Growth cone guidance: first steps towards a deeper understanding.

Growth cones, the hand-like structures at the tip of growing neurites, possess remarkable abilities to detect directional cues. On their way to their targets they traverse a dense jungle of many different cells, expressing a variety of different molecular guidance cues. Proper reading and integration of these cues is essential for precise wiring of different parts of the peripheral and central nervous systems. Guidance cues have been classified according to the response they elicit as either attractive or repulsive. Recent work, however, suggests that this might not represent an absolute distinction and that the internal state of the growth cone can dictate whether it detects a cue as repulsive or attractive. This article reviews some new experimental approaches to understanding growth cone signal transduction mechanisms induced by extracellular guidance cues.

[1]  S. Kenwrick,et al.  Neural cell recognition molecule L1: from cell biology to human hereditary brain malformations , 1998, Current Opinion in Neurobiology.

[2]  Jonas Frisén,et al.  Ephrin-A5 (AL-1/RAGS) Is Essential for Proper Retinal Axon Guidance and Topographic Mapping in the Mammalian Visual System , 1998, Neuron.

[3]  C. Chien Why Does the Growth Cone Cross the Road? , 1998, Neuron.

[4]  A. Hall,et al.  Rho GTPases and the actin cytoskeleton. , 1998, Science.

[5]  Marc Tessier-Lavigne,et al.  Roundabout Controls Axon Crossing of the CNS Midline and Defines a Novel Subfamily of Evolutionarily Conserved Guidance Receptors , 1998, Cell.

[6]  Jennifer A Zallen,et al.  The Conserved Immunoglobulin Superfamily Member SAX-3/Robo Directs Multiple Aspects of Axon Guidance in C. elegans , 1998, Cell.

[7]  F. Murakami,et al.  Change in chemoattractant responsiveness of developing axons at an intermediate target. , 1998, Science.

[8]  Yoshimi Takai,et al.  Induction of filopodium formation by a WASP-related actin-depolymerizing protein N-WASP , 1998, Nature.

[9]  A. Gierer Possible involvement of gradients in guidance of receptor cell axons towards their target position on the olfactory bulb , 1998, The European journal of neuroscience.

[10]  R. Guillery,et al.  Errors in corticospinal axon guidance in mice lacking the neural cell adhesion molecule L1 , 1998, Current Biology.

[11]  A. Davies,et al.  Met receptor signaling is required for sensory nerve development and HGF promotes axonal growth and survival of sensory neurons. , 1997, Genes & development.

[12]  C. Métin,et al.  A role for netrin-1 in the guidance of cortical efferents. , 1997, Development.

[13]  M. A. Barry,et al.  Semaphorin III can repulse and inhibit adult sensory afferents in vivo , 1997, Nature Medicine.

[14]  Mu-ming Poo,et al.  cAMP-Dependent Growth Cone Guidance by Netrin-1 , 1997, Neuron.

[15]  U. Drescher,et al.  The Eph family in the patterning of neural development , 1997, Current Biology.

[16]  Mu-ming Poo,et al.  Turning of Retinal Growth Cones in a Netrin-1 Gradient Mediated by the Netrin Receptor DCC , 1997, Neuron.

[17]  N. Nakao An increase in intracellular levels of cyclic AMP produces trophic effects on striatal neurons developing in culture , 1997, Neuroscience.

[18]  John G. Collard,et al.  The Guanine Nucleotide Exchange Factor Tiam1 Affects Neuronal Morphology; Opposing Roles for the Small GTPases Rac and Rho , 1997, The Journal of cell biology.

[19]  K. Kikuchi,et al.  Molecular cloning of a novel member of semaphorin family genes, semaphorin Z. , 1997, Brain research. Molecular brain research.

[20]  Ingrid W. Caras,et al.  A link between axon guidance and axon fasciculation suggested by studies of the tyrosine kinase receptor EphA5/REK7 and its ligand Ephrin-A5/AL-1 , 1997, Cell and Tissue Research.

[21]  J. Raper,et al.  A Role for Collapsin-1 in Olfactory and Cranial Sensory Axon Guidance , 1997, The Journal of Neuroscience.

[22]  T. Yagi,et al.  Neuropilin–Semaphorin III/D-Mediated Chemorepulsive Signals Play a Crucial Role in Peripheral Nerve Projection in Mice , 1997, Neuron.

