Navigating their way to the clinic: Emerging roles for axon guidance molecules in neurological disorders and injury

The mechanisms underlying formation of the basic network of the nervous system are of fundamental interest in developmental neurobiology. During the wiring of the nervous system, newborn neurons send axons that travel long distances to their targets. These axons are directed by environmental cues, known as guidance cues, to their correct destinations. Through extensive studies in vertebrates and invertebrates many of the guidance cues and their receptors have been identified. Recently, guidance molecules have been suggested to have important roles in pathological conditions of the nervous system. Mutations in guidance receptors have been associated with hereditary neurological disorders, and deregulation of guidance cues might be associated with predisposition to epilepsy. In addition, it was suggested that guidance molecules play roles in the ability of the adult nervous system to recover and repair after injury. Thus, molecules that were first discovered as “developmental cues” are now emerging as important factors in neurological disease and injury in the adult. © 2007 Wiley Periodicals, Inc. Develop Neurobiol, 2007

[1]  J. Sharpe,et al.  Familial paralysis of horizontal gaze , 1975, Neurology.

[2]  J. Rothberg,et al.  slit: An EGF-homologous locus of D. melanogaster involved in the development of the embryonic central nervous system , 1988, Cell.

[3]  J. Rothberg,et al.  slit: an extracellular protein necessary for development of midline glia and commissural axon pathways contains both EGF and LRR domains. , 1990, Genes & development.

[4]  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.

[5]  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.

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

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

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

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

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

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

[12]  J. McNamara,et al.  Mechanism of epilepsy. , 1994, Annual review of medicine.

[13]  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.

[14]  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.

[15]  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.

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

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

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

[19]  A. Flenniken,et al.  Eph Receptors and Ligands Comprise Two Major Specificity Subclasses and Are Reciprocally Compartmentalized during Embryogenesis , 1996, Neuron.

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

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

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

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

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

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

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

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

[28]  M. Yamasaki,et al.  Adhesion molecules and inherited diseases of the human nervous system. , 1998, Annual review of neuroscience.

[29]  C. Goodman,et al.  Plexin A Is a Neuronal Semaphorin Receptor that Controls Axon Guidance , 1998, Cell.

[30]  J. Verhaagen,et al.  Regulation of Semaphorin III/Collapsin-1 Gene Expression during Peripheral Nerve Regeneration , 1998, Experimental Neurology.

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

[32]  Shay Soker,et al.  Neuropilin-1 Is Expressed by Endothelial and Tumor Cells as an Isoform-Specific Receptor for Vascular Endothelial Growth Factor , 1998, Cell.

[33]  R. Dubose,et al.  A poxvirus-encoded semaphorin induces cytokine production from monocytes and binds to a novel cellular semaphorin receptor, VESPR. , 1998, Immunity.

[34]  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.

[35]  V. Gagliardini,et al.  Semaphorin III Can Induce Death in Sensory Neurons , 1999, Molecular and Cellular Neuroscience.

[36]  M. Ruitenberg,et al.  Expression of the Gene Encoding the Chemorepellent Semaphorin III Is Induced in the Fibroblast Component of Neural Scar Tissue Formed Following Injuries of Adult But Not Neonatal CNS , 1999, Molecular and Cellular Neuroscience.

[37]  M. Poo,et al.  Unified Nomenclature for the Semaphorins/Collapsins , 1999, Cell.

[38]  C. Goodman,et al.  Slit Is the Midline Repellent for the Robo Receptor in Drosophila , 1999, Cell.

[39]  Sophie Dupuis,et al.  Directional guidance of neuronal migration in the olfactory system by the protein Slit , 1999, Nature.

[40]  L. Cox,et al.  Cloning and functional studies of a novel gene aberrantly expressed in RB-deficient embryos. , 1999, Developmental biology.

[41]  Mu-ming Poo,et al.  A Ligand-Gated Association between Cytoplasmic Domains of UNC5 and DCC Family Receptors Converts Netrin-Induced Growth Cone Attraction to Repulsion , 1999, Cell.

