. Assessment of development and chemotaxis in Dictyostelium discoideum mutants. Methods Mol. Biol. 2011, 769:287-309.
5. Artemenko Y., Batsios P., Borleis J., Gagnon Z., Lee J., Rohlfs M., Sanséau D., Willard S.S., Schleicher M., Devreotes P.N. Tumor suppressor Hippo/MST1 kinase mediates chemotaxis by regulating spreading and adhesion. Proc. Natl. Acad. Sci. USA 2012, 109:13632-13637.
6. Barkai N., Leibler S. Robustness in simple biochemical networks. Nature 1997, 387:913-917.
7. Bayle J.H., Grimley J.S., Stankunas K., Gestwicki J.E., Wandless T.J., Crabtree G.R. Rapamycin analogs with differential binding specificity permit orthogonal control of protein activity. Chem. Biol. 2006, 13:99-107.
8. Becskei A., Serrano L. Engineering stability in gene networks by autoregulation. Nature 2000, 405:590-593.
9. Benard V., Bohl B.P., Bokoch G.M. Characterization of rac and cdc42 activation in chemoattractant-stimulated human neutrophils using a novel assay for active GTPases. J.Biol. Chem. 1999, 274:13198-13204.
10. Berg H.C. A physicist looks at bacterial chemotaxis. Cold Spring Harb. Symp. Quant. Biol. 1988, 53:1-9.
11. Berg H.C., Brown D.A. Chemotaxis in Escherichia coli analysed by three-dimensional tracking. Nature 1972, 239:500-504.
12. Bishop A.C., Ubersax J.A., Petsch D.T., Matheos D.P., Gray N.S., Blethrow J., Shimizu E., Tsien J.Z., Schultz P.G., Rose M.D., et al. A chemical switch for inhibitor-sensitive alleles of any protein kinase. Nature 2000, 407:395-401.
13. Bolourani P., Spiegelman G.B., Weeks G. Delineation of the roles played by RasG and RasC in cAMP-dependent signal transduction during the early development of Dictyostelium discoideum. Mol. Biol. Cell 2006, 17:4543-4550.
14. Boyden E.S., Zhang F., Bamberg E., Nagel G., Deisseroth K. Millisecond-timescale, genetically targeted optical control of neural activity. Nat. Neurosci. 2005, 8:1263-1268.
15. Brachmann S.M., Yballe C.M., Innocenti M., Deane J.A., Fruman D.A., Thomas S.M., Cantley L.C. Role of phosphoinositide 3-kinase regulatory isoforms in development and actin rearrangement. Mol. Cell. Biol. 2005, 25:2593-2606.
16. Brzostowski J.A., Sawai S., Rozov O., Liao X.-H., Imoto D., Parent C.A., Kimmel A.R. Phosphorylation of chemoattractant receptors regulates chemotaxis, actin reorganization and signal relay. J.Cell Sci. 2013, 126:4614-4626.
17. Burns M.E., Baylor D.A. Activation, deactivation, and adaptation in vertebrate photoreceptor cells. Annu. Rev. Neurosci. 2001, 24:779-805.
18. Cai H., Das S., Kamimura Y., Long Y., Parent C.A., Devreotes P.N. Ras-mediated activation of the TORC2-PKB pathway is critical for chemotaxis. J.Cell Biol. 2010, 190:233-245.
19. Chang H., Levchenko A. Adaptive molecular networks controlling chemotactic migration: dynamic inputs and selection of the network architecture. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2013, 368:20130117.
20. Charest P.G., Shen Z., Lakoduk A., Sasaki A.T., Briggs S.P., Firtel R.A. A Ras signaling complex controls the RasC-TORC2 pathway and directed cell migration. Dev. Cell 2010, 18:737-749.
21. Chen L., Iijima M., Tang M., Landree M.A., Huang Y.E., Xiong Y., Iglesias P.A., Devreotes P.N. PLA2 and PI3K/PTEN pathways act in parallel to mediate chemotaxis. Dev. Cell 2007, 12:603-614.