[23]  M. Schachner,et al.  Disruption of the mouse L1 gene leads to malformations of the nervous system , 1997, Nature Genetics.

[24]  P. Sonderegger Axonin-1 and NgCAM as ”recognition” components of the pathway sensor apparatus of growth cones: a synopsis , 1997, Cell and Tissue Research.

[25]  T. Kitsukawa,et al.  Roles of a neuronal cell-surface molecule, neuropilin, in nerve fiber fasciculation and guidance , 1997, Cell and Tissue Research.

[26]  Renping Zhou Regulation of topographic projection by the Eph family receptor Bsk (EphA5) and its ligands , 1997, Cell and Tissue Research.

[27]  Jürgen Bolz,et al.  How do wiring molecules specify cortical connections? , 1997, Cell and Tissue Research.

[28]  M. Mark,et al.  Patterning neuronal connections by chemorepulsion: the semaphorins , 1997, Cell and Tissue Research.

[29]  G. Yancopoulos,et al.  Ephrins and their receptors: a repulsive topic? , 1997, Cell and Tissue Research.

[30]  Elena B. Pasquale,et al.  The Eph family: a multitude of receptors that mediate cell recognition signals , 1997, Cell and Tissue Research.

[31]  E. Butcher,et al.  Elevation of Intracellular cAMP Inhibits RhoA Activation and Integrin-dependent Leukocyte Adhesion Induced by Chemoattractants* , 1997, The Journal of Biological Chemistry.

[32]  L. Van Aelst,et al.  Rho GTPases and signaling networks. , 1997, Genes & development.

[33]  T. O'Connor,et al.  Transmembrane grasshopper Semaphorin I promotes axon outgrowth in vivo. , 1997, Development.

[34]  C. Kenyon,et al.  Role of a New Rho Family Member in Cell Migration and Axon Guidance in C. elegans , 1997, Cell.

[35]  T. Yagi,et al.  Disruption of Semaphorin III/D Gene Causes Severe Abnormality in Peripheral Nerve Projection , 1997, Neuron.

[36]  Richard Threadgill,et al.  Regulation of Dendritic Growth and Remodeling by Rho, Rac, and Cdc42 , 1997, Neuron.

[37]  Hiroaki Kobayashi,et al.  A 70 Amino Acid Region within the Semaphorin Domain Activates Specific Cellular Response of Semaphorin Family Members , 1997, Neuron.

[38]  I. de Curtis,et al.  Differential Expression of Distinct Members of Rho Family GTP-Binding Proteins during Neuronal Development: Identification ofRac1B, a New Neural-Specific Member of the Family , 1997, The Journal of Neuroscience.

[39]  C. Goodman,et al.  Neuropilin-2, a Novel Member of the Neuropilin Family, Is a High Affinity Receptor for the Semaphorins Sema E and Sema IV but Not Sema III , 1997, Neuron.

[40]  E. Fransen,et al.  L1-associated diseases: clinical geneticists divide, molecular geneticists unite. , 1997, Human molecular genetics.

[41]  S. Strittmatter,et al.  A novel action of collapsin: collapsin-1 increases antero- and retrograde axoplasmic transport independently of growth cone collapse. , 1997, Journal of neurobiology.

[42]  Michael S. Deiner,et al.  Netrin-1 and DCC Mediate Axon Guidance Locally at the Optic Disc: Loss of Function Leads to Optic Nerve Hypoplasia , 1997, Neuron.

[43]  Hiroaki Kobayashi,et al.  Secreted Chick Semaphorins Bind Recombinant Neuropilin with Similar Affinities but Bind Different Subsets of Neurons In Situ , 1997, Neuron.

[44]  B. Margolis,et al.  Wiskott-Aldrich syndrome protein is associated with the adapter protein Grb2 and the epidermal growth factor receptor in living cells. , 1997, Molecular biology of the cell.

[45]  M. Tessier-Lavigne,et al.  Neuropilin Is a Receptor for the Axonal Chemorepellent Semaphorin III , 1997, Cell.

[46]  Alex L Kolodkin,et al.  Neuropilin Is a Semaphorin III Receptor , 1997, Cell.

