Mechanisms of Gradient Detection: A Comparison of Axon Pathfinding with Eukaryotic Cell Migration

International Review of Cytology

Volumn 263, Issue , 2007, Pages 1-62

  Philipsborn, Anne von ^a   Bastmeyer, Martin ^a  

^a UNIVERSITY OF KARLSRUHE   (Germany)

Author keywords

Axon guidance; Cell migration; Cell polarization; Dictyostelium; Fibroblast; Gradient detection; Growth cone; Neutrophil

Indexed keywords

ACETYLCHOLINE; BETA ACTIN; BRAIN DERIVED NEUROTROPHIC FACTOR; CHEMOTACTIC FACTOR; CYCLIC AMP; CYTOCHALASIN B; EPHRIN A1; F ACTIN; INTERLEUKIN 8; LATRUNCULIN A; MESSENGER RNA; NETRIN 1; NEUROTRANSMITTER; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PLATELET DERIVED GROWTH FACTOR; PROTEIN CDC42; RAC PROTEIN; RAC1 PROTEIN; RHO FACTOR; RHO GUANINE NUCLEOTIDE BINDING PROTEIN;

ACTIN POLYMERIZATION; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL MIGRATION; CELL STRAIN HL 60; CELL TYPE; CHEMOTAXIS; CYTOSKELETON; DICTYOSTELIUM; ENZYME ACTIVITY; EUKARYOTE; FIBROBLAST; GROWTH CONE; MAMMAL; MORPHOLOGY; NERVE FIBER; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PSEUDOPODIUM; REVIEW; SIGNAL TRANSDUCTION; SPINAL GANGLION;

ANIMALS; AXONS; CHEMOTAXIS, LEUKOCYTE; DICTYOSTELIUM; FIBROBLASTS; GROWTH CONES; HUMANS; NEUTROPHILS; SIGNAL TRANSDUCTION;

DICTYOSTELIUM; EUKARYOTA;

EID: 34548103595     PISSN: 00747696     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0074-7696(07)63001-0     Document Type: Review

References (207)

1. Abercrombie M., Heaysman J.E.M., and Pegrum S.M. The locomotion of fibroblasts in culture I. Movements of the leading edge. Exp. Cell Res. 59 (1970) 393-398
2. Affolter M., and Weijer C.J. Signaling to cytoskeletal dynamics during chemotaxis. Dev. Cell 9 (2005) 19-34
3. Aoki K., Nakamura T., Fujikawa K., and Matsuda M. Local phosphatidylinositol 3,4,5-trisphosphate accumulation recruits Vav2 and Vav3 to activate Rac1/Cdc42 and initiate neurite outgrowth in nerve growth factor-stimulated PC12 cells. Mol. Biol. Cell 16 (2005) 2207-2217
4. Baier H., and Bonhoeffer F. Axon guidance by gradients of a target-derived component. Science 255 (1992) 472-475
5. Baker M.D., Wolanin P.M., and Stock J.B. Signal transduction in bacterial chemotaxis. BioEssays 28 (2005) 9-22
6. Barallobre M.J., Pascual M., Del Rio J.A., and Soriano E. The Netrin family of guidance factors: Emphasis on Netrin-1 signaling. Brain Res. Rev. 49 (2005) 22-47
7. Bodin S., and Welch M.D. Plasma membrane organization is essential for balancing competing pseudopod- and uropod-promoting signals during neutrophil polarization and migration. Mol. Biol. Cell 16 12 (2005) 5773-5783
8. Brown A., Yates P.A., Burrola P., Ortuno D., Vaidya A., Jessel T.M., O'Leary D.D.M., and Lemke G. Topographically mapping from the retina to the midbrain is controlled by relative but not absolute levels of EphA receptor signaling. Cell 102 (2000) 77-88
9. Brunet I., Weinl C., Piper M., Trembleau A., Volovitch M., Harris W., Prochiantz A., and Holt C.E. The transcription factor Engrailed-2 guides retinal axons. Nature 438 (2005) 94-98
10. Buchanan F.G., Elliot C.M., Gibbs M., and Exton J.H. Translocation of the Rac1 guanine nucleotide exchange factor Tiam1 induced by platelet-derived growth factor and lysophosphatidic acid. J. Biol. Chem. 275 (2000) 9742-9748
11. Butler S.J., and Tear G. Getting axons onto the right path: The role of transcription factors in axon guidance. Development 134 (2007) 439-448
12. Campbell D.S., and Holt C.E. Chemotropic responses of retinal growth cones mediated by rapid local protein synthesis and degradation. Neuron 32 (2001) 1013-1026
13. Campbell D.S., and Holt C.E. Apoptotic pathway and MAPKs differentially regulate chemotropic responses of retinal growth cones. Neuron 37 (2003) 939-952
14. Cao X., and Shoichet M.S. Investigating the synergistic effect of combined neurotrophic factor concentration gradients to guide axonal growth. Neuroscience 122 (2003) 381-389
15. Carter A.N., and Downes C.P. Phosphatidylinositol 3-kinase is activated by nerve growth factor and epidermal growth factor in PC12 cells. J. Biol. Chem. 267 (1992) 14563-14567
16. Caterina M.J., Devreotes P.N., Borleis J., and Hereld D. Agonist-induced loss of ligand binding is correlated with phosphorylation of cAR1, a G protein-coupled chemoattractant receptor from dictyostelium. J. Biol. Chem. 270 (1995) 8667-8672
17. Chadborn N.H., Ahmed A.I., Holt M.R., Prinjha R., Dunn G.A., Jones G.E., and Eickholt B.J. PTEN couples Sema3A signaling to growth cone collapse. J. Cell Sci. 119 (2006) 951-957
18. Charest P.G., and Firtel R.A. Feedback signaling controls leading-edge formation during chemotaxis. Curr. Opin. Gen. Dev. 16 (2006) 339-347
19. Charest P.G., and Firtel R.A. Big roles for small GTPases in the control of directed cell movement. Biochem. J. 401 2 (2007) 377-390
20. Charron F., and Tessier-Lavigne M. Novel brain wiring functions for classical morphogens: A role as graded positional cues in axon guidance. Development 132 (2005) 2251-2262
