Crossing the floor plate triggers sharp turning of commissural axons.

During development of the vertebrate CNS, commissural axons initially grow circumferentially toward the ventral midline floor plate. After crossing the floor plate, they abruptly change their trajectory from the circumferential to the longitudinal axis. Although recent studies have unraveled the mechanisms that control navigation of these axons along the circumferential axis, those that result in the transition from circumferential to longitudinal trajectory remain unknown. Here, we examined whether an interaction with the floor plate is a prerequisite for the initiation of trajectory transition of commissural axons, using in vitro preparations of the rat metencephalon. We found that commissural axons in the metencephalon, once having crossed the floor plate, turned sharply to grow longitudinally. In contrast, axons extending in floor plate-deleted preparations, continued to grow circumferentially, ignoring the hypothetical turning point. These results suggest that a prior interaction of commissural axons with floor plate cells is a key step for these axons to activate a navigation program required for their change in axonal trajectory from the circumferential to the longitudinal axis.

[1]  S. Thanos,et al.  A study in developing visual systems with a new method of staining neurones and their processes in fixed tissue. , 1987, Development.

[2]  Y. Rao,et al.  The mouse SLIT family: secreted ligands for ROBO expressed in patterns that suggest a role in morphogenesis and axon guidance. , 1999, Developmental biology.

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

[4]  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.

[5]  T. Jessell,et al.  F-spondin: A gene expressed at high levels in the floor plate encodes a secreted protein that promotes neural cell adhesion and neurite extension , 1992, Cell.

[6]  Roger Keynes,et al.  Axon guidance to and from choice points , 1998, Current Opinion in Neurobiology.

[7]  P. Bovolenta,et al.  Perturbation of neuronal differentiation and axon guidance in the spinal cord of mouse embryos lacking a floor plate: analysis of Danforth's short-tail mutation. , 1991, Development.

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

[9]  P. Bovolenta,et al.  Guidance of commissural growth cones at the floor plate in embryonic rat spinal cord. , 1990, Development.

[10]  D. V. Vactor Axon guidance , 1999, Current Biology.

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

[12]  M. Bastiani,et al.  Requirement of RNA synthesis for pathfinding by growing axons , 1995, The Journal of comparative neurology.

[13]  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.

[14]  C. Sotelo,et al.  Proximal trajectory of the brachium conjunctivum in rat fetuses and its early association with the parabrachial nucleus. A study combining in vitro HRP anterograde axonal tracing and immunocytochemistry. , 1989, Brain research. Developmental brain research.

[15]  M. Edwards,et al.  Distribution of stage-specific neurite-associated proteins in the developing murine nervous system recognized by a monoclonal antibody , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  L. Landmesser,et al.  Axon guidance at choice points , 1998, Current Opinion in Neurobiology.

[17]  M. G. Honig,et al.  Dil and DiO: versatile fluorescent dyes for neuronal labelling and pathway tracing , 1989, Trends in Neurosciences.

[18]  F. Murakami,et al.  Guidance of Circumferentially Growing Axons by Netrin-Dependent and -Independent Floor Plate Chemotropism in the Vertebrate Brain , 1996, Neuron.

[19]  B. Condron Serotonergic Neurons Transiently Require a Midline-Derived FGF Signal , 1999, Neuron.

[20]  J. Clarke,et al.  Neuroanatomical and functional analysis of neural tube formation in notochordless Xenopus embryos; laterality of the ventral spinal cord is lost. , 1991, Development.

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

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

[23]  John G. Flanagan,et al.  The Middle and the End Slit Brings Guidance and Branching Together in Axon Pathway Selection , 1999, Neuron.

[24]  Marc Tessier-Lavigne,et al.  Squeezing Axons Out of the Gray Matter A Role for Slit and Semaphorin Proteins from Midline and Ventral Spinal Cord , 2000, Cell.

[25]  F. Murakami,et al.  Guidance of circumferentially growing axons by the floor plate in the vertebrate central nervous system , 1997, Cell and Tissue Research.

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

[27]  A. Frumkin,et al.  F-Spondin Is Required for Accurate Pathfinding of Commissural Axons at the Floor Plate , 1999, Neuron.

[28]  B. Mueller,et al.  Growth cone guidance: first steps towards a deeper understanding. , 1999, Annual review of neuroscience.

[29]  Toshiya Yamada,et al.  Distinct but overlapping expression patterns of two vertebrate slit homologs implies functional roles in CNS development and organogenesis , 1998, Mechanisms of Development.