[47]  S. Strittmatter,et al.  Rac1 Mediates Collapsin-1-Induced Growth Cone Collapse , 1997, The Journal of Neuroscience.

[48]  J. Livet,et al.  Hepatocyte growth factor (HGF/SF) is a muscle-derived survival factor for a subpopulation of embryonic motoneurons. , 1997, Development.

[49]  Mu-ming Poo,et al.  cAMP-induced switching in turning direction of nerve growth cones , 1997, Nature.

[50]  E. Vinson,et al.  Immunohistochemical Localization of Netrin-1 in the Embryonic Chick Nervous System , 1997, The Journal of Neuroscience.

[51]  J. Feinleib,et al.  CDO: An Oncogene-, Serum-, and Anchorage-regulated Member of the Ig/Fibronectin Type III Repeat Family , 1997, The Journal of cell biology.

[52]  C. Norris,et al.  Netrins evoke mixed reactions in motile cells. , 1997, Trends in genetics : TIG.

[53]  T. Pawson,et al.  Juxtamembrane tyrosine residues couple the Eph family receptor EphB2/Nuk to specific SH2 domain proteins in neuronal cells , 1997, The EMBO journal.

[54]  R. Klein,et al.  The N‐terminal globular domain of Eph receptors is sufficient for ligand binding and receptor signaling , 1997, The EMBO journal.

[55]  M. Barbacid,et al.  Aberrant axonal projections in mice lacking EphA8 (Eek) tyrosine protein kinase receptors , 1997, The EMBO journal.

[56]  M. Barbacid,et al.  Genetic analysis of the role of Eph receptors in the development of the mammalian nervous system , 1997, Cell and Tissue Research.

[57]  M. Masu,et al.  Vertebrate homologues of C. elegans UNC-5 are candidate netrin receptors , 1997, Nature.

[58]  R. Weinberg,et al.  Phenotype of mice lacking functional Deleted in colorectal cancer (Dec) gene , 1997, Nature.

[59]  Stefan A. Przyborski,et al.  The mouse rostral cerebellar malformation gene encodes an UNC-5-like protein , 1997, Nature.

[60]  L. Reichardt,et al.  A sensory axon repellent secreted from ventral spinal cord explants is neutralized by antibodies raised against collapsin-1. , 1997, Development.

[61]  O. Kranenburg,et al.  Lysophosphatidic acid: G-protein signalling and cellular responses. , 1997, Current opinion in cell biology.

[62]  L. Richards,et al.  Directed Growth of Early Cortical Axons Is Influenced by a Chemoattractant Released from an Intermediate Target , 1997, The Journal of Neuroscience.

[63]  Jürgen Löschinger,et al.  Shared and distinct functions of RAGS and ELF‐1 in guiding retinal axons , 1997, The EMBO journal.

[64]  E. Pasquale,et al.  Tyrosine Phosphorylation of Transmembrane Ligands for Eph Receptors , 1997, Science.

[65]  L. Lim,et al.  Rho family GTPases and neuronal growth cone remodelling: relationship between increased complexity induced by Cdc42Hs, Rac1, and acetylcholine and collapse induced by RhoA and lysophosphatidic acid , 1997, Molecular and cellular biology.

[66]  J. Wagner,et al.  Rac is required for growth cone function but not neurite assembly. , 1997, Journal of cell science.

[67]  G. Yancopoulos,et al.  Hepatocyte Growth Factor Promotes Motor Neuron Survival and Synergizes with Ciliary Neurotrophic Factor* , 1997, The Journal of Biological Chemistry.

[68]  L. Landmesser,et al.  Interference with Axonin-1 and NrCAM Interactions Unmasks a Floor-Plate Activity Inhibitory for Commissural Axons , 1997, Neuron.

[69]  F. Bonhoeffer,et al.  The Eph family in retinal axon guidance , 1997, Current Opinion in Neurobiology.

[70]  A. Varela-Echavarría,et al.  Motor Axon Subpopulations Respond Differentially to the Chemorepellents Netrin-1 and Semaphorin D , 1997, Neuron.

[71]  F. Bonhoeffer,et al.  Two Eph receptor tyrosine kinase ligands control axon growth and may be involved in the creation of the retinotectal map in the zebrafish. , 1997, Development.