21. Chen L., Janetopoulos C., Huang Y.E., Iijima M., Borleis J., and Devreotes P.N. Two phases of actin polymerization display different dependencies on PI(3,4,5)P3 accumulation and have unique roles during chemotaxis. Mol. Biol. Cell 14 (2003) 5028-5037
22. Chung C.Y., and Firtel R.A. PAKa, a putative PAK family member, is required for cytokinesis and the regulation of the cytoskeleton in dictyostelium discoideum cells during chemotaxis. J. Cell Biol. 147 (1999) 559-576
23. Chung C.Y., Lee S., Briscoe C., Ellsworth C., and Firtel R.A. Role of Rac in controlling the actin cytoskeleton and chemotaxis in motile cells. PNAS 97 (2000) 5225-5230
24. Chung C.Y., Potikyan G., and Firtel R.A. Control of cell polarity and chemotaxis by Akt/PKB and PI3 kinase through the regulation of PAKa. Mol. Cell 7 (2001) 937-947
25. Clotworthy M., and Traynor D. On the effects of cycloheximide on cell motility and polarisation in Dictyostelium discoideum. BMC Cell Biol. 7 (2006) 5-15
26. Condeelis J., Singer R.H., and Segall J.E. The great escape: When cancer cells hijack the genes for chemotaxis and motility. Annu. Rev. Cell Dev. Biol. 21 (2005) 695-718
27. Davis S., Gale N.W., Aldrich T.H., Maisonpierre P.C., Lhotak V., Pawson T., Goldfarb M., and Yancopoulos G.D. Ligands for EPH-related receptor tyrosine kinases that require membrane attachment or clustering for activity. Science 266 (1994) 816-819
28. Debreceni B., Gao Y., Guo F., Zhu K., Jia B., and Zheng Y. Mechanisms of guanine nucleotide exchange and Rac-mediated signaling revealed by a dominant negative trio mutant. J. Biol. Chem. 279 (2004) 3777-3786
29. Derman M.P., Toker A., Hartwig J.H., Spokes K., Falck J.R., Chen C.S., Cantley L.C., and Cantley L.G. The lipid products of phosphoinositide 3-kinase increase cell motility through protein kinase C. J. Biol. Chem. 272 (1997) 6465-6470
30. Deuel T.F., and Kawahara R.S. Growth factors and wound healing: Platelet-derived growth factor as a model cytokine. Annu. Rev. Med. 42 (1991) 567-584
31. Devreotes P., and Janetopoulos C. Eukaryotic chemotaxis: Distinctions between directional sensing and polarization. J. Biol. Chem. 278 (2003) 20445-20448
32. Devreotes P.N., and Zigmond S.H. Chemotaxis in eukaryotic cells: A focus on leukocytes and dictyostelium. Annu. Rev. Cell Biol. 4 (1988) 649-686
33. Dickson B.J. Rho GTPases in growth cone guidance. Curr. Opin. Neurobiol. 11 (2001) 103-110
34. Domeniconi M., and Filbin M.T. Overcoming inhibitors in myelin to promote axonal regeneration. J. Neurol. Sci. 33 (2005) 43-47
35. Dontchev V.D., and Letourneau P.C. Growth cones integrate signaling from multiple guidance cues. J. Histochem. Cytochem. 51 (2003) 435-444
36. Dormann D., and Weijer C.J. Chemotactic cell movement during Dictyostelium development and gastrulation. Curr. Opin. Gen. Dev. 16 (2006) 367-373
37. Dormann D., Vasiev B., and Weijer C.J. The control of chemotactic cell movement during Dictyostelium morphogenesis. Phil. Trans. R. Soc. Lond. B 355 (2000) 983-991
38. Dütting D., Handwerker C., and Drescher U. Topographic targeting and pathfinding errors of retinal axons following overexpressing of ephrinA ligands on retinal ganglion cell axons. Dev. Biol. 216 (1999) 297-311
39. Eddy R.J., Pierini L.M., and Maxfield F.R. Microtubule asymmetry during neutrophil polarization and migration. Mol. Biol. Cell 13 (2002) 4470-4483
40. Egea J., Nissen U.V., Dufour A., Sahin M., Greer P., Kullander K., Mrsic-Flogel T.D., Greenberg M.E., Kiehn O., Vanderhaeghen P., and Klein R. Regulation of EphA4 kinase activity is required for a subset of axon guidance decisions suggesting a key role for receptor clustering in Eph function. Neuron 47 (2005) 515-528
41. Eickholt B.J., Walsh F.S., and Doherty P. An inactive pool of GSK-3 at the leading edge of growth cones is implicated in Semaphorin 3A signaling. J. Cell Biol. 157 (2002) 211-217
42. Eisenbach M., and Giojalas L.C. Sperm guidance in mammals-an unpaved road to the egg. Nat. Rev. Mol. Cell Biol. 7 (2006) 276-285
43. Fan J., and Raper J.A. Localized collapsing cues can steer growth cones without inducing their full collapse. Neuron 14 (1995) 263-274
44. Feldheim D.A., Kim Y.I., Bergemann A.D., Frisen J., Barbacid M., and Flanagan J.G. Genetic analysis of ephrin-A2 and ephrin-A5 shows their requirement in multiple aspects of retinocollicular mapping. Neuron 25 (2000) 563-574
45. Feldheim D.A., Nakamoto M., Osterfield M., Gale N.W., DeChiara T.M., Rohatgi R., Yancopoulos G.D., and Flanagan J.G. Loss-of-function analysis of EphA receptors in retinotectal mapping. J. Neurosci. 24 (2004) 2542-2550
46. Fisher P.R., Merkl R., and Gerisch G. Quantitative analysis of cell motility and chemotaxis in Dictyostelium discoideum by using an image processing system and a novel chemotaxis chamber providing stationary chemical gradients. J. Cell Biol. 108 (1989) 973-984
47. Flanagan J.G. Neural map specification by gradients. Curr. Opin. Neurobiol. 16 (2006) 59-66