22. Cluzel P., Surette M., Leibler S. An ultrasensitive bacterial motor revealed by monitoring signaling proteins in single cells. Science 2000, 287:1652-1655.
23. D'Angelo M.A., Raices M., Panowski S.H., Hetzer M.W. Age-dependent deterioration of nuclear pore complexes causes a loss of nuclear integrity in postmitotic cells. Cell 2009, 136:284-295.
24. Devreotes P.N., Steck T.L. Cyclic 3',5' AMP relay in Dictyostelium discoideum. II. Requirements for the initiation and termination of the response. J.Cell Biol. 1979, 80:300-309.
25. Dinauer M.C., Steck T.L., Devreotes P.N. Cyclic 3',5'-AMP relay in Dictyostelium discoideum V. Adaptation of the cAMP signaling response during cAMP stimulation. J.Cell Biol. 1980, 86:554-561.
26. El-Samad H., Goff J.P., Khammash M. Calcium homeostasis and parturient hypocalcemia: an integral feedback perspective. J.Theor. Biol. 2002, 214:17-29.
27. Franca-Koh J., Kamimura Y., Devreotes P. Navigating signaling networks: chemotaxis in Dictyostelium discoideum. Curr. Opin. Genet. Dev. 2006, 16:333-338.
28. Frank C.A., Kennedy M.J., Goold C.P., Marek K.W., Davis G.W. Mechanisms underlying the rapid induction and sustained expression of synaptic homeostasis. Neuron 2006, 52:663-677.
29. Funamoto S., Meili R., Lee S., Parry L., Firtel R.A. Spatial and temporal regulation of 3-phosphoinositides by PI 3-kinase and PTEN mediates chemotaxis. Cell 2002, 109:611-623.
30. Geda P., Patury S., Ma J., Bharucha N., Dobry C.J., Lawson S.K., Gestwicki J.E., Kumar A. A small molecule-directed approach to control protein localization and function. Yeast 2008, 25:577-594.
31. Goodman O.B., Krupnick J.G., Santini F., Gurevich V.V., Penn R.B., Gagnon A.W., Keen J.H., Benovic J.L. Beta-arrestin acts as a clathrin adaptor in endocytosis of the beta2-adrenergic receptor. Nature 1996, 383:447-450.
32. Gu Y., Filippi M.-D., Cancelas J.A., Siefring J.E., Williams E.P., Jasti A.C., Harris C.E., Lee A.W., Prabhakar R., Atkinson S.J., et al. Hematopoietic cell regulation by Rac1 and Rac2 guanosine triphosphatases. Science 2003, 302:445-449.
33. Hall A.L., Schlein A., Condeelis J. Relationship of pseudopod extension to chemotactic hormone-induced actin polymerization in amoeboid cells. J.Cell. Biochem. 1988, 37:285-299.
34. Han X., Boyden E.S. Multiple-color optical activation, silencing, and desynchronization of neural activity, with single-spike temporal resolution. PLoS ONE 2007, 2:e299.
35. Haruki H., Nishikawa J., Laemmli U.K. The anchor-away technique: rapid, conditional establishment of yeast mutant phenotypes. Mol. Cell 2008, 31:925-932.
36. Hoeller O., Kay R.R. Chemotaxis in the absence of PIP3 gradients. Curr. Biol. 2007, 17:813-817.
37. Hoeller O., Bolourani P., Clark J., Stephens L.R., Hawkins P.T., Weiner O.D., Weeks G., Kay R.R. Two distinct functions for PI3-kinases in macropinocytosis. J.Cell Sci. 2013, 126:4296-4307.
38. Hsu M.H., Chiang S.C., Ye R.D., Prossnitz E.R. Phosphorylation of the N-formyl peptide receptor is required for receptor internalization but not chemotaxis. J.Biol. Chem. 1997, 272:29426-29429.
39. Huang Y.E., Iijima M., Parent C.A., Funamoto S., Firtel R.A., Devreotes P. Receptor-mediated regulation of PI3Ks confines PI(3,4,5)P3 to the leading edge of chemotaxing cells. Mol. Biol. Cell 2003, 14:1913-1922.