[72]  F. Walsh,et al.  Expression of a Dominant Negative FGF Receptor Inhibits Axonal Growth and FGF Receptor Phosphorylation Stimulated by CAMs , 1997, Neuron.

[73]  Y. Jan,et al.  Rho family small GTP-binding proteins in growth cone signalling , 1997, Current Opinion in Neurobiology.

[74]  Wange Lu,et al.  Activation of Pak by membrane localization mediated by an SH3 domain from the adaptor protein Nck , 1997, Current Biology.

[75]  S. Guthrie Axon guidance: Netrin receptors are revealed , 1997, Current Biology.

[76]  K. Saigo,et al.  Still life, a Protein in Synaptic Terminals of Drosophila Homologous to GDP-GTP Exchangers , 1997, Science.

[77]  Hao Wang,et al.  Netrin-1 Is Required for Commissural Axon Guidance in the Developing Vertebrate Nervous System , 1996, Cell.

[78]  M. Hanson,et al.  Hepatocyte Growth Factor/Scatter Factor Is an Axonal Chemoattractant and a Neurotrophic Factor for Spinal Motor Neurons , 1996, Neuron.

[79]  C. Goodman,et al.  The Molecular Biology of Axon Guidance , 1996, Science.

[80]  T. Pawson,et al.  Sek4 and Nuk receptors cooperate in guidance of commissural axons and in palate formation. , 1996, The EMBO journal.

[81]  F. Bonhoeffer,et al.  Chromophore-assisted laser inactivation of a repulsive axonal guidance molecule , 1996, Current Biology.

[82]  J. Schmidt,et al.  Myosin light chain kinase: expression in neurons and upregulation during axon regeneration. , 1996, Journal of neurobiology.

[83]  T. Pawson,et al.  Bidirectional signalling through the EPH-family receptor Nuk and its transmembrane ligands , 1996, Nature.

[84]  M. Masu,et al.  Deleted in Colorectal Cancer (DCC) Encodes a Netrin Receptor , 1996, Cell.

[85]  Y. Jan,et al.  frazzled Encodes a Drosophila Member of the DCC Immunoglobulin Subfamily and Is Required for CNS and Motor Axon Guidance , 1996, Cell.

[86]  J. Culotti,et al.  UNC-40, a C. elegans Homolog of DCC (Deleted in Colorectal Cancer), Is Required in Motile Cells Responding to UNC-6 Netrin Cues , 1996, Cell.

[87]  Jeffrey A. Golden,et al.  Semaphorin III is needed for normal patterning and growth of nerves, bones and heart , 1996, Nature.

[88]  M. Hortsch,et al.  The L1 Family of Neural Cell Adhesion Molecules: Old Proteins Performing New Tricks , 1996, Neuron.

[89]  K. Miura,et al.  N‐WASP, a novel actin‐depolymerizing protein, regulates the cortical cytoskeletal rearrangement in a PIP2‐dependent manner downstream of tyrosine kinases. , 1996, The EMBO journal.

[90]  S. Strittmatter,et al.  A Family of Rat CRMP Genes Is Differentially Expressed in the Nervous System , 1996, The Journal of Neuroscience.

[91]  X. Q. Chen,et al.  The p160 RhoA-binding kinase ROK alpha is a member of a kinase family and is involved in the reorganization of the cytoskeleton , 1996, Molecular and cellular biology.

[92]  Chun-Fang Wu,et al.  Reduced Growth Cone Motility in Cultured Neurons fromDrosophila Memory Mutants with a Defective cAMP Cascade , 1996, The Journal of Neuroscience.

[93]  John G Flanagan,et al.  Topographically Specific Effects of ELF-1 on Retinal Axon Guidance In Vitro and Retinal Axon Mapping In Vivo , 1996, Cell.

[94]  J. Wolenski,et al.  Function of Myosin-V in Filopodial Extension of Neuronal Growth Cones , 1996, Science.

[95]  Jennifer L. Doyle,et al.  Genetic Analysis of Netrin Genes in Drosophila: Netrins Guide CNS Commissural Axons and Peripheral Motor Axons , 1996, Neuron.

[96]  M. Seeger,et al.  Guidance Cues at the Drosophila CNS Midline: Identification and Characterization of Two Drosophila Netrin/UNC-6 Homologs , 1996, Neuron.