48. Foxman E.F., Campbell J.J., and Butcher E.C. Multistep navigation and the combinatorial control of leukocyte chemotaxis. J. Cell Biol. 139 (1997) 1349-1360
49. Foxman E.F., Kunkel E.J., and Butcher E.C. Integrating conflicting chemotactic signals: The role of memory in leukocyte navigation. J. Cell Biol. 147 (1999) 577-588
50. Funamoto S., Meili R., Lee S., Parry L., and Firtel R.A. Spatial and temporal regulation of 3-phosphoinositides by PI 3-kinase and PTEN mediates chemotaxis. Cell 109 (2002) 611-623
51. Gallo G. RhoA-kinase coordinates F-actin organization and myosin II activity during semaphorin-3A-induced axon retraction. J. Cell Sci. 119 (2006) 3413-3423
52. Gierer A. Model for the retino-tectal projection. Proc. R. Soc. Lond. B 218 (1983) 77-93
53. Gomez T.M., and Zheng J.Q. The molecular basis for calcium-dependent axon pathfinding. Nat. Rev. Neurosci. 7 (2006) 115-125
54. Gomez-Mouton C., Lacalle R.A., Mira E., Jiminez-Baranda S., Barber D.F., Carerra A.C., Martinez A., and Manes S. Dynamic redistribution of raft domains as an organizing platform for signaling during cell chemotaxis. J. Cell Biol. 164 (2004) 759-798
55. Goodhill G.J., and Urbach J.S. Theoretical analysis of gradient detection by growth cones. J. Neurobiol. 41 (1999) 230-241
56. Guan K.L., and Rao Y. Signaling mechanisms mediating neuronal responses to guidance cues. Nat. Rev. Neurosci. 4 (2003) 941-956
57. Guirland C., Suzuki S., Kojima M., Lu B., and Zheng J.Q. Lipid rafts mediate chemotropic guidance of nerve growth cones. Neuron 45 (2004) 51-62
58. Gundersen R.W., and Barrett J.N. Neuronal chemotaxis: Chick dorsal-root axons turn toward high concentrations of nerve growth factor. Science 206 (1979) 1079-1080
59. Gundersen R.W., and Barrett J.N. Characterization of the turning response of dorsal root neurites toward nerve growth factor. J. Cell Biol. 87 (1980) 546-554
60. Han J., Han L., Tiwari P., Wen Z., and Zheng J.Q. Spatial targeting of type II protein kinase A to filopodia mediates the regulation of growth cone guidance by cAMP. J. Cell Biol. 176 1 (2007) 101-111
61. Hannigan M., Zhan L., Li Z., Ai Y., Wu D., and Huang C.K. Neutrophils lacking phosphoinositide 3-kinase gamma show loss of directionality during N-formyl-Met-Leu-Phe-induced chemotaxis. PNAS 99 (2002) 3603-3608
62. Hansen M.J., Dallal G.E., and Flanagan J.G. Retinal axon response to ephrin-As shows a graded, concentration-dependent transition from growth promotion to inhibition. Neuron 42 (2004) 717-730
63. Haugh J.M. Deterministic model of dermal wound invasion incorporating receptor-mediated signal transduction and spatial gradient sensing. Biophys. J. 90 (2006) 2297-2308
64. Haugh J.M., Codazzi F., Teruel M., and Meyer T. Spatial sensing in fibroblasts mediated by 3′ phosphoinositides. J. Cell Biol. 151 (2000) 1269-1280
65. Heit B., Tavener S., Raharjo E., and Kubes P. An intracellular signaling hierarchy determines direction of migration in opposing chemotactic gradients. J. Cell Biol. 159 (2002) 91-102
66. Henley J., and Poo M.M. Guiding neuronal growth cones using Ca2+ signals. Trends Cell Biol. 14 (2004) 320-330
67. Henley J.R., Huang K.H., Wang D., and Poo M.M. Calcium mediates bidirectional growth cone turning induced by myelin-associated glycoprotein. Neuron 44 (2004) 909-916
68. Hirsch E., Katanaev V.L., Garlanda C., Azzolino O., Pirola L., Silengo L., Sozzani S., Mantovani A., Altruda F., and Wymann M.P. Central role for G protein-coupled phosphoinositide 3-kinase gamma in inflammation. Science 287 (2000) 1049-1053
69. Honda H. Competitive interactions between retinal ganglion axons for tectal targets explain plasticity of retinotectal projection in the servomechanism model of retinotectal mapping. Dev. Growth Differ. 46 (2004) 425-437
70. Hong K., Nishiyama M., Henley J., Tessier-Lavigne M., and Poo M. Calcium signalling in the guidance of nerve growth by netrin-1. Nature 403 (2000) 93-98
71. Howard T.H., and Oresajo C.O. The kinetics of chemotactic peptide-induced change in F-actin content, F-actin distribution, and the shape of neutrophils. J. Cell Biol. 101 (1985) 1078-1085
72. Höpker V.H., Shewan D., Tessier-Lavigne M., Poo M., and Holt C.E. Growth-cone attraction to netrin-1 is converted to repulsion by laminin-1. Nature 401 (1999) 69-73
73. Hüttelmaier S., Zenklusen D., Lederer M., Dictenberg J., Lorenz M., Meng X., Bassell G.J., Condeelis J., and Singer R.H. Spatial regulation of [beta]-actin translation by Src-dependent phosphorylation of ZBP1. Nature 438 (2005) 512-515
74. Iijima M., and Devreotes P. Tumor suppressor PTEN mediates sensing of chemoattractant gradients. Cell 109 (2002) 599-610
75. Jackson T.R., Blader I.J., Hammonds-Odie L.P., Burga C.R., Cooke F., Hawkins P.T., Wolf A.G., Heldman K.A., and Theibert A.B. Initiation and maintenance of NGF-stimulated neurite outgrowth requires activation of a phosphoinositide 3-kinase. J. Cell Sci. 109 (1996) 289-300