40. 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.
41. Iglesias P.A., Devreotes P.N. Navigating through models of chemotaxis. Curr. Opin. Cell Biol. 2008, 20:35-40.
42. Iglesias P.A., Devreotes P.N. Biased excitable networks: how cells direct motion in response to gradients. Curr. Opin. Cell Biol. 2012, 24:245-253.
43. Iijima M., Devreotes P. Tumor suppressor PTEN mediates sensing of chemoattractant gradients. Cell 2002, 109:599-610.
44. 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.
45. Inoue T., Heo W.D., Grimley J.S., Wandless T.J., Meyer T. An inducible translocation strategy to rapidly activate and inhibit small GTPase signaling pathways. Nat. Methods 2005, 2:415-418.
46. Janetopoulos C., Jin T., Devreotes P. Receptor-mediated activation of heterotrimeric G-proteins in living cells. Science 2001, 291:2408-2411.
47. Janetopoulos C., Ma L., Devreotes P.N., Iglesias P.A. Chemoattractant-induced phosphatidylinositol 3,4,5-trisphosphate accumulation is spatially amplified and adapts, independent of the actin cytoskeleton. Proc. Natl. Acad. Sci. USA 2004, 101:8951-8956.
48. Jeon T.J., Lee D.-J., Merlot S., Weeks G., Firtel R.A. Rap1 controls cell adhesion and cell motility through the regulation of myosin II. J.Cell Biol. 2007, 176:1021-1033.
49. Kae H., Lim C.J., Spiegelman G.B., Weeks G. Chemoattractant-induced Ras activation during Dictyostelium aggregation. EMBO Rep. 2004, 5:602-606.
50. Kae H., Kortholt A., Rehmann H., Insall R.H., Van Haastert P.J.M., Spiegelman G.B., Weeks G. Cyclic AMP signalling in Dictyostelium: G-proteins activate separate Ras pathways using specific RasGEFs. EMBO Rep. 2007, 8:477-482.
51. Kappel S., Matthess Y., Kaufmann M., Strebhardt K. Silencing of mammalian genes by tetracycline-inducible shRNA expression. Nat. Protoc. 2007, 2:3257-3269.
52. Karunarathne W.K.A., Giri L., Patel A.K., Venkatesh K.V., Gautam N. Optical control demonstrates switch-like PIP3 dynamics underlying the initiation of immune cell migration. Proc. Natl. Acad. Sci. USA 2013, 110:E1575-E1583.
53. 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.
54. Kim J.Y., Soede R.D., Schaap P., Valkema R., Borleis J.A., Van Haastert P.J., Devreotes P.N., Hereld D. Phosphorylation of chemoattractant receptors is not essential for chemotaxis or termination of G-protein-mediated responses. J.Biol. Chem. 1997, 272:27313-27318.
55. Kollmann M., Løvdok L., Bartholomé K., Timmer J., Sourjik V. Design principles of a bacterial signalling network. Nature 2005, 438:504-507.
56. Komatsu T., Kukelyansky I., McCaffery J.M., Ueno T., Varela L.C., Inoue T. Organelle-specific, rapid induction of molecular activities and membrane tethering. Nat. Methods 2010, 7:206-208.
57. Krupnick J.G., Benovic J.L. The role of receptor kinases and arrestins in G protein-coupled receptor regulation. Annu. Rev. Pharmacol. Toxicol. 1998, 38:289-319.
58. Ku C.-J., Wang Y., Weiner O.D., Altschuler S.J., Wu L.F. Network crosstalk dynamically changes during neutrophil polarization. Cell 2012, 149:1073-1083.
59. 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.
60. Li S., Yamauchi A., Marchal C.C., Molitoris J.K., Quilliam L.A., Dinauer M.C. Chemoattractant-stimulated Rac activation in wild-type and Rac2-deficient murine neutrophils: preferential activation of Rac2 and Rac2 gene dosage effect on neutrophil functions. J.Immunol. 2002, 169:5043-5051.