[42]  Y. Rao,et al.  Vertebrate Slit, a Secreted Ligand for the Transmembrane Protein Roundabout, Is a Repellent for Olfactory Bulb Axons , 1999, Cell.

[43]  C. Goodman,et al.  Biochemical Purification of a Mammalian Slit Protein as a Positive Regulator of Sensory Axon Elongation and Branching , 1999, Cell.

[44]  R. Kalb,et al.  Plexin-Neuropilin-1 Complexes Form Functional Semaphorin-3A Receptors , 1999, Cell.

[45]  Philippe Soriano,et al.  Compartmentalized signaling by GPI-anchored ephrin-A5 requires the Fyn tyrosine kinase to regulate cellular adhesion. , 1999, Genes & development.

[46]  J. Dodd,et al.  BMPs as Mediators of Roof Plate Repulsion of Commissural Neurons , 1999, Neuron.

[47]  C. Goodman,et al.  Slit Proteins Bind Robo Receptors and Have an Evolutionarily Conserved Role in Repulsive Axon Guidance , 1999, Cell.

[48]  Julie H. Simpson,et al.  Short-Range and Long-Range Guidance by Slit and Its Robo Receptors Robo and Robo2 Play Distinct Roles in Midline Guidance , 2000, Neuron.

[49]  B. Dickson,et al.  Crossing the Midline Roles and Regulation of Robo Receptors , 2000, Neuron.

[50]  Julie H. Simpson,et al.  Short-Range and Long-Range Guidance by Slit and Its Robo Receptors A Combinatorial Code of Robo Receptors Controls Lateral Position , 2000, Cell.

[51]  J. Frisén,et al.  Regulation of repulsion versus adhesion by different splice forms of an Eph receptor , 2000, Nature.

[52]  Anirvan Ghosh,et al.  Semaphorin 3A is a chemoattractant for cortical apical dendrites , 2000, Nature.

[53]  S. Rastan,et al.  Neuropilin-2 Is Required In Vivo for Selective Axon Guidance Responses to Secreted Semaphorins , 2000, Neuron.

[54]  B. Dickson,et al.  Selecting a Longitudinal Pathway Robo Receptors Specify the Lateral Position of Axons in the Drosophila CNS , 2000, Cell.

[55]  M. Schachner,et al.  Analysis of the L1-Deficient Mouse Phenotype Reveals Cross-Talk between Sema3A and L1 Signaling Pathways in Axonal Guidance , 2000, Neuron.

[56]  M. Poo,et al.  Plexins Are a Large Family of Receptors for Transmembrane, Secreted, and GPI-Anchored Semaphorins in Vertebrates , 1999, Cell.

[57]  M. Tessier-Lavigne,et al.  Plexin-A3 Mediates Semaphorin Signaling and Regulates the Development of Hippocampal Axonal Projections , 2001, Neuron.

[58]  P. Bovolenta,et al.  Control of retinal ganglion cell axon growth: a new role for Sonic hedgehog. , 2001, Development.

[59]  J. Verhaagen,et al.  Peripheral nerve injury fails to induce growth of lesioned ascending dorsal column axons into spinal cord scar tissue expressing the axon repellent Semaphorin3A , 2001, The European journal of neuroscience.

[60]  T. Kennedy,et al.  Widespread Expression of Netrin-1 by Neurons and Oligodendrocytes in the Adult Mammalian Spinal Cord , 2001, The Journal of Neuroscience.

[61]  C. Goodman,et al.  The Transmembrane Protein Off-Track Associates with Plexins and Functions Downstream of Semaphorin Signaling during Axon Guidance , 2001, Neuron.

[62]  Cori Bargmann,et al.  Dynamic regulation of axon guidance , 2001, Nature Neuroscience.

[63]  B. Dickson,et al.  Short- and Long-Range Repulsion by the Drosophila Unc5 Netrin Receptor , 2001, Neuron.