76. Jaffe A.B., and Hall A. RHO GTPases: Biochemistry and biology. Annu. Rev. Cell Dev. Biol. 21 1 (2005) 247-269
77. Janetopoulos C., Ma L., Devreotes P.N., and Iglesias P.A. Chemoattractant-induced phosphatidylinositol 3,4,5-trisphosphate accumulation is spatially amplified and adapts, independent of the actin cytoskeleton. PNAS 101 (2004) 8951-8956
78. Jiang H., Guo W., Liang X., and Rao Y. Both the establishment and the maintenance of neuronal polarity require active mechanisms: Critical roles of GSK-3[beta] and its upstream regulators. Cell 120 (2005) 123-135
79. Jin M., Guan C.B., Jiang Y.A., Chen G., Zhao C.T., Cui K., Song Y.Q., Wu C.P., Poo M.M., and Yuan X.B. Ca2+-dependent regulation of Rho GTPases triggers turning of nerve growth cones. J. Neurosci. 25 (2005) 2338-2347
80. Jin T., Zhang N., Long Y., Parent C.A., and Devreotes P.N. Localization of the G protein complex in living cells during chemotaxis. Science 287 (2000) 1034-1036
81. Jurney W.M., Gallo G., Letourneau P.C., and McLoon S.C. Rac1-mediated endocytosis during ephrin-A2- and semaphorin 3A-induced growth cone collapse. J. Neurosci. 22 (2002) 6019-6028
82. Kazlauskas A., and Cooper J.A. Phosphorylation of the PDGF receptor beta subunit creates a tight binding site for phosphatidylinositol 3-kinase. EMBO J. 9 (1990) 3279-3286
83. Kennedy T.E., Wang H., Marshall W., and Tessier-Lavigne M. Axon guidance by diffusible chemoattractants: A gradient of netrin protein in the developing spinal cord. J. Neurosci. 26 (2006) 8866-8874
84. Kimura K., Hattori S., Kabuyama Y., Shizawa Y., Takayanagi J., Nakamura S., Toki S., Matsuda Y., Onodera K., and Fukui Y. Neurite outgrowth of PC12 cells is suppressed by wortmannin, a specific inhibitor of phosphatidylinositol 3-kinase. J. Biol. Chem. 269 (1994) 18961-18967
85. Kislauskis E.H., Zhu X., and Singer R.H. Sequences responsible for intracellular localization of beta-actin messenger RNA also affect cell phenotype. J. Cell Biol. 127 (1994) 441-451
86. Kislauskis E.H., Zhu X.C., and Singer R.H. b-Actin messenger RNA localization and protein synthesis augment cell motility. J. Cell Biol. 136 (1997) 1263-1270
87. Kita Y., Kimura K.D., Kobayashi M., Ihara S., Kaibuchi K., Kuroda S., Ui M., Iba H., Konishi H., Kikkawa U., Nagata S., and Fukui Y. Microinjection of activated phosphatidylinositol-3 kinase induces process outgrowth in rat PC12 cells through the Rac-JNK signal transduction pathway. J. Cell Sci. 111 (1998) 907-915
88. Kole T.P., Tseng Y., Jiang I., Katz J.L., and Wirtz D. Intracellular mechanics of migrating fibroblasts. Mol. Biol. Cell 16 (2005) 328-338
89. Koulakov A.A., and Tsigankov D.N. A stochastic model for retinocollicular map development. BMC Neurosci. 5 (2004) 30-47
90. Kraynov V.S., Chamberlain C., Bokoch G.M., Schwartz M.A., Slabaugh S., and Hahn K.M. Localized Rac activation dynamics visualized in living cells. Science 290 (2000) 333-337
91. Kruger R.P., Aurandt J., and Guan K.L. Semaphorins command cells to move. Nat. Rev. Mol. Cell Biol. 6 (2005) 789-800
92. Kundra V., Escobedo J.A., Kazlauskas A., Kim H.K., Rhee S.G., Williams L.T., and Zetter B.R. Regulation of chemotaxis by the platelet-derived growth factor receptor-[beta]. Nature 367 (1994) 474-476
93. Kunwar P.S., Siekhaus D.E., and Lehmann R. In vivo migration: A germ cell perspective. Annu. Rev. Cell Dev. Biol. 22 (2006) 237-265
94. Lacalle R.A., Gomez-Mouton C., Barber D.F., Jimenez-Baranda S., Mira E., Martinez A., Carrera A.C., and Manes S. PTEN regulates motility but not directionality during leukocyte chemotaxis. J. Cell Sci. 117 (2004) 6207-6215
95. Letourneau P.C. Chemotactic response of nerve fiber elongation to nerve growth factor. Dev. Biol. 66 (1978) 183-196
96. Leung K.M., van Horck F.P., Lin A.C., Allison R., Standart N., and Holt C.E. Asymmetrical [beta]-actin mRNA translation in growth cones mediates attractive turning to netrin-1. Nat. Neurosci. 9 (2006) 1247-1256
97. Li Y., Jia Y.C., Cui K., Li N., Zheng Z.Y., Wang Y.Z., and Yuan X.B. Essential role of TRPC channels in the guidance of nerve growth cones by brain-derived neurotrophic factor. Nature 434 (2005) 894-898
98. Li Z., Jiang H., Xie W., Zhang Z., Smrcka A.V., and Wu D. Roles of PLC-2 and -3 and PI3K in chemoattractant-mediated signal transduction. Science 287 (2000) 1046-1049
99. Liliental J., Moon S.Y., Lesche R., Mamillapalli R., Li D., Zheng Y., Sun H., and Wu H. Genetic deletion of the PTEN tumor suppressor gene promotes cell motility by activation of Rac1 and Cdc42 GTPases. Curr. Biol. 10 (2000) 401-404
100. Lin F., Nguyen C.M.-C., Wang S.J., Saadi W., Gross S.P., and Jeon N.L. Effective neutrophil chemotaxis is strongly influenced by mean IL-8 concentration. Biochem. Biophys. Res. Comm. 319 (2004) 576-581
101. Lin F., Nguyen C.M.-C., Wang S.J., Saadi W., Gross S.P., and Jeon N.L. Neutrophil migration in opposing chemoattractant gradients using microfluidic chemotaxis devices. Annu. Biomed. Eng. 33 (2005) 475-482