61. Li Z., Hannigan M., Mo Z., Liu B., Lu W., Wu Y., Smrcka A.V., Wu G., Li L., Liu M., et al. Directional sensing requires G beta gamma-mediated PAK1 and PIX alpha-dependent activation of Cdc42. Cell 2003, 114:215-227.
62. Liu L., Das S., Losert W., Parent C.A. mTORC2 regulates neutrophil chemotaxis in a cAMP- and RhoA-dependent fashion. Dev. Cell 2010, 19:845-857.
63. Lohse M.J., Andexinger S., Pitcher J., Trukawinski S., Codina J., Faure J.P., Caron M.G., Lefkowitz R.J. Receptor-specific desensitization with purified proteins. Kinase dependence and receptor specificity of beta-arrestin and arrestin in the beta 2-adrenergic receptor and rhodopsin systems. J.Biol. Chem. 1992, 267:8558-8564.
64. Ma W., Trusina A., El-Samad H., Lim W.A., Tang C. Defining network topologies that can achieve biochemical adaptation. Cell 2009, 138:760-773.
65. Macnab R.M., Koshland D.E. The gradient-sensing mechanism in bacterial chemotaxis. Proc. Natl. Acad. Sci. USA 1972, 69:2509-2512.
66. Meili R., Ellsworth C., Lee S., Reddy T.B., Ma H., Firtel R.A. Chemoattractant-mediated transient activation and membrane localization of Akt/PKB is required for efficient chemotaxis to cAMP in Dictyostelium. EMBO J. 1999, 18:2092-2105.
67. Murthy V.N., Schikorski T., Stevens C.F., Zhu Y. Inactivity produces increases in neurotransmitter release and synapse size. Neuron 2001, 32:673-682.
68. Muzzey D., Gómez-Uribe C.A., Mettetal J.T., van Oudenaarden A. A systems-level analysis of perfect adaptation in yeast osmoregulation. Cell 2009, 138:160-171.
69. Nishio M., Watanabe K., Sasaki J., Taya C., Takasuga S., Iizuka R., Balla T., Yamazaki M., Watanabe H., Itoh R., et al. Control of cell polarity and motility by the PtdIns(3,4,5)P3 phosphatase SHIP1. Nat. Cell Biol. 2007, 9:36-44.
70. Pankov R., Endo Y., Even-Ram S., Araki M., Clark K., Cukierman E., Matsumoto K., Yamada K.M. A Rac switch regulates random versus directionally persistent cell migration. J.Cell Biol. 2005, 170:793-802.
71. Parent C.A., Blacklock B.J., Froehlich W.M., Murphy D.B., Devreotes P.N. G protein signaling events are activated at the leading edge of chemotactic cells. Cell 1998, 95:81-91.
72. Park K.C., Rivero F., Meili R., Lee S., Apone F., Firtel R.A. Rac regulation of chemotaxis and morphogenesis in Dictyostelium. EMBO J. 2004, 23:4177-4189.
73. Peng G.E., Wilson S.R., Weiner O.D. A pharmacological cocktail for arresting actin dynamics in living cells. Mol. Biol. Cell 2011, 22:3986-3994.
74. Pluta K., Diehl W., Zhang X.-Y., Kutner R., Bialkowska A., Reiser J. Lentiviral vectors encoding tetracycline-dependent repressors and transactivators for reversible knockdown of gene expression: a comparative study. BMC Biotechnol. 2007, 7:41.
75. Porter S.L., Wadhams G.H., Armitage J.P. Signal processing in complex chemotaxis pathways. Nat. Rev. Microbiol. 2011, 9:153-165.
76. Pringle J.R. Induction, selection, and experimental uses of temperature-sensitive and other conditional mutants of yeast. Methods Cell Biol. 1975, 12:233-272.
77. Purvis J.E., Karhohs K.W., Mock C., Batchelor E., Loewer A., Lahav G. p53 dynamics control cell fate. Science 2012, 336:1440-1444.