[64]  David G. Wilkinson,et al.  Multiple roles of eph receptors and ephrins in neural development , 2001, Nature Reviews Neuroscience.

[65]  J. Darnell,et al.  Fragile X Mental Retardation Protein Targets G Quartet mRNAs Important for Neuronal Function , 2001, Cell.

[66]  W. Chia,et al.  Characterization and mutant analysis of the Drosophila sema 5c gene , 2001, Developmental dynamics : an official publication of the American Association of Anatomists.

[67]  A. Teleman,et al.  Shaping Morphogen Gradients , 2001, Cell.

[68]  S. Whittemore,et al.  Upregulation of EphA Receptor Expression in the Injured Adult Rat Spinal Cord , 2002, Cell transplantation.

[69]  C. Goodman,et al.  Regulation of Cortical Dendrite Development by Slit-Robo Interactions , 2002, Neuron.

[70]  C. Sabatti,et al.  Familial horizontal gaze palsy with progressive scoliosis maps to chromosome 11q23-25 , 2002, Neurology.

[71]  J. Verhaagen,et al.  Injury-Induced Class 3 Semaphorin Expression in the Rat Spinal Cord , 2002, Experimental Neurology.

[72]  D. O'Leary,et al.  EphB Forward Signaling Controls Directional Branch Extension and Arborization Required for Dorsal-Ventral Retinotopic Mapping , 2002, Neuron.

[73]  S. Kenwrick,et al.  Cis and trans interactions of L1 with neuropilin‐1 control axonal responses to semaphorin 3A , 2002, The EMBO journal.

[74]  B. Dickson Molecular Mechanisms of Axon Guidance , 2002, Science.

[75]  A. Barzilai,et al.  Anti-semaphorin 3A Antibodies Rescue Retinal Ganglion Cells from Cell Death following Optic Nerve Axotomy* , 2002, The Journal of Biological Chemistry.

[76]  E. Berry-Kravis,et al.  Epilepsy in fragile X syndrome , 2002, Developmental medicine and child neurology.

[77]  B. Dickson,et al.  Comm Sorts Robo to Control Axon Guidance at the Drosophila Midline , 2002, Cell.

[78]  W. Greenough,et al.  Altered mossy fiber distributions in adult Fmr1 (FVB) knockout mice , 2002, Hippocampus.

[79]  Carol A. Mason,et al.  Slit1 and Slit2 Cooperate to Prevent Premature Midline Crossing of Retinal Axons in the Mouse Visual System , 2002, Neuron.

[80]  Matthias Mann,et al.  RGM is a repulsive guidance molecule for retinal axons , 2002, Nature.

[81]  A. B. Huber,et al.  Signaling at the growth cone: ligand-receptor complexes and the control of axon growth and guidance. , 2003, Annual review of neuroscience.

[82]  A. Kolodkin,et al.  Semaphorin 3F Is Critical for Development of Limbic System Circuitry and Is Required in Neurons for Selective CNS Axon Guidance Events , 2003, The Journal of Neuroscience.

[83]  Paul J. Harrison,et al.  The axonal chemorepellant semaphorin 3A is increased in the cerebellum in schizophrenia and may contribute to its synaptic pathology , 2003, Molecular Psychiatry.

[84]  S. Niclou,et al.  Meningeal cell-derived semaphorin 3A inhibits neurite outgrowth , 2003, Molecular and Cellular Neuroscience.

[85]  J. McNamara,et al.  Temporal specific patterns of semaphorin gene expression in rat brain after kainic acid‐induced status epilepticus , 2003, Hippocampus.

[86]  S. Whittemore,et al.  Transection of the Adult Rat Spinal Cord Upregulates EphB3 Receptor and Ligand Expression , 2003, Cell transplantation.

[87]  J. Dodd,et al.  A Role for BMP Heterodimers in Roof Plate-Mediated Repulsion of Commissural Axons , 2003, Neuron.

[88]  P. Mehlen,et al.  The dependence receptors DCC and UNC5H as a link between neuronal guidance and survival , 2003, Biology of the cell.

