Signaling to cytoskeletal dynamics during chemotaxis.

We review insights in signaling pathways controlling cell polarization and cytoskeletal organization during chemotactic movement in Dictyostelium amoebae and neutrophils. We compare and contrast these insights with our current understanding of pathways controlling chemotactic movements in more-complex multicellular developmental contexts.

[1]  P. Rørth,et al.  Invasive cell migration is initiated by guided growth of long cellular extensions , 2002, Nature Cell Biology.

[2]  N. Perrimon,et al.  The nonreceptor protein tyrosine phosphatase corkscrew functions in multiple receptor tyrosine kinase pathways in Drosophila. , 1996, Developmental biology.

[3]  Marc W. Kirschner,et al.  A PtdInsP3- and Rho GTPase-mediated positive feedback loop regulates neutrophil polarity , 2002, Nature Cell Biology.

[4]  K. Manova,et al.  The Docking Protein FRS2α Is an Essential Component of Multiple Fibroblast Growth Factor Responses during Early Mouse Development , 2005, Molecular and Cellular Biology.

[5]  J. Casanova,et al.  The alternative migratory pathways of the Drosophila tracheal cells are associated with distinct subsets of mesodermal cells. , 2000, Developmental biology.

[6]  M. Kirschner,et al.  Expression of a dominant negative mutant of the FGF receptor disrupts mesoderm formation in xenopus embryos , 1991, Cell.

[7]  A. Kimmel,et al.  Breaking symmetries: regulation of Dictyostelium development through chemoattractant and morphogen signal-response. , 2004, Current opinion in genetics & development.

[8]  R. Lehmann,et al.  The chemokine SDF1/CXCL12 and its receptor CXCR4 regulate mouse germ cell migration and survival , 2003, Development.

[9]  M. Affolter,et al.  Genetic Control of Cell Intercalation during Tracheal Morphogenesis in Drosophila , 2004, Current Biology.

[10]  C. Saxe,et al.  SCAR, a WASP-related Protein, Isolated as a Suppressor of Receptor Defects in Late Dictyostelium Development , 1998, The Journal of cell biology.

[11]  I. Mason,et al.  Expression of Fgf4 during early development of the chick embryo , 1999, Mechanisms of Development.

[12]  J. Spudich,et al.  Disruption of the Dictyostelium myosin heavy chain gene by homologous recombination. , 1987, Science.

[13]  M. Leptin,et al.  FGF signalling and the mechanism of mesoderm spreading in Drosophila embryos , 2005, Development.

[14]  D. Soll,et al.  Phosphorylation of the Dictyostelium myosin II heavy chain is necessary for maintaining cellular polarity and suppressing turning during chemotaxis. , 1998, Cell motility and the cytoskeleton.

[15]  N. Ueno,et al.  PKC delta is essential for Dishevelled function in a noncanonical Wnt pathway that regulates Xenopus convergent extension movements. , 2003, Genes & development.

[16]  Xufeng Wu,et al.  The Dictyostelium Carmil Protein Links Capping Protein and the Arp2/3 Complex to Type I Myosins through Their Sh3 Domains , 2001, The Journal of cell biology.

[17]  Emerald Huang,et al.  Dictyostelium PAKc is required for proper chemotaxis. , 2004, Molecular biology of the cell.

[18]  P. Devreotes,et al.  Eukaryotic Chemotaxis: Distinctions between Directional Sensing and Polarization* , 2003, Journal of Biological Chemistry.

[19]  E. Raz.  Guidance of primordial germ cell migration. , 2004, Current opinion in cell biology.

[20]  Yoichi Kato,et al.  Wnt/Frizzled Activation of Rho Regulates Vertebrate Gastrulation and Requires a Novel Formin Homology Protein Daam1 , 2001, Cell.

[21]  M. Affolter,et al.  In vivo imaging reveals different cellular functions for FGF and Dpp signaling in tracheal branching morphogenesis. , 2002, Developmental cell.