102. Lohof A.M., Quillan M., Dan Y., and Poo M. Asymmetric modulation of cytosolic cAMP activity induces growth cone turning. J. Neurosci. 12 (1992) 1253-1261
103. Löschinger J., Bandtlow C.E., Jung J., Klostermann S., Schwab M.E., Bonhoeffer F., and Kater S.B. Retinal axon growth cone responses to different environmental cues are mediated by different second-messenger systems. J. Neurobiol. 33 (1997) 825-834
104. Löschinger J., Weth F., and Bonhoeffer F. Reading of concentration gradients by axonal growth cones. Phil. Trans. R. Soc. Lond. B 355 (2000) 971-982
105. Marotte L.R., Vidovic M., Wheeler E., and Jhaveri S. Brain-derived neurotrophic factor is expressed in a gradient in the superior colliculus during development of the retinocollicular projection. Eur. J. Neurosci. 20 (2004) 843-847
106. Mato J.M., Losada A., Nanjundiah V., and Konijn T.M. Signal input for a chemotactic response in the cellular slime mold Dictyostelium discoideum. PNAS 72 (1975) 4991-4993
107. McLaughlin T., and O'Leary D.D.M. Molecular gradients and development of retinotopic maps. Annu. Rev. Neurosci. 28 (2005) 327-355
108. Meinhardt H. Orientation of chemotactic cells and growth cones: Models and Mechanisms. J. Cell Sci. 112 (1999) 2867-2874
109. Mellstrom K., Heldin C.H., and Westermark B. Induction of circular membrane ruffling on human fibroblasts by platelet-derived growth factor. Exp. Cell Res. 177 (1988) 347-359
110. Ménager C., Arimura N., Fukata Y., and Kaibuchi K. PIP3 is involved in neuronal polarization and axon formation. J. Neurochem. 89 (2004) 109-118
111. Miki H., Suetsugu S., and Takenawa T. WAVE, a novel WASP-family protein involved in actin reorganization induced by Rac. EMBO J. 17 (1998) 6932-6941
112. Ming G., Wong S.T., Henley J., Yuan X., Song H.J., Spitzer N.C., and Poo M. Adaptation in the chemotactic guidance of nerve growth cones. Nature 417 (2002) 411-418
113. Ming G.L., Song H.J., Berninger B., Holt C.E., Tessier-Lavigne M., and Poo M. cAMP-dependent growth cone guidance by netrin-1. Neuron 19 (1997) 1225-1235
114. Ming G.L., Song H.J., Berninger B., Inagaki N., Tessier-Lavigne M., and Poo M. Phospholipase C-[gamma] and phosphoinositide 3-kinase mediate cytoplasmic signaling in nerve growth cone guidance. Neuron 23 (1999) 139-148
115. Miyamoto Y., Yamauchi J., Tanoue A., Wu C., and Mobley W.C. TrkB binds and tyrosine-phosphorylates Tiam1, leading to activation of Rac1 and induction of changes in cellular morphology. PNAS 103 (2006) 10444-10449
116. Monschau B., Kremoser C., Ohta K., Tanaka H., Kaneki T., Yamada T., Handwerker C., Hornberger M.R., Löschinger J., Pasquale E.B., Siever D.A., Verderame M.F., et al. Shared and distinct functions of RAGS and ELF-1 in guiding retinal axons. EMBO J. 16 (1997) 1258-1267
117. Munck S., Bedner P., Bottaro T., and Harz H. Spatiotemporal properties of cytoplasmic cyclic AMP gradients can alter the turning behavior of neuronal growth cones. Eur. J. Neurosci. 19 (2004) 791-797
118. Myers S.A., Han J.W., Lee Y., Firtel R.A., and Chung C.Y. A dictyostelium homologue of WASP is required for polarized f-actin assembly during chemotaxis. Mol. Biol. Cell 16 (2005) 2191-2206
119. Nakamoto M., Cheng H.J., Friedmann G.C., McLaughlin T., Hansen M.J., Yoon C.H., O'Leary D.D.M., and Flanagan J.G. Topographically specific effects of ELF-1 on retinal axon guidance in vitro and retinal axon mapping in vivo. Cell 86 (1996) 755-766
120. Nakamura T., Aoki K., and Matsuda M. FRET imaging in nerve growth cones reveals a high level of RhoA activity within the peripheral domain. Mol. Brain Res. 139 (2005) 277-287
121. Nebl T., and Fisher P.R. Intracellular Ca2+ signals in Dictyostelium chemotaxis are mediated exclusively by Ca2+ influx. J. Cell Sci. 110 (1997) 2845-2853
122. Niggli V. A membrane-permeant ester of phosphatidylinositol 3,4,5-trisphosphate (PIP3) is an activator of human neutrophil migration. FEBS Lett. 473 (2000) 217-221
123. Niggli V. Signaling to migration in neutrophils: Importance of localized pathways. Int. J. Biochem. Cell Biol. 5 (2003) 1619-1638
124. Nishio M., Watanabe K.I., Sasaki J., Taya C., Takasuga S., Iizuka R., Balla T., Yamazaki M., Watanabe H., Itoh R., Kuroda S., Horie Y., et al. Control of cell polarity and motility by the PtdIns(3,4,5)P3 phosphatase SHIP1. Nat. Cell Biol. 9 1 (2007) 36-44
125. Nishiyama M., Hoshino A., Tsai L., Henley J.R., Goshima Y., Tessier-Lavigne M., Poo M.M., and Hong K. Cyclic AMP/GMP-dependent modulation of Ca2+ channels sets the polarity of nerve growth-cone turning. Nature 423 (2003) 990-995
126. Nobes C.D., Hawkins P., Stephens L., and Hall A. Activation of the small GTP-binding proteins rho and Rac by growth factor receptors. J. Cell Sci. 108 (1995) 225-233
127. Parent C.A., Blacklock B.J., Froehlich W.M., Murphy D.B., and Devreotes P.N. G protein signaling events are activated at the leading edge of chemotactic cells. Cell 95 (1998) 81-91
128. Parent C.A., and Devreotes P.N. A cell's sense of direction. Science 284 (1999) 765-770