[97]  Kozo Kaibuchi,et al.  Regulation of Myosin Phosphatase by Rho and Rho-Associated Kinase (Rho-Kinase) , 1996, Science.

[98]  T. Pawson,et al.  Nuk Controls Pathfinding of Commissural Axons in the Mammalian Central Nervous System , 1996, Cell.

[99]  R. Adams,et al.  A novel class of murine semaphorins with homology to thrombospondin is differentially expressed during early embryogenesis , 1996, Mechanisms of Development.

[100]  T. Pawson,et al.  Drosophila Photoreceptor Axon Guidance and Targeting Requires the Dreadlocks SH2/SH3 Adapter Protein , 1996, Cell.

[101]  D. Wilkinson,et al.  Function of the Eph-related kinase rtk1 in patterning of the zebrafish forebrain , 1996, Nature.

[102]  J Wagner,et al.  Src, ras, and rac mediate the migratory response elicited by NGF and PMA in PC12 cells , 1996, Journal of neuroscience research.

[103]  T. Yamamoto,et al.  Rho‐associated kinase, a novel serine/threonine kinase, as a putative target for small GTP binding protein Rho. , 1996, The EMBO journal.

[104]  K. Fujisawa,et al.  The small GTP‐binding protein Rho binds to and activates a 160 kDa Ser/Thr protein kinase homologous to myotonic dystrophy kinase. , 1996, The EMBO journal.

[105]  P. Forscher,et al.  Myosin Drives Retrograde F-Actin Flow in Neuronal Growth Cones , 1996, Neuron.

[106]  K. Matsumoto,et al.  Neurotrophic effect of hepatocyte growth factor on central nervous system neurons in vitro , 1996, Journal of neuroscience research.

[107]  C. Goodman,et al.  commissureless Controls Growth Cone Guidance across the CNS Midline in Drosophila and Encodes a Novel Membrane Protein , 1996, Neuron.

[108]  Y. Jan,et al.  Differential effects of the Rac GTPase on Purkinje cell axons and dendritic trunks and spines , 1996, Nature.

[109]  L. Goldstein,et al.  Receptor Tyrosine Phosphatases Are Required for Motor Axon Guidance in the Drosophila Embryo , 1996, Cell.

[110]  C. Goodman,et al.  The Transmembrane Tyrosine Phosphatase DLAR Controls Motor Axon Guidance in Drosophila , 1996, Cell.

[111]  R. Miledi,et al.  Lysophosphatidic Acid‐Induced Neurite Retraction in PC12 Cells: Neurite‐Protective Effects of Cyclic AMP Signaling , 1996, Journal of neurochemistry.

[112]  D. O'Leary,et al.  Eph receptor tyrosine kinases and their ligands in neural development , 1996, Current Opinion in Neurobiology.

[113]  R. Stancou,et al.  Protein kinase A phosphorylation of RhoA mediates the morphological and functional effects of cyclic AMP in cytotoxic lymphocytes. , 1996, The EMBO journal.

[114]  R. Miledi,et al.  Lysophosphatidic Acid‐Induced Neurite Retraction in PC12 Cells: Control by Phosphoinositide‐Ca2+ Signaling and Rho , 1996, Journal of neurochemistry.

[115]  A. Sobel,et al.  Identification and molecular characterization of Unc-33-like phosphoprotein (Ulip), a putative mammalian homolog of the axonal guidance-associated unc-33 gene product , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[116]  D. Wilkinson,et al.  Expression of truncated Sek-1 receptor tyrosine kinase disrupts the segmental restriction of gene expression in the Xenopus and zebrafish hindbrain. , 1995, Development.

[117]  T. Kitsukawa,et al.  Overexpression of a membrane protein, neuropilin, in chimeric mice causes anomalies in the cardiovascular system, nervous system and limbs. , 1995, Development.

[118]  W. Dreyer,et al.  Binding between the neural cell adhesion molecules axonin-1 and Nr- CAM/Bravo is involved in neuron-glia interaction , 1995, The Journal of cell biology.

[119]  C. Nobes,et al.  The Rho's progress: a potential role during neuritogenesis for the Rho family of GTPases , 1995, Trends in Neurosciences.