[22]  S. Gygi,et al.  Toca-1 Mediates Cdc42-Dependent Actin Nucleation by Activating the N-WASP-WIP Complex , 2004, Cell.

[23]  Charles Boone,et al.  Formins: signaling effectors for assembly and polarization of actin filaments , 2003, Journal of Cell Science.

[24]  Cornelis J. Weijer,et al.  Visualizing Signals Moving in Cells , 2003, Science.

[25]  P. Adler,et al.  Planar signaling and morphogenesis in Drosophila. , 2002, Developmental cell.

[26]  V. Litvak,et al.  Sprouty Fine-Tunes EGF Signaling through Interlinked Positive and Negative Feedback Loops , 2003, Current Biology.

[27]  K. Anderson,et al.  Essential Role of Glycosaminoglycans in Fgf Signaling during Mouse Gastrulation , 2003, Cell.

[28]  E. Voss,et al.  Computer-assisted analysis of filopod formation and the role of myosin II heavy chain phosphorylation in Dictyostelium , 2005, Journal of Cell Science.

[29]  C J Weijer,et al.  cAMP receptor affinity controls wave dynamics, geometry and morphogenesis in Dictyostelium. , 2001, Journal of cell science.

[30]  R. Chisholm,et al.  During multicellular migration, myosin ii serves a structural role independent of its motor function. , 2001, Developmental biology.

[31]  M. Mercola,et al.  Embryonic mesoderm cells spread in response to platelet-derived growth factor and signaling by phosphatidylinositol 3-kinase. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[32]  C. Heisenberg,et al.  Phosphoinositide 3-Kinase Is Required for Process Outgrowth and Cell Polarization of Gastrulating Mesendodermal Cells , 2003, Current Biology.

[33]  C. Samakovlis,et al.  Drosophila tracheal morphogenesis: intricate cellular solutions to basic plumbing problems. , 2003, Trends in cell biology.

[34]  Y. Yarden,et al.  Negative regulation of receptor tyrosine kinases: unexpected links to c-Cbl and receptor ubiquitylation , 2005, Cell Research.

[35]  P. Devreotes,et al.  Tumor Suppressor PTEN Mediates Sensing of Chemoattractant Gradients , 2002, Cell.

[36]  P. Rørth,et al.  Guidance of cell migration by EGF receptor signaling during Drosophila oogenesis. , 2001, Science.

[37]  D. Soll,et al.  A novel cGMP signalling pathway mediating myosin phosphorylation and chemotaxis in Dictyostelium , 2002, EMBO Journal.

[38]  P. Devreotes,et al.  Chemotaxis: signalling the way forward , 2004, Nature Reviews Molecular Cell Biology.

[39]  M. Meier-Schellersheim,et al.  Quantitative imaging of single live cells reveals spatiotemporal dynamics of multistep signaling events of chemoattractant gradient sensing in Dictyostelium. , 2004, Molecular biology of the cell.

[40]  H. Müller,et al.  FGF8-like1 and FGF8-like2 Encode Putative Ligands of the FGF Receptor Htl and Are Required for Mesoderm Migration in the Drosophila Gastrula , 2004, Current Biology.

[41]  Marten Postma,et al.  Chemotaxis: signalling modules join hands at front and tail , 2004, EMBO reports.

[42]  Laura M. Machesky,et al.  Scar1 and the related Wiskott–Aldrich syndrome protein, WASP, regulate the actin cytoskeleton through the Arp2/3 complex , 1998, Current Biology.

[43]  J. Faix,et al.  DGAP1, a homologue of rasGTPase activating proteins that controls growth, cytokinesis, and development in Dictyostelium discoideum , 1996, FEBS letters.

[44]  Wei Lu,et al.  Directional Sensing Requires Gβγ-Mediated PAK1 and PIXα-Dependent Activation of Cdc42 , 2003, Cell.

[45]  R. Schuh,et al.  Single mesodermal cells guide outgrowth of ectodermal tubular structures in Drosophila. , 2000, Genes & development.