78. Quail P.H. Phytochrome photosensory signalling networks. Nat. Rev. Mol. Cell Biol. 2002, 3:85-93.
79. Ridley A.J., Schwartz M.A., Burridge K., Firtel R.A., Ginsberg M.H., Borisy G., Parsons J.T., Horwitz A.R. Cell migration: integrating signals from front to back. Science 2003, 302:1704-1709.
80. Robinson M.S., Sahlender D.A., Foster S.D. Rapid inactivation of proteins by rapamycin-induced rerouting to mitochondria. Dev. Cell 2010, 18:324-331.
81. Sasaki A.T., Chun C., Takeda K., Firtel R.A. Localized Ras signaling at the leading edge regulates PI3K, cell polarity, and directional cell movement. J.Cell Biol. 2004, 167:505-518.
82. Sasaki A.T., Janetopoulos C., Lee S., Charest P.G., Takeda K., Sundheimer L.W., Meili R., Devreotes P.N., Firtel R.A. G protein-independent Ras/PI3K/F-actin circuit regulates basic cell motility. J.Cell Biol. 2007, 178:185-191.
83. 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.
84. Spencer D.M., Wandless T.J., Schreiber S.L., Crabtree G.R. Controlling signal transduction with synthetic ligands. Science 1993, 262:1019-1024.
85. Stankunas K., Bayle J.H., Gestwicki J.E., Lin Y.-M., Wandless T.J., Crabtree G.R. Conditional protein alleles using knockin mice and a chemical inducer of dimerization. Mol. Cell 2003, 12:1615-1624.
86. Stankunas K., Bayle J.H., Havranek J.J., Wandless T.J., Baker D., Crabtree G.R., Gestwicki J.E. Rescue of degradation-prone mutants of the FK506-rapamycin binding (FRB) protein with chemical ligands. ChemBioChem 2007, 8:1162-1169.
87. Stephens L.R., Hughes K.T., Irvine R.F. Pathway of phosphatidylinositol(3,4,5)-trisphosphate synthesis in activated neutrophils. Nature 1991, 351:33-39.
88. 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.
89. Sun C.X., Downey G.P., Zhu F., Koh A.L.Y., Thang H., Glogauer M. Rac1 is the small GTPase responsible for regulating the neutrophil chemotaxis compass. Blood 2004, 104:3758-3765.
90. Szobota S., Gorostiza P., Del Bene F., Wyart C., Fortin D.L., Kolstad K.D., Tulyathan O., Volgraf M., Numano R., Aaron H.L., et al. Remote control of neuronal activity with a light-gated glutamate receptor. Neuron 2007, 54:535-545.
91. Takeda K., Shao D., Adler M., Charest P.G., Loomis W.F., Levine H., Groisman A., Rappel W.-J., Firtel R.A. Incoherent feedforward control governs adaptation of activated ras in a eukaryotic chemotaxis pathway. Sci. Signal. 2012, 5:ra2.
92. Tan G., Chen M., Foote C., Tan C. Temperature-sensitive mutations made easy: generating conditional mutations by using temperature-sensitiveinteins that function within different temperature ranges. Genetics 2009, 183:13-22.
93. Thiagarajan T.C., Piedras-Renteria E.S., Tsien R.W. alpha- and betaCaMKII. Inverse regulation by neuronal activity and opposing effects on synaptic strength. Neuron 2002, 36:1103-1114.
94. Toettcher J.E., Gong D., Lim W.A., Weiner O.D. Light-based feedback for controlling intracellular signaling dynamics. Nat. Methods 2011, 8:837-839.
95. Toettcher J.E., Weiner O.D., Lim W.A. Using optogenetics to interrogate the dynamic control of signal transmission by the Ras/Erk module. Cell 2013, 155:1422-1434.
96. Turrigiano G., Abbott L.F., Marder E. Activity-dependent changes in the intrinsic properties of cultured neurons. Science 1994, 264:974-977.
97. Van Haastert P.J., Van der Heijden P.R. Excitation, adaptation, and deadaptation of the cAMP-mediated cGMP response in Dictyostelium discoideum. J.Cell Biol. 1983, 96:347-353.