[89]  John B. Thomas,et al.  Wnt-mediated axon guidance via the Drosophila Derailed receptor , 2003, Nature.

[90]  M. Tessier-Lavigne,et al.  Stereotyped Pruning of Long Hippocampal Axon Branches Triggered by Retraction Inducers of the Semaphorin Family , 2003, Cell.

[91]  C. Jaillard,et al.  The Transmembrane Semaphorin Sema4D/CD100, an Inhibitor of Axonal Growth, Is Expressed on Oligodendrocytes and Upregulated after CNS Lesion , 2003, The Journal of Neuroscience.

[92]  Ken Watanabe,et al.  UNC5H1 Induces Apoptosis via Its Juxtamembrane Region through an Interaction with NRAGE* , 2003, The Journal of Biological Chemistry.

[93]  Marc Tessier-Lavigne,et al.  Anterior-Posterior Guidance of Commissural Axons by Wnt-Frizzled Signaling , 2003, Science.

[94]  K. Kikuchi,et al.  In Vitro and in Vivo Characterization of a Novel Semaphorin 3A Inhibitor, SM-216289 or Xanthofulvin* , 2003, Journal of Biological Chemistry.

[95]  A. Holtmaat,et al.  Transient downregulation of sema3a mrna in a rat model for temporal lobe epilepsy A novel molecular event potentially contributing to mossy fiber sprouting , 2003, Experimental Neurology.

[96]  A. Wanaka,et al.  Slit and glypican‐1 mRNAs are coexpressed in the reactive astrocytes of the injured adult brain , 2003, Glia.

[97]  L. F. Kromer,et al.  Ephrin-B2 and EphB2 Regulation of Astrocyte-Meningeal Fibroblast Interactions in Response to Spinal Cord Lesions in Adult Rats , 2003, The Journal of Neuroscience.

[98]  A. McMahon,et al.  The Morphogen Sonic Hedgehog Is an Axonal Chemoattractant that Collaborates with Netrin-1 in Midline Axon Guidance , 2003, Cell.

[99]  D. Geschwind,et al.  Mutations in a Human ROBO Gene Disrupt Hindbrain Axon Pathway Crossing and Morphogenesis , 2004, Science.

[100]  C. Goodman,et al.  Conserved Roles for Slit and Robo Proteins in Midline Commissural Axon Guidance , 2004, Neuron.

[101]  W. Mandemakers,et al.  An Oligodendrocyte Lineage-Specific Semaphorin, Sema5A, Inhibits Axon Growth by Retinal Ganglion Cells , 2004, The Journal of Neuroscience.

[102]  R. Yuste,et al.  Regulation of dendritic length and branching by semaphorin 3A. , 2004, Journal of neurobiology.

[103]  C. Sotelo,et al.  The Slit Receptor Rig-1/Robo3 Controls Midline Crossing by Hindbrain Precerebellar Neurons and Axons , 2004, Neuron.

[104]  F. Murakami,et al.  The Divergent Robo Family Protein Rig-1/Robo3 Is a Negative Regulator of Slit Responsiveness Required for Midline Crossing by Commissural Axons , 2004, Cell.

[105]  Jerry Silver,et al.  Regeneration beyond the glial scar , 2004, Nature Reviews Neuroscience.

[106]  G. Alvarez-Bolado,et al.  Expression pattern of the repulsive guidance molecules RGM A, B and C during mouse development. , 2004, Gene expression patterns : GEP.

[107]  D. Pleasure,et al.  Modulation of Sciatic Nerve Expression of Class 3 Semaphorins by Nerve Injury , 2004, Neurochemical Research.

[108]  S. Arber,et al.  Repulsive Guidance Molecule (RGM) Gene Function Is Required for Neural Tube Closure But Not Retinal Topography in the Mouse Visual System , 2004, The Journal of Neuroscience.

[109]  Chen Li,et al.  Repelling class discrimination: ephrin-A5 binds to and activates EphB2 receptor signaling , 2004, Nature Neuroscience.