129. Pertz O., Hodgson L., Klemke R.L., and Hahn K.M. Spatiotemporal dynamics of RhoA activity in migrating cells. Nature 440 (2006) 1069-1072
130. Piper M., and Holt C. RNA translation in axons. Annu. Rev. Cell Dev. Biol. 20 (2004) 505-523
131. Piper M., Salih S., Weinl C., Holt C.E., and Harris W.A. Endocytosis-dependent desensitization and protein synthesis-dependent resensitization in retinal growth cone adaptation. Nat. Neurosci. 8 (2005) 179-186
132. Piper M., Anderson R., Dwivedy A., Weinl C., van Horck F., Leung K.M., Cogill E., and Holt C. Signaling mechanisms underlying Slit2-induced collapse of Xenopus retinal growth cones. Neuron 49 (2006) 215-228
133. Postma M., Roelofs J., Goedhart J., Gadella T.W.J., Visser A.J.W.G., and Van Haastert P.J.M. Uniform cAMP stimulation of Dictyostelium cells induces localized patches of signal transduction and pseudopodia. Mol. Biol. Cell 14 (2003) 5019-5027
134. Postma M., Roelofs J., Goedhart J., Loovers H.M., Visser A.J.W.G., and Van Haastert P.J.M. Sensitization of Dictyostelium chemotaxis by phosphoinositide-3-kinase-mediated self-organizing signaling patches. J. Cell Sci. 117 (2004) 2925-2935
135. Reber M., Burrola P., and Lemke G. A relative signaling model for the formation of a topographic neural map. Nature 431 (2004) 847-853
136. Richardson R.M., Ali H., Tomhave E.D., Haribabu B., and Snyderman R. Cross-desensitization of chemoattractant receptors occurs at multiple levels. J. Biol. Chem. 270 (1995) 27829-27833
137. Rosentreter S.M., Davenport R.W., Löschinger J., Huf J., Jung J., and Bonhoeffer F. Response of retinal ganglion cell axons to striped linear gradients of repellent guidance molecules. J. Neurobiol. 37 (1998) 541-562
138. Rosoff W.J., McAllister R.G., Esrick M.A., Goodhill G.J., and Urbach J.S. Generating controlled molecular gradients in 3D gels. Biotechnol. Bioeng. 91 6 (2005) 754-759
139. Rubin H., and Ravid S. Polarization of myosin II heavy chain-protein kinase C in chemotaxing Dictyostelium cells. J. Biol. Chem. 277 (2002) 36005-36008
140. Sahin M., Greer P.L., Lin M.Z., Poucher H., Eberhart J., Schmidt S., Wright T.M., Shamah S.M., O'Connell S., Cowan C.W., Hu L., Goldberg J.L., et al. Eph-dependent tyrosine phosphorylation of ephexin1 modulates growth cone collapse. Neuron 46 (2005) 191-204
141. Sander E.E., ten Klooster J.P., van Delft S., van der Kammen R.A., and Collard J.G. Rac downregulates rho activity: Reciprocal balance between both GTPases determines cellular morphology and migratory behavior. J. Cell Biol. 147 (1999) 1009-1022
142. Sasaki T., Irie-Sasaki J., Jones R.G., Oliveira-dos-Santos A.J., Stanford W.L., Bolon B., Wakeham A., Itie A., Bouchard D., Kozieradzki I., Joza N., Mak T.W., et al. Function of PI3K in thymocyte development, T cell activation, and neutrophil migration. Science 287 (2000) 1040-1046
143. Schneider I.C., and Haugh J.M. Quantitative elucidation of a distinct spatial gradient-sensing mechanism in fibroblasts. J. Cell Biol. 171 (2005) 883-892
144. Seppä H., Grotendorst G., Seppa S., Schiffmann E., and Martin G.R. Platelet-derived growth factor in chemotactic for fibroblasts. J. Cell Biol. 92 (1982) 584-588
145. Servant G., Weiner O.D., Neptune E.R., Sedat J.W., and Bourne H.R. Dynamics of a chemoattractant receptor in living neutrophils during chemotaxis. Mol. Biol. Cell 10 (1999) 1163-1178
146. Servant G., Weiner O.D., Herzmark P., Balla T., Sedat J.W., and Bourne H.R. Polarization of chemoattractant receptor signaling during neutrophil chemotaxis. Science 287 (2000) 1037-1040
147. Seveau S., Eddy R.J., Maxfield F.R., and Pierini L.M. Cytoskeleton-dependent membrane domain segregation during neutrophil polarization. Mol. Biol. Cell 12 (2001) 3550-3562
148. Shah K., and Vincent F. Divergent roles of c-Src in controlling platelet-derived growth factor-dependent signaling in fibroblasts. Mol. Biol. Cell 16 (2005) 5418-5432
149. Shamah S.M., Lin M.Z., Goldberg J.L., Estrach S., Sahin M., Hu L., Bazalakova M., Neve R.L., Corfas G., Debant A., and Greenberg M.E. EphA receptors regulate growth cone dynamics through the novel guanine nucleotide exchange factor ephexin. Cell 105 (2001) 233-244
150. Shestakova E.A., Singer R.H., and Condeelis J. The physiological significance of beta-actin mRNA localization in determining cell polarity and directional motility 192. PNAS 98 (2001) 7045-7050
151. Shi S.H., Jan L.Y., and Jan Y.N. Hippocampal neuronal polarity specified by spatially localized mPar3/mPar6 and PI 3-kinase activity. Cell 112 (2003) 63-75
152. Shim S., Goh E.L., Ge S., Sailor K., Yuan J.P., Roderick H.L., Bootman M.D., Worley P.F., Song H., and Ming G.l. XTRPC1-dependent chemotropic guidance of neuronal growth cones. Nat. Neurosci. 8 (2005) 730-735
153. Simpson J.H., Bland K.S., Fetter R.D., and Goodman C.S. Short-range and long-range guidance by slit and its Robo receptors: A combinatorial code of Robo receptors controls lateral position. Cell 103 (2000) 1019-1032