[120]  E. Tanaka,et al.  Making the connection: Cytoskeletal rearrangements during growth cone guidance , 1995, Cell.

[121]  S. Hockfield,et al.  TOAD-64, a gene expressed early in neuronal differentiation in the rat, is related to unc-33, a C. elegans gene involved in axon outgrowth , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[122]  A. Marcilla,et al.  Wiskott-Aldrich syndrome protein physically associates with Nck through Src homology 3 domains , 1995, Molecular and cellular biology.

[123]  A. Pandey,et al.  Cell Signalling: Receptor orphans find a family , 1995, Current Biology.

[124]  T. Furuyama,et al.  Identification of a member of mouse semaphorin family. , 1995, FEBS letters.

[125]  Jürgen Löschinger,et al.  In vitro guidance of retinal ganglion cell axons by RAGS, a 25 kDa tectal protein related to ligands for Eph receptor tyrosine kinases , 1995, Cell.

[126]  M. Tessier-Lavigne,et al.  Eph receptor tyrosine kinases, axon repulsion, and the development of topographic maps , 1995, Cell.

[127]  John G Flanagan,et al.  Complementary gradients in expression and binding of ELF-1 and Mek4 in development of the topographic retinotectal projection map , 1995, Cell.

[128]  Fumio Nakamura,et al.  Collapsin-induced growth cone collapse mediated by an intracellular protein related to UNC-33 , 1995, Nature.

[129]  H. Peng,et al.  Presynaptic differentiation induced in cultured neurons by local application of basic fibroblast growth factor , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[130]  A. Schnapp,et al.  Membrane‐bound LERK2 ligand can signal through three different Eph‐related receptor tyrosine kinases. , 1995, The EMBO journal.

[131]  L. Landmesser,et al.  Axonin-1, Nr-CAM, and Ng-CAM play different roles in the in vivo guidance of chick commissural neurons , 1995, Neuron.

[132]  John G. Collard,et al.  A role for Rac in Tiaml-induced membrane ruffling and invasion , 1995, Nature.

[133]  C. Goodman,et al.  Semaphorin II can function as a selective inhibitor of specific synaptic arborizations , 1995, Cell.

[134]  M. Tessier-Lavigne,et al.  The axonal chemoattractant netrin-1 is also a chemorepellent for trochlear motor axons , 1995, Cell.

[135]  F. Hefti,et al.  Cloning of AL-1, a ligand for an Eph-related tyrosine kinase receptor involved in axon bundle formation , 1995, Neuron.

[136]  F. McCormick,et al.  A novel serine kinase activated by rac1/CDC42Hs‐dependent autophosphorylation is related to PAK65 and STE20. , 1995, The EMBO journal.

[137]  R. Adams,et al.  Murine semaphorin D/collapsin is a member of a diverse gene family and creates domains inhibitory for axonal extension , 1995, Neuron.

[138]  F. Murakami,et al.  Guidance of cerebellofugal axons in the rat embryo: Directed growth toward the floor plate and subsequent elongation along the longitudinal axis , 1995, Neuron.

[139]  C. Shatz,et al.  Sernaphorin III can function as a selective chemorepellent to pattern sensory projections in the spinal cord , 1995, Neuron.

[140]  C. Nobes,et al.  Rho, Rac, and Cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia , 1995, Cell.

[141]  L. Lim,et al.  The Ras-related protein Cdc42Hs and bradykinin promote formation of peripheral actin microspikes and filopodia in Swiss 3T3 fibroblasts , 1995, Molecular and cellular biology.

[142]  Jinhong Fan,et al.  Localized collapsing cues can steer growth cones without inducing their full collapse , 1995, Neuron.

[143]  E. Rosen,et al.  Scatter factor and the c-met receptor: a paradigm for mesenchymal/epithelial interaction , 1994, The Journal of cell biology.

[144]  T Pawson,et al.  Ligands for EPH-related receptor tyrosine kinases that require membrane attachment or clustering for activity. , 1994, Science.

[145]  J. Schmidt,et al.  Kinase requirement for retinal growth cone motility. , 1994, Journal of neurobiology.

[146]  T. Jessell,et al.  The netrins define a family of axon outgrowth-promoting proteins homologous to C. elegans UNC-6 , 1994, Cell.

