Binding and complementary expression patterns of semaphorin 3E and plexin D1 in the mature neocortices of mice and monkeys

Although axon guidance molecules play critical roles in neural circuit formation during development, their roles in the adult circuit are not well understood. In this study we examined the expression patterns of Semaphorin 3E (Sema3E), a member of the semaphorin family, in the mature neocortices of monkeys and mice by in situ hybridization (ISH). We found that Sema3E mRNA is highly specific to layer VI throughout the macaque monkey neocortex. We further examined the ratio of Sema3E+ cells among the layer VI excitatory neurons in areas M1, S1, TE, and V1 by fluorescence double ISH, using the vesicular glutamate transporter 1 (VGluT1) gene as a specific marker for excitatory neurons. Among these areas, 34–63% of the VGluT1+ neurons expressed Sema3E mRNA. In the mouse cortex, two significant differences were observed in the pattern of Sema3E mRNA distribution. 1) Sema3E mRNA was expressed in layer Vb, in addition to layer VI in mice. 2) A subset of GABAergic interneurons expressed Sema3E mRNA in mice. By an in vitro binding experiment, we provide evidence that Plexin D1 is the specific receptor for Sema3E. Plexin D1 mRNA was preferentially expressed in layers II–V in both monkey and mouse cortices. The detailed lamina analysis by double ISH, however, revealed that Plexin D1 mRNA is expressed in layers II–Va, but not in layer Vb in the mouse cortex. Thus, the Plexin D1 and Sema3E mRNAs exhibit conserved complementary lamina patterns in mice and monkeys, despite the species differences in the pattern of each gene. J. Comp. Neurol. 499:258–273, 2006. © 2006 Wiley‐Liss, Inc.

[1]  K. Svoboda,et al.  Cell Type-Specific Structural Plasticity of Axonal Branches and Boutons in the Adult Neocortex , 2006, Neuron.

[2]  Edward M Callaway,et al.  Local connections to specific types of layer 6 neurons in the rat visual cortex. , 2006, Journal of neurophysiology.

[3]  R Kötter,et al.  Morphology, electrophysiology and functional input connectivity of pyramidal neurons characterizes a genuine layer va in the primary somatosensory cortex. , 2006, Cerebral cortex.

[4]  Yevgenia Kozorovitskiy,et al.  Experience induces structural and biochemical changes in the adult primate brain. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[5]  K. Guan,et al.  Semaphorins command cells to move , 2005, Nature Reviews Molecular Cell Biology.

[6]  W. Gan,et al.  Development of Long-Term Dendritic Spine Stability in Diverse Regions of Cerebral Cortex , 2005, Neuron.

[7]  G. Shepherd,et al.  Transient and Persistent Dendritic Spines in the Neocortex In Vivo , 2005, Neuron.

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

[9]  T. Hashikawa,et al.  Retinol-binding protein gene is highly expressed in higher-order association areas of the primate neocortex. , 2004, Cerebral cortex.

[10]  H. Fujisawa Discovery of semaphorin receptors, neuropilin and plexin, and their functions in neural development. , 2004, Journal of neurobiology.

[11]  J. D. Wit,et al.  Role of semaphorins in the adult nervous system , 2003, Progress in Neurobiology.

[12]  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.

[13]  G. Raivich,et al.  Connective tissue growth factor: a novel marker of layer vii neurons in the rat cerebral cortex , 2003, Neuroscience.

[14]  A. Kolodkin,et al.  Semaphorin junction: making tracks toward neural connectivity , 2003, Current Opinion in Neurobiology.

[15]  T. Kaneko,et al.  Evidence that Sema3A and Sema3F regulate the migration of GABAergic neurons in the developing neocortex , 2003, The Journal of comparative neurology.

[16]  B. Schlosshauer,et al.  Semaphorin 3E/collapsin-5 inhibits growing retinal axons. , 2002, Experimental cell research.

[17]  J. Rubenstein,et al.  Sorting of Striatal and Cortical Interneurons Regulated by Semaphorin-Neuropilin Interactions , 2001, Science.

[18]  F. Fujiyama,et al.  Immunocytochemical localization of candidates for vesicular glutamate transporters in the rat cerebral cortex , 2001, The Journal of comparative neurology.

[19]  R. Kötter,et al.  Layer-Specific Intracolumnar and Transcolumnar Functional Connectivity of Layer V Pyramidal Cells in Rat Barrel Cortex , 2001, The Journal of Neuroscience.

[20]  F. Briggs,et al.  Layer-Specific Input to Distinct Cell Types in Layer 6 of Monkey Primary Visual Cortex , 2001, The Journal of Neuroscience.

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

[22]  T. Hashikawa,et al.  Differential expression of γ‐aminobutyric acid type B receptor‐1a and ‐1b mRNA variants in GABA and non‐GABAergic neurons of the rat brain , 2000 .

[23]  A. Toga,et al.  The Rhesus Monkey Brain in Stereotaxic Coordinates , 1999 .