154. Skupsky R., Losert W., and Nossal R.J. Distinguishing modes of eukaryotic gradient sensing. Biophys. J. 89 (2005) 2806-2823
155. Small J.V., Geiger B., Kaverina I., and Bershadsky A. How do microtubules guide migrating cells?. Nat. Rev. Mol. Cell Biol. 3 (2002) 957-964
156. Song H.J., Ming G., and Poo M. cAMP-induced switching in turning direction of nerve growth cones. Nature 388 (1997) 275-279
157. Song H.J., Ming G.L., He Z., Lehmann M., McKerracher L., Tessier-Lavigne M., and Poo M.M. Conversion of neuronal growth cone responses from repulsion to attraction by cyclic nucleotides. Science 281 (1998) 1515-1518
158. Sperry R.W. Chemoaffinity in the orderly growth of nerve fiber patterns and connections. PNAS 50 (1963) 703-710
159. Srinivasan S., Wang F., Glavas S., Ott A., Hofmann F., Aktories K., Kalman D., and Bourne H.R. Rac and Cdc42 play distinct roles in regulating PI(3,4,5)P3 and polarity during neutrophil chemotaxis. J. Cell Biol. 160 (2003) 375-385
160. Strmecki L., Greene D.M., and Pears C.J. Developmental decisions in Dictyostelium discoideum. Dev. Biol. 284 (2005) 25-36
161. Suetsugu S., Yamazaki D., Kurisu S., and Takenawa T. Differential roles of WAVE1 and WAVE2 in dorsal and peripheral ruffle formation for fibroblast cell migration. Dev. Cell 5 (2003) 595-609
162. Swanson J.A., and Taylor D.L. Local and spatially coordinated movements in Dictyostelium discoideum amoebae during chemotaxis. Cell 28 (1982) 225-232
163. Takahashi Y., Morales F.C., Kreimann E.L., and Georgescu M. PTEN tumor suppressor associates with NHERF proteins to attenuate PDGF receptor signaling. EMBO J. 25 (2006) 910-920
164. Tamura M., Gu J., Matsumoto K., Aota S.I., Parsons R., and Yamada K.M. Inhibition of cell migration, spreading, and focal adhesions by tumor suppressor PTEN. Science 280 (1998) 1614-1617
165. Tani T., and Naitoh Y. Chemotactic responses of Dictyostelium discoideum amoebae to a cyclic AMP concentration gradient: Evidence to support a spatial mechanism for sensing cyclic AMP. J. Exp. Biol. 202 (1999) 1-12
166. Tojima T., Akiyama H., Itofusa R., Li Y., Katayama H., Miyawaki A., and Kamiguchi H. Attractive axon guidance involves asymmetric membrane transport and exocytosis in the growth cone. Nat. Neurosci. 10 1 (2007) 58-66
167. Toyofuku T., Yoshida J., Sugimoto T., Zhang H., Kumanogoh A., Hori M., and Kikutani H. FARP2 triggers signals for Sema3A-mediated axonal repulsion 239. Nat. Neurosci. 8 (2005) 1712-1719
168. Van Haastert P.J.M., and Devreotes P.N. Chemotaxis: Signaling the way forward. Nat. Rev. Mol. Cell Biol. 5 (2004) 626-634
169. Van Keymeulen A., Wong K., Knight Z.A., Govaerts C., Hahn K.M., Shokat K.M., and Bourne H.R. To stabilize neutrophil polarity, PIP3 and Cdc42 augment RhoA activity at the back as well as signals at the front. J. Cell Biol. 174 (2006) 437-445
170. Vanhaesebroeck B., Leevers S.J., Ahmadi K., Timms J., Katso R., Driscoll P.C., Woscholski R., Parker P.J., and Waterfield M.D. Synthesis and function of 3-phosphorylated inositol lipids. Annu. Rev. Biochem. 70 (2001) 535-602
171. Vasiliev J.M. Polarization of pseudopodial activities: Cytoskeletal mechanisms. J. Cell Sci. 98 (1991) 1-4
172. Vidali L., Chen F., Cicchetti G., Ohta Y., and Kwiatkowski D.J. Rac1-null mouse embryonic fibroblasts are motile and respond to platelet-derived growth factor. Mol. Biol. Cell 17 (2006) 2377-2390
173. Vielmetter J., Stolze B., Bonhoeffer F., and Stuermer C.A.O. In vitro assay to test differential substrate affinities of growing axons and migratory cells. Exp. Brain Res. 81 (1990) 283-287
174. von Philipsborn A.C., Lang S., Loeschinger J., Bernard A., David C., Lehnert D., Bonhoeffer F., and Bastmeyer M. Growth cone navigation in substrate-bound ephrin gradients. Development 133 (2006) 2487-2495
175. Wadhams G.H., and Armitage J.P. Making sense of it all: Bacterial chemotaxis. Nat. Rev. Mol. Cell Biol. 5 (2004) 1024-1037
176. Wahl S., Barth H., Ciossek T., Aktories K., and Mueller B.K. Ephrin-A5 induces collapse of growth cones by activating rho and rho kinase. J. Cell Biol. 149 (2000) 263-270
177. Walter J., Kern-Veits B., Huf J., Stolze B., and Bonhoeffer F. Recognition of position-specific properties of tectal cell membranes by retinal axons in vitro. Development 101 (1987) 685-696
178. Wang F., Herzmark P., Weiner O.D., Srinivasan S., Servant G., and Bourne H.R. Lipid products of PI(3)Ks maintain persistent cell polarity and directed motility in neutrophils. Nat. Cell Biol. 4 (2002) 513-518
179. Wang G.X., and Poo M.M. Requirement of TRPC channels in netrin-1-induced chemotropic turning of nerve growth cones. Nature 434 (2005) 898-904
180. Weiner O.D., Neilsen P.O., Prestwich G.D., Kirschner M.W., Cantley L.C., and Bourne H.R. A PtdInsP3- and Rho GTPase-mediated positive feedback loop regulates neutrophil polarity. Nat. Cell Biol. 4 (2002) 509-513
181. Weiner O.D., Rentel M., Ott A., Brown G.E., Jedrychowski M., Yaffe M.B., Gygi S.P., Cantley L.C., Bourne H.R., and Kirschner M.W. Hem-1 complexes are essential for Rac activation, actin polymerization, and myosin regulation during neutrophil chemotaxis. Plos Biol. 4 (2006) 186-199