[147]  Timothy E. Kennedy,et al.  Netrins are diffusible chemotropic factors for commissural axons in the embryonic spinal cord , 1994, Cell.

[148]  Y. Jan,et al.  Distinct morphogenetic functions of similar small GTPases: Drosophila Drac1 is involved in axonal outgrowth and myoblast fusion. , 1994, Genes & development.

[149]  J. Culotti Axon guidance mechanisms in Caenorhabditis elegans. , 1994, Current opinion in genetics & development.

[150]  S. Narumiya,et al.  Inhibition of lysophosphatidate- and thrombin-induced neurite retraction and neuronal cell rounding by ADP ribosylation of the small GTP-binding protein Rho , 1994, The Journal of cell biology.

[151]  E. Castrén,et al.  Expression and functional interaction of hepatocyte growth factor- scatter factor and its receptor c-met in mammalian brain , 1994, The Journal of cell biology.

[152]  T. Hunter,et al.  Phosphorylation of receptor protein‐tyrosine phosphatase alpha on Tyr789, a binding site for the SH3‐SH2‐SH3 adaptor protein GRB‐2 in vivo. , 1994, The EMBO journal.

[153]  Yosef Yarden,et al.  B61 is a ligand for the ECK receptor protein-tyrosine kinase , 1994, Nature.

[154]  Philippe Soriano,et al.  Impaired neurite outgrowth of src-minus cerebellar neurons on the cell adhesion molecule L1 , 1994, Neuron.

[155]  W. Gullick,et al.  eph, the largest known family of putative growth factor receptors. , 1994, British Journal of Cancer.

[156]  L. Lim,et al.  A brain serine/threonine protein kinase activated by Cdc42 and Rac1 , 1994, Nature.

[157]  C. Goodman,et al.  The semaphorin genes encode a family of transmembrane and secreted growth cone guidance molecules , 1993, Cell.

[158]  Mark S. Boguski,et al.  Proteins regulating Ras and its relatives , 1993, Nature.

[159]  D. Raible,et al.  Collapsin: A protein in brain that induces the collapse and paralysis of neuronal growth cones , 1993, Cell.

[160]  T. Pawson,et al.  The N‐terminal region of GAP regulates cytoskeletal structure and cell adhesion. , 1993, The EMBO journal.

[161]  P. Jhabvala,et al.  Tyrosine phosphorylation in early embryonic growth cones , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[162]  S. Takagi,et al.  The membrane protein A5, a putative neuronal recognition molecule, promotes neurite outgrowth , 1993, Neuroscience Research.

[163]  J. Culotti,et al.  Expression of the UNC-5 guidance receptor in the touch neurons of C. elegans steers their axons dorsally , 1993, Nature.

[164]  P. Bork,et al.  The CUB domain. A widespread module in developmentally regulated proteins. , 1993, Journal of molecular biology.

[165]  C. Goodman,et al.  Mutations affecting growth cone guidance in drosophila: Genes necessary for guidance toward or away from the midline , 1993, Neuron.

[166]  C. Shatz,et al.  Developmental mechanisms that generate precise patterns of neuronal connectivity , 1993, Cell.

[167]  J. Culotti,et al.  UNC-6, a laminin-related protein, guides cell and pioneer axon migrations in C. elegans , 1992, Neuron.

[168]  N. Patel,et al.  Fasciclin IV: Sequence, expression, and function during growth cone guidance in the grasshopper embryo , 1992, Neuron.

[169]  R. K. Herman,et al.  Analysis of the Caenorhabditis elegans axonal guidance and outgrowth gene unc-33. , 1992, Genetics.

[170]  J. Culotti,et al.  UNC-5, a transmembrane protein with immunoglobulin and thrombospondin type 1 domains, guides cell and pioneer axon migrations in C. elegans , 1992, Cell.

[171]  M. Schachner,et al.  Cell Type‐specific Effects of the Neural Adhesion Molecules L1 and N‐CAM on Diverse Second Messenger Systems , 1992, The European journal of neuroscience.

[172]  A. Ullrich,et al.  Growth factor signaling by receptor tyrosine kinases , 1992, Neuron.

[173]  Anne J. Ridley,et al.  The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors , 1992, Cell.