[46]  S. Zigmond.  Formin-induced nucleation of actin filaments. , 2004, Current opinion in cell biology.

[47]  Kenji Nakamura,et al.  Rac1 is required for the formation of three germ layers during gastrulation , 1998, Oncogene.

[48]  A. Noegel,et al.  The Dictyostelium discoideum family of Rho-related proteins. , 2001, Nucleic acids research.

[49]  G. Schoenwolf,et al.  Classification scheme for genes expressed during formation and progression of the avian primitive streak , 2001, The Anatomical record.

[50]  P. Rørth.  Communication by Touch Role of Cellular Extensions in Complex Animals , 2003, Cell.

[51]  D. Murphy,et al.  G Protein Signaling Events Are Activated at the Leading Edge of Chemotactic Cells , 1998, Cell.

[52]  R. Ladher,et al.  Comparison of the expression patterns of several fibroblast growth factors during chick gastrulation and neurulation , 2002, Anatomy and Embryology.

[53]  C. Holt,et al.  Xenopus Sprouty2 inhibits FGF-mediated gastrulation movements but does not affect mesoderm induction and patterning. , 2001, Genes & development.

[54]  J. Rossant,et al.  Chimeric analysis of fibroblast growth factor receptor-1 (Fgfr1) function: a role for FGFR1 in morphogenetic movement through the primitive streak. , 1997, Development.

[55]  R. Insall,et al.  Control of SCAR activity in Dictyostelium discoideum. , 2004, Biochemical Society transactions.

[56]  R. Schuh,et al.  Drosophila tracheal system formation involves FGF‐dependent cell extensions contacting bridge‐cells , 2002, EMBO reports.

[57]  C. MacArthur,et al.  Receptor Specificity of the Fibroblast Growth Factor Family* , 1996, The Journal of Biological Chemistry.

[58]  C. Nüsslein-Volhard,et al.  A zebrafish homologue of the chemokine receptor Cxcr4 is a germ-cell guidance receptor , 2003, Nature.

[59]  E. Raz,et al.  Autonomous modes of behavior in primordial germ cell migration. , 2004, Developmental cell.

[60]  T. Egelhoff,et al.  Biochemical characterization of a Dictyostelium myosin II heavy-chain phosphatase that promotes filament assembly. , 1999, European journal of biochemistry.

[61]  U. Tepass,et al.  DE-Cadherin Is Required for Intercellular Motility during Drosophila Oogenesis , 1999, The Journal of cell biology.

[62]  J. Segall,et al.  Epidermal growth factor receptor distribution during chemotactic responses. , 2000, Molecular biology of the cell.

[63]  M. Frasch,et al.  pyramus and thisbe: FGF genes that pattern the mesoderm of Drosophila embryos. , 2004, Genes & development.

[64]  Gun-Hwa Kim,et al.  JNK and ROKα function in the noncanonical Wnt/RhoA signaling pathway to regulate Xenopus convergent extension movements , 2005, Developmental dynamics : an official publication of the American Association of Anatomists.

[65]  B. Shilo,et al.  breathless, a Drosophila FGF receptor homolog, is essential for migration of tracheal and specific midline glial cells. , 1992, Genes & development.

[66]  John S. Condeelis,et al.  Cofilin Promotes Actin Polymerization and Defines the Direction of Cell Motility , 2004, Science.

[67]  G. Shaulsky,et al.  LagC is required for cell-cell interactions that are essential for cell-type differentiation in Dictyostelium. , 1994, Genes & development.

[68]  V. Tarabykin,et al.  Primordial germ cell migration in the chick and mouse embryo: the role of the chemokine SDF-1/CXCL12. , 2004, Developmental biology.

[69]  C. Weijer,et al.  A temperature‐sensitive adenylyl cyclase mutant of Dictyostelium , 2000, The EMBO journal.

[70]  B. S. Baker,et al.  Sex-Specific Deployment of FGF Signaling in Drosophila Recruits Mesodermal Cells into the Male Genital Imaginal Disc , 2002, Cell.