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

[25]  T. Furuyama,et al.  Developmental localization of semaphorin H messenger RNA acting as a collapsing factor on sensory axons in the mouse brain , 1999, Neuroscience.

[26]  L. Cauller,et al.  Widespread projections from subgriseal neurons (layer VII) to layer I in adult rat cortex , 1999, The Journal of comparative neurology.

[27]  N. Chaudhari,et al.  An Optimized Method for In Situ Hybridization with Signal Amplification That Allows the Detection of Rare mRNAs , 1999, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

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

[29]  Alex L Kolodkin,et al.  Neuropilin-2 Is a Receptor for Semaphorin IV Insight into the Structural Basis of Receptor Function and Specificity , 1998, Neuron.

[30]  R. Kalb,et al.  Semaphorins A and E act as antagonists of neuropilin-1 and agonists of neuropilin-2 receptors , 1998, Nature Neuroscience.

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

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

[33]  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.

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

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

[36]  D. Fitzpatrick,et al.  The sublaminar organization of corticogeniculate neurons in layer 6 of macaque striate cortex , 1994, Visual Neuroscience.

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

[38]  Yamamura Ken-ichi,et al.  Efficient selection for high-expression transfectants with a novel eukaryotic vector , 1991 .

[39]  H. Niwa,et al.  Efficient selection for high-expression transfectants with a novel eukaryotic vector. , 1991, Gene.

[40]  D. Raczkowski,et al.  Sublaminar organization within layer VI of the striate cortex in Galago , 1990, The Journal of comparative neurology.

[41]  H. Killackey,et al.  Laminar and areal differences in the origin of the subcortical projection neurons of the rat somatosensory cortex , 1989, The Journal of comparative neurology.

[42]  P S Goldman-Rakic,et al.  Mediodorsal nucleus: Areal, laminar, and tangential distribution of afferents and efferents in the frontal lobe of rhesus monkeys , 1988, The Journal of comparative neurology.

[43]  H. Kennedy,et al.  A double-labeling investigation of the afferent connectivity to cortical areas V1 and V2 of the macaque monkey , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[44]  M. Glickstein,et al.  Corticopontine projection in the macaque: The distribution of labelled cortical cells after large injections of horseradish peroxidase in the pontine nuclei , 1985, The Journal of comparative neurology.

[45]  T. L. Neal,et al.  The rat claustrum: Afferent and efferent connections with visual cortex , 1985, Brain Research.

[46]  W. Fries Cortical projections to the superior colliculus in the macaque monkey: A retrograde study using horseradish peroxidase , 1984, The Journal of comparative neurology.

[47]  H Sherk,et al.  The visual claustrum of the cat. I. Structure and connections , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[48]  E. Murray,et al.  Organization of corticospinal neurons in the monkey , 1981, The Journal of comparative neurology.

[49]  Mark F. Bear,et al.  The laminar organization of the reciprocal projections between the claustrum and striate cortex in the tree shrew, Tupaia glis , 1980, Brain Research.

[50]  K. Rockland,et al.  Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey , 1979, Brain Research.

[51]  S P Wise,et al.  Size, laminar and columnar distribution of efferent cells in the sensory‐motor cortex of monkeys , 1977, The Journal of comparative neurology.

[52]  S. Wise,et al.  Cells of origin and terminal distribution of descending projections of the rat somatic sensory cortex , 1977, The Journal of comparative neurology.

[53]  S. Jacobson,et al.  The morphology and laminar distribution of cortico-pulvinar neurons in the Rhesus monkey , 1977, Experimental Brain Research.

[54]  J. Trojanowski,et al.  Corticothalamic neurons and thalamocortical terminal fields: An investigation in rat using horseradish peroxidase and autoradiography , 1975, Brain Research.

[55]  M. Tessier-Lavigne,et al.  Neuropilins as Semaphorin receptors: in vivo functions in neuronal cell migration and axon guidance. , 2002, Advances in experimental medicine and biology.

[56]  M. Tessier-Lavigne,et al.  Neuropilins as Semaphorin Receptors , 2002 .

[57]  Hwai-Jong Cheng,et al.  Alkaline phosphatase fusion proteins for molecular characterization and cloning of receptors and their ligands. , 2000, Methods in enzymology.

[58]  N. Nomura,et al.  Construction and characterization of human brain cDNA libraries suitable for analysis of cDNA clones encoding relatively large proteins. , 1997, DNA research : an international journal for rapid publication of reports on genes and genomes.

[59]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[60]  M. Glickstein,et al.  Corticopontine projection in the rat: The distribution of labelled cortical cells after large injections of horseradish peroxidase in the pontine nuclei , 1989, The Journal of comparative neurology.

[61]  D. Pandya,et al.  Architecture and Connections of Cortical Association Areas , 1985 .

[62]  J. Kaas,et al.  What, if anything, is SI? Organization of first somatosensory area of cortex. , 1983, Physiological reviews.