[174]  Anne J. Ridley,et al.  The small GTP-binding protein rac regulates growth factor-induced membrane ruffling , 1992, Cell.

[175]  K. Jalink,et al.  Thrombin receptor activation causes rapid neural cell rounding and neurite retraction independent of classic second messengers , 1992, The Journal of cell biology.

[176]  R. Weinberg,et al.  Molecular cloning of cDNAs encoding the GAP-associated protein p190: Implications for a signaling pathway from ras to the nucleus , 1992, Cell.

[177]  K. Agata,et al.  The A5 antigen, a candidate for the neuronal recognition molecule, has homologies to complement components and coagulation factors , 1991, Neuron.

[178]  R. Pittman,et al.  Intracellular calcium levels do not change during contact-mediated collapse of chick DRG growth cone structure , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[179]  D. Baltimore,et al.  The noncatalytic src homology region 2 segment of abl tyrosine kinase binds to tyrosine-phosphorylated cellular proteins with high affinity. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[180]  D. Trisler,et al.  Cell recognition and pattern formation in the developing nervous system. , 1990, The Journal of experimental biology.

[181]  D. Hall,et al.  The unc-5, unc-6, and unc-40 genes guide circumferential migrations of pioneer axons and mesodermal cells on the epidermis in C. elegans , 1990, Neuron.

[182]  S. B. Kater,et al.  Intracellular messengers in the generation and degeneration of hippocampal neuroarchitecture , 1988, Journal of neuroscience research.

[183]  S. Kater,et al.  Neurite outgrowth in individual neurons of a neuronal population is differentially regulated by calcium and cyclic AMP , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[184]  T. Jessell,et al.  Spatial regulation of axonal glycoprotein expression on subsets of embryonic spinal neurons , 1988, Neuron.

[185]  L. Greene,et al.  cAMP analogs promote survival and neurite outgrowth in cultures of rat sympathetic and sensory neurons independently of nerve growth factor. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[186]  Alfred Gierer,et al.  Directional cues for growing axons forming the retinotectal projection , 1987 .

[187]  M. Schachner,et al.  Immunocytological and biochemical characterization of a new neuronal cell surface component (L1 antigen) which is involved in cell adhesion. , 1984, The EMBO journal.

[188]  S. Brenner The genetics of Caenorhabditis elegans. , 1974, Genetics.

[189]  S. Ackerman,et al.  Embryonic phenotype of Unc5h3 mutant mice suggests chemorepulsion during the formation of the rostral cerebellar boundary. , 1998, Development.

[190]  Claire Russell,et al.  Dosage-Sensitive and Complementary Functions of Roundabout and Commissureless Control Axon Crossing of the CNS Midline , 1998, Neuron.

[191]  F. Walsh,et al.  Neural cell adhesion molecules of the immunoglobulin superfamily: role in axon growth and guidance. , 1997, Annual review of cell and developmental biology.

[192]  C. Goodman,et al.  Mechanisms and molecules that control growth cone guidance. , 1996, Annual review of neuroscience.

[193]  Uno Lindberg,et al.  Two GTPases, Cdc42 and Rac, bind directly to a protein implicated in the immunodeficiency disorder Wiskott–Aldrich syndrome , 1996, Current Biology.

[194]  A. Kolodkin Semaphorins: mediators of repulsive growth cone guidance. , 1996, Trends in cell biology.

[195]  E. Hedgecock,et al.  Neuroglia and Pioneer Neurons Express UNC-6 to Provide Global and Local Netrin Cues for Guiding Migrations in C. elegans , 1996, Neuron.

[196]  M. Tessier-Lavigne,et al.  The role of the floor plate in axon guidance. , 1995, Annual review of neuroscience.

[197]  A. Hall,et al.  Small GTP-binding proteins and the regulation of the actin cytoskeleton. , 1994, Annual review of cell biology.

[198]  S. B. Kater,et al.  Role of intracellular calcium in NI-35-evoked collapse of neuronal growth cones. , 1993, Science.

[199]  D. Baltimore,et al.  Signalling through SH2 and SH3 domains. , 1993, Trends in cell biology.

[200]  R. Timpl,et al.  Laminin and other basement membrane components. , 1987, Annual review of cell biology.