[71]  K. Hahn,et al.  Designing biosensors for Rho family proteins — deciphering the dynamics of Rho family GTPase activation in living cells , 2004, Journal of Cell Science.

[72]  J. Xu,et al.  Neutrophil microtubules suppress polarity and enhance directional migration. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[73]  D. Montell,et al.  Border-cell migration: the race is on , 2003, Nature Reviews Molecular Cell Biology.

[74]  P. Rørth,et al.  Evidence for tension-based regulation of Drosophila MAL and SRF during invasive cell migration. , 2004, Developmental cell.

[75]  M. Affolter,et al.  The Drosophila protein Dof is specifically required for FGF signaling. , 1998, Molecular cell.

[76]  D. Barber,et al.  Cell migration requires both ion translocation and cytoskeletal anchoring by the Na-H exchanger NHE1 , 2002, The Journal of cell biology.

[77]  D. Montell,et al.  A Role for Drosophila IAP1-Mediated Caspase Inhibition in Rac-Dependent Cell Migration , 2004, Cell.

[78]  H. Hamm,et al.  Essential roles of Gα12/13 signaling in distinct cell behaviors driving zebrafish convergence and extension gastrulation movements , 2005, The Journal of cell biology.

[79]  K. Inouye,et al.  Talin B is required for force transmission in morphogenesis of Dictyostelium , 2004, The EMBO journal.

[80]  R. Firtel,et al.  Requirement of a Vasodilator-stimulated Phosphoprotein Family Member for Cell Adhesion, the Formation of Filopodia, and Chemotaxis in Dictyostelium* 210 , 2002, The Journal of Biological Chemistry.

[81]  C J Weijer,et al.  The role of the cortical cytoskeleton: F-actin crosslinking proteins protect against osmotic stress, ensure cell size, cell shape and motility, and contribute to phagocytosis and development. , 1996, Journal of cell science.

[82]  T. Yanagida,et al.  Single-Molecule Analysis of Chemotactic Signaling in Dictyostelium Cells , 2001, Science.

[83]  T. Pawson,et al.  Morphogenetic movements at gastrulation require the SH2 tyrosine phosphatase Shp2. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[84]  D R Soll,et al.  Computer-assisted three-dimensional reconstruction and motion analysis of living, crawling cells. , 1999, Computerized medical imaging and graphics : the official journal of the Computerized Medical Imaging Society.

[85]  J. Spudich,et al.  A novel positive selection for identifying cold-sensitive myosin II mutants in Dictyostelium. , 1995, Genetics.

[86]  T. Uyeda,et al.  ForC, a novel type of formin family protein lacking an FH1 domain, is involved in multicellular development in Dictyostelium discoideum , 2003, Journal of Cell Science.

[87]  T. Meyer,et al.  A local coupling model and compass parameter for eukaryotic chemotaxis. , 2005, Developmental cell.

[88]  K. Hahn,et al.  Spatial and Temporal Analysis of Rac Activation during Live Neutrophil Chemotaxis , 2002, Current Biology.

[89]  J. Spudich,et al.  Differential localization in cells of myosin II heavy chain kinases during cytokinesis and polarized migration , 2002, BMC Cell Biology.

[90]  R. Winklbauer,et al.  Establishment of substratum polarity in the blastocoel roof of the Xenopus embryo. , 1999, Development.

[91]  D. Montell,et al.  Myosin VI is required for E-cadherin-mediated border cell migration , 2002, Nature Cell Biology.

[92]  C. Parent,et al.  Making all the right moves: chemotaxis in neutrophils and Dictyostelium. , 2004, Current opinion in cell biology.

[93]  P. Rørth.  Initiating and guiding migration: lessons from border cells. , 2002, Trends in cell biology.

[94]  D. Knecht,et al.  Mutants lacking myosin II cannot resist forces generated during multicellular morphogenesis. , 1995, Journal of cell science.