[110]  S. Strittmatter,et al.  RGM and its receptor neogenin regulate neuronal survival , 2004, Nature Cell Biology.

[111]  Srikanth Rajagopalan,et al.  Neogenin mediates the action of repulsive guidance molecule , 2004, Nature Cell Biology.

[112]  M. Hori,et al.  Dual roles of Sema6D in cardiac morphogenesis through region-specific association of its receptor, Plexin-A1, with off-track and vascular endothelial growth factor receptor type 2. , 2004, Genes & development.

[113]  D. Perl,et al.  A role for semaphorin 3A signaling in the degeneration of hippocampal neurons during Alzheimer's disease , 2004, Journal of neurochemistry.

[114]  Mary P Galea,et al.  Axonal Regeneration and Lack of Astrocytic Gliosis in EphA4-Deficient Mice , 2004, The Journal of Neuroscience.

[115]  D. Engelkamp,et al.  Isolation and expression pattern of three mouse homologues of chick Rgm. , 2004, Gene expression patterns : GEP.

[116]  Dual Functional Activity of Semaphorin 3B Is Required for Positioning the Anterior Commissure , 2005, Neuron.

[117]  K. Alitalo,et al.  Neural guidance molecules regulate vascular remodeling and vessel navigation. , 2005, Genes & development.

[118]  Jun Shi,et al.  Ryk-mediated Wnt repulsion regulates posterior-directed growth of corticospinal tract , 2005, Nature Neuroscience.

[119]  Takeshi Yagi,et al.  Plexin-A4 Mediates Axon-Repulsive Activities of Both Secreted and Transmembrane Semaphorins and Plays Roles in Nerve Fiber Guidance , 2005, The Journal of Neuroscience.

[120]  M. Tessier-Lavigne,et al.  Differential Requirement for Plexin-A3 and -A4 in Mediating Responses of Sensory and Sympathetic Neurons to Distinct Class 3 Semaphorins , 2005, Neuron.

[121]  C. Sotelo,et al.  Expression of netrin‐1, slit‐1 and slit‐3 but not of slit‐2 after cerebellar and spinal cord lesions , 2005, The European journal of neuroscience.

[122]  L. Parada,et al.  Ephrin-B3 is a myelin-based inhibitor of neurite outgrowth. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[123]  V. Pekarik,et al.  Sonic hedgehog guides commissural axons along the longitudinal axis of the spinal cord , 2005, Nature Neuroscience.

[124]  J. Sanes,et al.  Dual Functional Activity of Semaphorin 3B Is Required for Positioning the Anterior Commissure , 2005, Neuron.

[125]  R. Huganir,et al.  Secreted Semaphorins Modulate Synaptic Transmission in the Adult Hippocampus , 2005, The Journal of Neuroscience.

[126]  Thomas M. Jessell,et al.  Semaphorin 3E and Plexin-D1 Control Vascular Pattern Independently of Neuropilins , 2005, Science.

[127]  P. Carmeliet,et al.  Common mechanisms of nerve and blood vessel wiring , 2005, Nature.

[128]  Marc Tessier-Lavigne,et al.  Novel brain wiring functions for classical morphogens: a role as graded positional cues in axon guidance , 2005, Development.

[129]  B. Dickson,et al.  Comm function in commissural axon guidance: cell-autonomous sorting of Robo in vivo , 2005, Nature Neuroscience.

[130]  Juha Kere,et al.  The Axon Guidance Receptor Gene ROBO1 Is a Candidate Gene for Developmental Dyslexia , 2005, PLoS genetics.

[131]  G. Neufeld,et al.  Semaphorins in cancer. , 2005, Frontiers in bioscience : a journal and virtual library.

[132]  A. Chédotal,et al.  The brain within the tumor: new roles for axon guidance molecules in cancers , 2005, Cell Death and Differentiation.

[133]  Jeff W Lichtman,et al.  In vivo imaging of axonal degeneration and regeneration in the injured spinal cord , 2005, Nature Medicine.