182. Weinl C., Drescher U., Lang S., Bonhoeffer F., and Löschinger J. On the turning of Xenopus retinal axons induced by ephrin-A5. Development 130 (2003) 1635-1643
183. Wen Z., Guirland C., Ming G.I., and Zheng J.Q. A CaMKII/Calcineurin switch controls the direction of Ca2+-dependent growth cone guidance. Neuron 43 (2004) 835-846
184. Williams R.S.B., Boeckeler K., Graf R., Muller-Taubenberger A., Li Z., Isberg R.R., Wessels D., Soll D.R., Alexander H., and Alexander S. Towards a molecular understanding of human diseases using Dictyostelium discoideum. Trends Mol. Med. 12 (2006) 415-424
185. Wong E.V., Kerner J.A., and Jay D.G. Convergent and divergent signaling mechanisms of growth cone collapse by ephrinA5 and slit2. J. Neurobiol. 59 (2004) 66-81
186. Wong K., Ren X.R., Huang Y.Z., Xie Y., Liu G., Saito H., Tang H., Wen L., Brady-Kalnay S.M., and Mei L. Signal transduction in neuronal migration: Roles of GTPase activating proteins and the small GTPase Cdc42 in the slit-robo pathway. Cell 107 (2001) 209-221
187. Wong K., Pertz O., Hahn K., and Bourne H. Neutrophil polarization: Spatiotemporal dynamics of RhoA activity support a self-organizing mechanism. PNAS 103 (2006) 3639-3644
188. Wu K.Y., Hengst U., Cox L.J., Macosko E.Z., Jeromin A., Urquhart E.R., and Jaffrey S.R. Local translation of RhoA regulates growth cones collapse. Nature 436 (2005) 1020-1024
189. Xiao Z., Zhang N., Murphy D.B., and Devreotes P.N. Dynamic distribution of chemoattractant receptors in living cells during chemotaxis and persistent stimulation. J. Cell Biol. 139 (1997) 365-374
190. Xu J., Wang F., Van Keymeulen A., Herzmark P., Straight A., Kelly K., Takuwa Y., Sugimoto N., Mitchison T., and Bourne H.R. Divergent signals and cytoskeletal assemblies regulate self-organizing polarity in neutrophils. Cell 114 (2003) 201-214
191. Xu J., Wang F., Van Keymeulen A., Rentel M., and Bourne H.R. Neutrophil microtubules suppress polarity and enhance directional migration. PNAS 102 (2005) 6884-6889
192. Xu X., Meier-Schellersheim M., Jiao X., Nelson L.E., and Jin T. Quantitative imaging of single live cells reveals spatiotemporal dynamics of multistep signaling events of chemoattractant gradient sensing in dictyostelium. Mol. Biol. Cell 16 (2005) 676-688
193. Yang L., and Bashaw G.J. Son of sevenless directly links the Robo receptor to Rac activation to control axon repulsion at the midline. Neuron 52 (2006) 595-607
194. Yang S., and Huang X.Y. Ca2+ Influx through L-type Ca2+ channels controls the trailing tail contraction in growth factor-induced fibroblast cell migration. J. Biol. Chem. 280 (2005) 27130-27137
195. Yao J., Sasaki Y., Wen Z., Bassell G.J., and Zheng J.Q. An essential role for [beta]-actin mRNA localization and translation in Ca2+-dependent growth cone guidance. Nat. Neurosci. 9 (2006) 1265-1273
196. Yates P.A., Holub A.D., McLaughlin T., Sejnowski T.J., and O'Leary D.D.M. Computational modeling of retinotopic map development to define contributions of EphA-EphrinA gradients, axon-axon interactions, and patterned activity. J. Neurobiol. 59 (2004) 95-113
197. Yuan X.B., Jin M., Xu X., Song Y.Q., Wu C.P., Poo M.M., and Duan S. Signaling and crosstalk of Rho GTPases in mediating axon guidance. Nat. Cell Biol. 5 (2003) 38-45
198. Yumura S., Furuya K., and Takeuchi I. Intracellular free calcium responses during chemotaxis of Dictyostelium cells. J. Cell Sci. 109 (1996) 2673-2678
199. Zheng J.Q. Turning of nerve growth cones induced by localized increases in intracellular calcium ions. Nature 403 (2000) 89-93
200. Zheng J.Q., Felder M., Connor J.A., and Poo M.M. Turning of nerve growth cones induced by neurotransmitters. Nature 368 (1994) 140-144
201. Zheng J.Q., Wan J.J., and Poo M.M. Essential role of filopodia in chemotropic turning of nerve growth cone induced by a glutamate gradient. J. Neurosci. 16 (1996) 1140-1149
202. Zhou F., Waterman-Storer C.M., and Cohan C.S. Focal loss of actin bundles causes microtubule redistribution and growth cone turning. J. Cell Biol. 157 (2002) 839-849
203. Zhou F.Q., Zhou J., Dedhar S., Wu Y.H., and Snider W.D. NGF-induced axon growth is mediated by localized inactivation of GSK-3[beta] and functions of the microtubule plus end binding protein APC. Neuron 42 (2004) 897-912
204. Zigmond S.H. Mechanisms of sensing chemical gradients by polymorphonuclear leukocytes. Nature 249 (1974) 450-452
205. Zigmond S.H. Ability of polymorphonuclear leukocytes to orient in gradients of chemotactic factors. J. Cell Biol. 75 (1977) 606-616
206. Zigmond S.H., and Sullivan S.J. Sensory adaptation of leukocytes to chemotactic peptides. J. Cell Biol. 82 (1979) 517-527
207. Zigmond S.H., Levitsky H.I., and Kreel B.J. Cell polarity: An examination of its behavioral expression and its consequences for polymorphonuclear leukocyte chemotaxis. J. Cell Biol. 89 (1981) 585-592