[95]  J. Rossant,et al.  Expression of the fibroblast growth factor receptor FGFR-1/flg during gastrulation and segmentation in the mouse embryo. , 1992, Developmental biology.

[96]  J. Segall,et al.  Local signaling by the EGF receptor , 2003, The Journal of cell biology.

[97]  Richard A. Firtel,et al.  Spatial and Temporal Regulation of 3-Phosphoinositides by PI 3-Kinase and PTEN Mediates Chemotaxis , 2002, Cell.

[98]  W. Loomis,et al.  Disruption of the gene encoding the cell adhesion molecule DdCAD-1 leads to aberrant cell sorting and cell-type proportioning during Dictyostelium development. , 2002, Development.

[99]  S. Diez,et al.  Dynamic Actin Patterns and Arp2/3 Assembly at the Substrate-Attached Surface of Motile Cells , 2004, Current Biology.

[100]  H. Meinhardt.  Orientation of chemotactic cells and growth cones: models and mechanisms. , 1999, Journal of cell science.

[101]  W. Loomis,et al.  The membrane glycoprotein gp150 is encoded by the lagC gene and mediates cell-cell adhesion by heterophilic binding during Dictyostelium development. , 2000, Developmental biology.

[102]  A. Hall,et al.  Cell migration: Rho GTPases lead the way. , 2004, Developmental biology.

[103]  G. Gerisch,et al.  Cytoskeletons from a mutant of Dictyostelium discoideum with flattened cells. , 1986, Journal of cell science.

[104]  J. Condeelis,et al.  Measurement of barbed ends, actin polymerization, and motility in live carcinoma cells after growth factor stimulation. , 2004, Cell motility and the cytoskeleton.

[105]  P. Leder,et al.  Murine FGFR-1 is required for early postimplantation growth and axial organization. , 1994, Genes & development.

[106]  G. Laevsky,et al.  Cross-linking of actin filaments by myosin II is a major contributor to cortical integrity and cell motility in restrictive environments , 2003, Journal of Cell Science.

[107]  P. Finan,et al.  Regulation of P-Rex1 by Phosphatidylinositol (3,4,5)-Trisphosphate and Gβγ Subunits* , 2005, Journal of Biological Chemistry.

[108]  D. Montell,et al.  Requirement for Par-6 and Bazooka in Drosophila border cell migration , 2004, Development.

[109]  D. Barber,et al.  A developmentally regulated Na-H exchanger in Dictyostelium discoideum is necessary for cell polarity during chemotaxis , 2005, The Journal of cell biology.

[110]  R. Firtel,et al.  Paka, a Putative Pak Family Member, Is Required for Cytokinesis and the Regulation of the Cytoskeleton in Dictyostelium discoideum Cells during Chemotaxis , 1999, The Journal of cell biology.

[111]  C J Weijer,et al.  Propagating chemoattractant waves coordinate periodic cell movement in Dictyostelium slugs. , 2001, Development.

[112]  Ivan Dikic,et al.  Negative receptor signalling. , 2003, Current opinion in cell biology.

[113]  D. Meyer,et al.  Guidance of Primordial Germ Cell Migration by the Chemokine SDF-1 , 2002, Cell.

[114]  Xi He,et al.  Coactivation of Rac and Rho by Wnt/Frizzled signaling is required for vertebrate gastrulation. , 2003, Genes & development.

[115]  T. Egelhoff,et al.  Actin Activation of Myosin Heavy Chain Kinase A in Dictyostelium , 2005, Journal of Biological Chemistry.

[116]  R. Insall,et al.  PIR121 Regulates Pseudopod Dynamics and SCAR Activity in Dictyostelium , 2003, Current Biology.

[117]  R. Firtel,et al.  The Dictyostelium LIM domain-containing protein LIM2 is essential for proper chemotaxis and morphogenesis. , 2000, Molecular biology of the cell.

[118]  M. Krasnow,et al.  Genetic control of branching morphogenesis. , 1999, Science.

[119]  Christof Niehrs,et al.  Fibroblast growth factor signaling during early vertebrate development. , 2005, Endocrine reviews.