[134]  G. Smith,et al.  Genetic background regulates semaphorin gene expression and epileptogenesis in mouse brain after kainic acid status epilepticus , 2005, Neuroscience.

[135]  T. Yamashita,et al.  RGMa inhibition promotes axonal growth and recovery after spinal cord injury , 2006, The Journal of cell biology.

[136]  B. Zheng,et al.  Genetic mouse models for studying inhibitors of spinal axon regeneration , 2006, Trends in Neurosciences.

[137]  L. DeLisi,et al.  Identification of the semaphorin receptor PLXNA2 as a candidate for susceptibility to schizophrenia , 2006, Molecular Psychiatry.

[138]  A. Schmitt,et al.  Wnt–Ryk signalling mediates medial–lateral retinotectal topographic mapping , 2006, Nature.

[139]  S. Niclou,et al.  The expression of the chemorepellent Semaphorin 3A is selectively induced in terminal Schwann cells of a subset of neuromuscular synapses that display limited anatomical plasticity and enhanced vulnerability in motor neuron disease , 2006, Molecular and Cellular Neuroscience.

[140]  D. Sretavan,et al.  EphB3: An Endogenous Mediator of Adult Axonal Plasticity and Regrowth after CNS Injury , 2006, The Journal of Neuroscience.

[141]  B. Pennington,et al.  Breakthroughs in the search for dyslexia candidate genes. , 2006, Trends in molecular medicine.

[142]  M. Tessier-Lavigne,et al.  UNC5A promotes neuronal apoptosis during spinal cord development independent of netrin-1 , 2006, Nature Neuroscience.

[143]  Yamit Hagalili,et al.  Semaphorin 3A and neurotrophins: a balance between apoptosis and survival signaling in embryonic DRG neurons , 2006, Journal of neurochemistry.

[144]  Dominique Debanne,et al.  Semaphorin3A regulates synaptic function of differentiated hippocampal neurons , 2006, The European journal of neuroscience.

[145]  H. Okano,et al.  A selective Sema3A inhibitor enhances regenerative responses and functional recovery of the injured spinal cord , 2006, Nature Medicine.

[146]  Nicole H. Wilson,et al.  Neogenin interacts with RGMa and netrin-1 to guide axons within the embryonic vertebrate forebrain. , 2006, Developmental biology.

[147]  A. Chédotal,et al.  Repulsive Guidance Molecule Plays Multiple Roles in Neuronal Differentiation and Axon Guidance , 2006, The Journal of Neuroscience.

[148]  E. Engle,et al.  Horizontal gaze palsy with progressive scoliosis can result from compound heterozygous mutations in ROBO3 , 2005, Journal of Medical Genetics.

[149]  T. Yagi,et al.  Regulation of Dendritic Branching and Spine Maturation by Semaphorin3A-Fyn Signaling , 2006, The Journal of Neuroscience.

[150]  Zhigang He,et al.  Glial inhibition of CNS axon regeneration , 2006, Nature Reviews Neuroscience.

[151]  A. Kolodkin,et al.  Drosophila Plexin B is a Sema-2a receptor required for axon guidance , 2006, Development.

[152]  Giorgio F. Gilestro,et al.  Regulation of commissural axon pathfinding by slit and its Robo receptors. , 2006, Annual review of cell and developmental biology.

[153]  Franklin Peale,et al.  Blocking neuropilin-1 function has an additive effect with anti-VEGF to inhibit tumor growth. , 2007, Cancer cell.

[154]  N. Wray,et al.  Anxiety and comorbid measures associated with PLXNA2. , 2007, Archives of general psychiatry.

[155]  L. Benowitz,et al.  Combinatorial treatments for promoting axon regeneration in the CNS: Strategies for overcoming inhibitory signals and activating neurons' intrinsic growth state , 2007, Developmental neurobiology.

[156]  D. Rujescu,et al.  Plexin B3 is genetically associated with verbal performance and white matter volume in human brain , 2007, Molecular Psychiatry.