98. van Haastert P.J.M., Keizer-Gunnink I., Kortholt A. Essential role of PI3-kinase and phospholipase A2 in Dictyostelium discoideum chemotaxis. J.Cell Biol. 2007, 177:809-816.
99. Veltman D.M., Keizer-Gunnik I., Van Haastert P.J.M. Four key signaling pathways mediating chemotaxis in Dictyostelium discoideum. J.Cell Biol. 2008, 180:747-753.
100. Vlahou G., Rivero F. Rho GTPase signaling in Dictyostelium discoideum: insights from the genome. Eur. J. Cell Biol. 2006, 85:947-959.
101. Wang C.J., Bergmann A., Lin B., Kim K., Levchenko A. Diverse sensitivity thresholds in dynamic signaling responses by social amoebae. Sci. Signal. 2012, 5:ra17.
102. Weinberger L.S., Dar R.D., Simpson M.L. Transient-mediated fate determination in a transcriptional circuit of HIV. Nat. Genet. 2008, 40:466-470.
103. 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.
104. 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.
105. Welch H.C.E., Coadwell W.J., Ellson C.D., Ferguson G.J., Andrews S.R., Erdjument-Bromage H., Tempst P., Hawkins P.T., Stephens L.R. P-Rex1, a PtdIns(3,4,5)P3- and Gbetagamma-regulated guanine-nucleotide exchange factor for Rac. Cell 2002, 108:809-821.
106. Wong K., Pertz O., Hahn K., Bourne H. Neutrophil polarization: spatiotemporal dynamics of RhoA activity support a self-organizing mechanism. Proc. Natl. Acad. Sci. USA 2006, 103:3639-3644.
107. 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.
108. 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. USA 2010, 107:17079-17086.
109. Xu X., Meier-Schellersheim M., Jiao X., Nelson L.E., Jin T. Quantitative imaging of single live cells reveals spatiotemporal dynamics of multistep signaling events of chemoattractant gradient sensing in Dictyostelium. Mol. Biol. Cell 2005, 16:676-688.
110. Yang H.W., Shin M.-G., Lee S., Kim J.-R., Park W.S., Cho K.-H., Meyer T., Heo W.D. Cooperative activation of PI3K by Ras and Rho family small GTPases. Mol. Cell 2012, 47:281-290.
111. Yang X., Jost A.P.-T., 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.
112. Yi T.M., Huang Y., Simon M.I., Doyle J. Robust perfect adaptation in bacterial chemotaxis through integral feedback control. Proc. Natl. Acad. Sci. USA 2000, 97:4649-4653.
113. Yoo S.K., Deng Q., Cavnar P.J., Wu Y.I., Hahn K.M., Huttenlocher A. Differential regulation of protrusion and polarity by PI3K during neutrophil motility in live zebrafish. Dev. Cell 2010, 18:226-236.
114. Yuan J., Berg H.C. Ultrasensitivity of an adaptive bacterial motor. J.Mol. Biol. 2013, 425:1760-1764.
115. Yuan J., Branch R.W., Hosu B.G., Berg H.C. Adaptation at the output of the chemotaxis signalling pathway. Nature 2012, 484:233-236.
116. Zhang S., Charest P.G., Firtel R.A. Spatiotemporal regulation of Ras activity provides directional sensing. Curr. Biol. 2008, 18:1587-1593.
117. Zhao M., Jin T., McCaig C.D., Forrester J.V., Devreotes P.N. Genetic analysis of the role of G protein-coupled receptor signaling in electrotaxis. J.Cell Biol. 2002, 157:921-927.
118. Zheng L., Eckerdal J., Dimitrijevic I., Andersson T. Chemotactic peptide-induced activation of Ras in human neutrophils is associated with inhibition of p120-GAP activity. J.Biol. Chem. 1997, 272:23448-23454.
119. 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.
120. Zigmond S.H. Ability of polymorphonuclear leukocytes to orient in gradients of chemotactic factors. J.Cell Biol. 1977, 75:606-616.
121. Zigmond S.H., Sullivan S.J. Sensory adaptation of leukocytes to chemotactic peptides. J.Cell Biol. 1979, 82:517-527.