[120]  Y. Matsui,et al.  Impaired colonization of the gonads by primordial germ cells in mice lacking a chemokine, stromal cell-derived factor-1 (SDF-1) , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[121]  P. Devreotes,et al.  Two phases of actin polymerization display different dependencies on PI(3,4,5)P3 accumulation and have unique roles during chemotaxis. , 2003, Molecular biology of the cell.

[122]  Jingsong Xu,et al.  Divergent Signals and Cytoskeletal Assemblies Regulate Self-Organizing Polarity in Neutrophils , 2003, Cell.

[123]  E. Raz,et al.  Signaling pathways controlling primordial germ cell migration in zebrafish , 2004, Journal of Cell Science.

[124]  F. Rivero,et al.  Signal transduction pathways regulated by Rho GTPases in Dictyostelium , 2004, Journal of Muscle Research & Cell Motility.

[125]  M. Metzstein,et al.  Branching morphogenesis of the Drosophila tracheal system. , 2003, Annual review of cell and developmental biology.

[126]  G. Spiegelman,et al.  Chemoattractant‐induced Ras activation during Dictyostelium aggregation , 2004, EMBO reports.

[127]  G. Côté,et al.  Regulation of Dictyostelium myosin I and II. , 2001, Biochimica et biophysica acta.

[128]  Tetsuya Muramoto,et al.  A comparative sequence analysis reveals a common GBD/FH3-FH1-FH2-DAD architecture in formins from Dictyostelium, fungi and metazoa , 2005, BMC Genomics.

[129]  M. Affolter,et al.  Downstream-of-FGFR Is a Fibroblast Growth Factor-Specific Scaffolding Protein and Recruits Corkscrew upon Receptor Activation , 2004, Molecular and Cellular Biology.

[130]  J. Spudich,et al.  Chemoattractant-elicited increases in Dictyostelium myosin phosphorylation are due to changes in myosin localization and increases in kinase activity. , 1987, The Journal of biological chemistry.

[131]  J. Ng,et al.  Rac promotes epithelial cell rearrangement during tracheal tubulogenesis in Drosophila , 2003, Development.

[132]  Scott E Fraser,et al.  Convergent extension: the molecular control of polarized cell movement during embryonic development. , 2002, Developmental Cell.

[133]  S. Chapman,et al.  Analysis of spatial and temporal gene expression patterns in blastula and gastrula stage chick embryos. , 2002, Developmental biology.

[134]  Jin-Kwan Han,et al.  Xenopus Cdc42 regulates convergent extension movements during gastrulation through Wnt/Ca2+ signaling pathway. , 2002, Developmental biology.

[135]  T. Soldati.  Unconventional Myosins, Actin Dynamics and Endocytosis: A Ménage à Trois? , 2003, Traffic.

[136]  G. Martin,et al.  Targeted disruption of Fgf8 causes failure of cell migration in the gastrulating mouse embryo. , 1999, Genes & development.

[137]  M. Chou,et al.  PDGF signalling is required for gastrulation of Xenopus laevis. , 1995, Development.

[138]  R. Insall,et al.  Solving the WAVE function , 2004, Nature Cell Biology.

[139]  R. Firtel,et al.  A Dictyostelium homologue of WASP is required for polarized F-actin assembly during chemotaxis. , 2005, Molecular biology of the cell.

[140]  J. Rossant,et al.  FGF signaling regulates mesoderm cell fate specification and morphogenetic movement at the primitive streak. , 2001, Developmental cell.

[141]  P. Iglesias,et al.  Chemoattractant-induced phosphatidylinositol 3,4,5-trisphosphate accumulation is spatially amplified and adapts, independent of the actin cytoskeleton , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[142]  M. Kirschner,et al.  The Interaction between N-WASP and the Arp2/3 Complex Links Cdc42-Dependent Signals to Actin Assembly , 1999, Cell.

[143]  D. Dormann,et al.  Simultaneous quantification of cell motility and protein-membrane-association using active contours. , 2002, Cell motility and the cytoskeleton.

[144]  Jun Wang,et al.  Regulation of cell-cell adhesion during Dictyostelium development. , 2004, Seminars in cell & developmental biology.

[145]  N. Xylourgidis,et al.  Attractive and repulsive functions of Slit are mediated by different receptors in the Drosophila trachea. , 2002, Development.

[146]  G. Borisy,et al.  Cell Migration: Integrating Signals from Front to Back , 2003, Science.

[147]  Francisca Vazquez,et al.  Novel Mechanism of PTEN Regulation by Its Phosphatidylinositol 4,5-Bisphosphate Binding Motif Is Critical for Chemotaxis* , 2004, Journal of Biological Chemistry.

[148]  Ray Keller,et al.  Shaping the Vertebrate Body Plan by Polarized Embryonic Cell Movements , 2002, Science.

[149]  N. Hacohen,et al.  Development of the Drosophila tracheal system occurs by a series of morphologically distinct but genetically coupled branching events. , 1996, Development.

[150]  Alexandre V. Podtelejnikov,et al.  Mechanism of regulation of WAVE1-induced actin nucleation by Rac1 and Nck , 2002, Nature.

[151]  Makoto Sato,et al.  FGF is an essential mitogen and chemoattractant for the air sacs of the drosophila tracheal system. , 2002, Developmental cell.

[152]  D. Murphy,et al.  Dynamic Distribution of Chemoattractant Receptors in Living Cells During Chemotaxis and Persistent Stimulation , 1997, The Journal of cell biology.

[153]  J. Rossant,et al.  Promotion of trophoblast stem cell proliferation by FGF4. , 1998, Science.

[154]  D. Lauffenburger,et al.  Cell Migration: A Physically Integrated Molecular Process , 1996, Cell.

[155]  Thomas D Pollard,et al.  Cellular Motility Driven by Assembly and Disassembly of Actin Filaments , 2003, Cell.

[156]  D. Montell,et al.  PVF1, a PDGF/VEGF homolog, is sufficient to guide border cells and interacts genetically with Taiman , 2003, Development.

[157]  D. Dormann,et al.  Visualizing PI3 Kinase-Mediated Cell-Cell Signaling during Dictyostelium Development , 2002, Current Biology.

[158]  Paul Herzmark,et al.  Lipid products of PI(3)Ks maintain persistent cell polarity and directed motility in neutrophils , 2002, Nature Cell Biology.

[159]  Cornelis J Weijer,et al.  Cell movement patterns during gastrulation in the chick are controlled by positive and negative chemotaxis mediated by FGF4 and FGF8. , 2002, Developmental cell.

[160]  P. Rørth,et al.  Guidance of Cell Migration by the Drosophila PDGF/VEGF Receptor , 2001, Cell.

[161]  R. Firtel,et al.  Role of Rac in controlling the actin cytoskeleton and chemotaxis in motile cells. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[162]  K. Yahata,et al.  A unique talin homologue with a villin headpiece-like domain is required for multicellular morphogenesis in Dictyostelium , 1999, Current Biology.

[163]  V. Papaioannou,et al.  Requirement of FGF-4 for postimplantation mouse development , 1995, Science.

[164]  Dianqing Wu,et al.  Neutrophils lacking phosphoinositide 3-kinase γ show loss of directionality during N-formyl-Met-Leu-Phe-induced chemotaxis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[165]  D. Dormann,et al.  In vivo analysis of 3-phosphoinositide dynamics during Dictyostelium phagocytosis and chemotaxis , 2004, Journal of Cell Science.

[166]  Fabio Apone,et al.  Rac regulation of chemotaxis and morphogenesis in Dictyostelium , 2004, The EMBO journal.

[167]  J. Spudich,et al.  Chemoattractant-elicited increases in myosin phosphorylation in dictyostelium , 1985, Cell.

[168]  J. Condeelis,et al.  Transduction of the chemotactic signal to the actin cytoskeleton of Dictyostelium discoideum. , 1989, Developmental biology.

[169]  Stephen S. Gisselbrecht,et al.  heartless encodes a fibroblast growth factor receptor (DFR1/DFGF-R2) involved in the directional migration of early mesodermal cells in the Drosophila embryo. , 1996, Genes & development.

[170]  Emilios Tahinci,et al.  Guidance of mesoderm cell migration in the Xenopus gastrula requires PDGF signaling , 2004, Development.

[171]  R. Firtel,et al.  Receptor-mediated regulation of PI3Ks confines PI(3,4,5)P3 to the leading edge of chemotaxing cells. , 2003, Molecular biology of the cell.

[172]  Emilios Tahinci,et al.  Distinct functions of Rho and Rac are required for convergent extension during Xenopus gastrulation. , 2003, Developmental biology.

[173]  T. Bretschneider,et al.  Differential localization of the Dictyostelium kinase DPAKa during cytokinesis and cell migration , 2004, Journal of Muscle Research & Cell Motility.

[174]  T. Pawson,et al.  The SH2 tyrosine phosphatase Shp2 is required for mammalian limb development , 2000, Nature Genetics.

[175]  J. Faix,et al.  Rac1 GTPases control filopodia formation, cell motility, endocytosis, cytokinesis and development in Dictyostelium. , 2000, Journal of cell science.

[176]  M. Leptin,et al.  A Functional Domain of Dof That Is Required for Fibroblast Growth Factor Signaling , 2004, Molecular and Cellular Biology.

[177]  Richard A. Firtel,et al.  Localized Ras signaling at the leading edge regulates PI3K, cell polarity, and directional cell movement , 2004, The Journal of cell biology.

[178]  R. Firtel,et al.  Control of cell polarity and chemotaxis by Akt/PKB and PI3 kinase through the regulation of PAKa. , 2001, Molecular cell.

[179]  Van Haastert.  Sensory adaptation of Dictyostelium discoideum cells to chemotactic signals , 1983, The Journal of cell biology.

[180]  D. Soll,et al.  RasGEF-containing proteins GbpC and GbpD have differential effects on cell polarity and chemotaxis in Dictyostelium , 2005, Journal of Cell Science.

[181]  Nobuyuki Itoh,et al.  Tube or not tube: remodeling epithelial tissues by branching morphogenesis. , 2003, Developmental cell.

[182]  T. Pawson,et al.  Abnormal mesoderm patterning in mouse embryos mutant for the SH2 tyrosine phosphatase Shp‐2 , 1997, The EMBO journal.

[183]  C. Huang,et al.  Roles of PI3K in neutrophil function. , 2004, Current topics in microbiology and immunology.

[184]  Richard A. Firtel,et al.  Role of Phosphatidylinositol 3′ Kinase and a Downstream Pleckstrin Homology Domain–Containing Protein in Controlling Chemotaxis inDictyostelium , 2001, The Journal of cell biology.

[185]  M. Affolter,et al.  Specificity of FGF signaling in cell migration in Drosophila. , 2001, Development.

[186]  J. Rossant,et al.  fgfr-1 is required for embryonic growth and mesodermal patterning during mouse gastrulation. , 1994, Genes & development.

[187]  Rong Zeng,et al.  Regulation of PTEN by Rho small GTPases , 2005, Nature Cell Biology.

[188]  J. Sivak,et al.  FGF signal interpretation is directed by Sprouty and Spred proteins during mesoderm formation. , 2005, Developmental cell.

[189]  M. Krasnow,et al.  branchless Encodes a Drosophila FGF Homolog That Controls Tracheal Cell Migration and the Pattern of Branching , 1996, Cell.

[190]  P. Devreotes,et al.  Receptor-Mediated Activation of Heterotrimeric G-Proteins in Living Cells , 2001, Science.

[191]  P. Devreotes,et al.  Temporal and spatial regulation of chemotaxis. , 2002, Developmental cell.