Emerging roles for semaphorins and VEGFs in synaptogenesis and synaptic plasticity

Synapse formation, maintenance and plasticity are critical for the correct function of the nervous system and its target organs. During development, these processes enable the establishment of appropriate neural circuits. During adulthood, they allow adaptation to both physiological and environmental changes. In this review, we discuss emerging roles for two families of classical axon and vascular guidance cues in synaptogenesis and synaptic plasticity, the semaphorins and the vascular endothelial growth factors (VEGFs). Their contribution to synapse formation and function add a new facet to the spectrum of overlapping and complementary roles for these molecules in development, adulthood and disease.

[1]  S. Koch,et al.  Signal transduction by vascular endothelial growth factor receptors. , 2012, Cold Spring Harbor perspectives in medicine.

[2]  Kihwan Lee,et al.  An Activity-Regulated microRNA, miR-188, Controls Dendritic Plasticity and Synaptic Transmission by Downregulating Neuropilin-2 , 2012, The Journal of Neuroscience.

[3]  F. Mackenzie,et al.  Diverse roles for VEGF-A in the nervous system , 2012, Development.

[4]  B. Sabatini,et al.  Semaphorin 3E–Plexin-D1 signaling controls pathway-specific synapse formation in the striatum , 2011, Nature Neuroscience.

[5]  Paul Antoine Salin,et al.  VEGF modulates NMDA receptors activity in cerebellar granule cells through Src-family kinases before synapse formation , 2011, Proceedings of the National Academy of Sciences.

[6]  H. Bading,et al.  Nuclear Calcium-VEGFD Signaling Controls Maintenance of Dendrite Arborization Necessary for Memory Formation , 2011, Neuron.

[7]  C. Ruhrberg,et al.  VEGF Signaling through Neuropilin 1 Guides Commissural Axon Crossing at the Optic Chiasm , 2011, Neuron.

[8]  P. Carmeliet,et al.  VEGF Mediates Commissural Axon Chemoattraction through Its Receptor Flk1 , 2011, Neuron.

[9]  G. Mitchell,et al.  Spinal Vascular Endothelial Growth Factor Induces Phrenic Motor Facilitation via Extracellular Signal-Regulated Kinase and Akt Signaling , 2011, The Journal of Neuroscience.

[10]  Tamar Licht,et al.  Reversible modulations of neuronal plasticity by VEGF , 2011, Proceedings of the National Academy of Sciences.

[11]  W. Robberecht,et al.  VEGF protects motor neurons against excitotoxicity by upregulation of GluR2 , 2010, Neurobiology of Aging.

[12]  P. Verstreken,et al.  Impaired Autonomic Regulation of Resistance Arteries in Mice With Low Vascular Endothelial Growth Factor or Upon Vascular Endothelial Growth Factor Trap Delivery , 2010, Circulation.

[13]  Pierre Vanderhaeghen,et al.  Guidance molecules in axon pruning and cell death. , 2010, Cold Spring Harbor perspectives in biology.

[14]  R. Adams,et al.  Axon guidance molecules in vascular patterning. , 2010, Cold Spring Harbor perspectives in biology.

[15]  G. Rougon,et al.  VEGFR2 (KDR/Flk1) Signaling Mediates Axon Growth in Response to Semaphorin 3E in the Developing Brain , 2010, Neuron.

[16]  K. Hsu,et al.  Pharmacological and Genetic Accumulation of Hypoxia-Inducible Factor-1α Enhances Excitatory Synaptic Transmission in Hippocampal Neurons through the Production of Vascular Endothelial Growth Factor , 2010, The Journal of Neuroscience.

[17]  K. Shen,et al.  Guidance molecules in synapse formation and plasticity. , 2010, Cold Spring Harbor perspectives in biology.

[18]  Diether Lambrechts,et al.  Downregulation of genes with a function in axon outgrowth and synapse formation in motor neurones of the VEGFδ/δ mouse model of amyotrophic lateral sclerosis , 2010, BMC Genomics.

[19]  I. Goshen,et al.  VEGF is required for dendritogenesis of newly born olfactory bulb interneurons , 2010, Development.

[20]  R. Huganir,et al.  Secreted Semaphorins Control Spine Distribution and Morphogenesis in the Postnatal CNS , 2009, Nature.

[21]  Wa Shen,et al.  Semaphorin3a regulates endothelial cell number and podocyte differentiation during glomerular development , 2009, Development.

[22]  N. Bresolin,et al.  VEGF genetic variability is associated with increased risk of developing Alzheimer's disease , 2009, Journal of the Neurological Sciences.

[23]  T. O'Connor,et al.  Semaphorin 5B mediates synapse elimination in hippocampal neurons , 2009, Neural Development.

[24]  K. Alitalo,et al.  VEGFs and receptors involved in angiogenesis versus lymphangiogenesis. , 2009, Current opinion in cell biology.

[25]  H. Scharfman,et al.  Modulation of vascular endothelial growth factor (VEGF) expression in motor neurons and its electrophysiological effects , 2008, Brain Research Bulletin.

[26]  June-Seek Choi,et al.  Vascular endothelial growth factor (VEGF) signaling regulates hippocampal neurons by elevation of intracellular calcium and activation of calcium/calmodulin protein kinase II and mammalian target of rapamycin. , 2008, Cellular signalling.

[27]  R. Pasterkamp,et al.  Semaphorin signaling: progress made and promises ahead. , 2008, Trends in biochemical sciences.

[28]  H. Scharfman,et al.  Vascular endothelial growth factor is up-regulated after status epilepticus and protects against seizure-induced neuronal loss in hippocampus , 2008, Neuroscience.

[29]  B. Fadeel,et al.  VEGF reduces astrogliosis and preserves neuromuscular junctions in ALS transgenic mice. , 2007, Biochemical and biophysical research communications.

[30]  P. Greengard,et al.  Cyclin-dependent kinase 5 governs learning and synaptic plasticity via control of NMDAR degradation , 2007, Nature Neuroscience.

[31]  G. Rougon,et al.  Semaphorins in development and adult brain: Implication for neurological diseases , 2007, Progress in Neurobiology.

[32]  Eric C. Griffith,et al.  An RNAi-Based Approach Identifies Molecules Required for Glutamatergic and GABAergic Synapse Development , 2007, Neuron.

[33]  C. Gillberg,et al.  Constitutional Downregulation of SEMA5A Expression in Autism , 2006, Neuropsychobiology.

[34]  H. Gohlke,et al.  Possible gender-dependent association of vascular endothelial growth factor (VEGF) gene and ALS , 2006, Neurology.

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

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

[37]  P. Carmeliet,et al.  VEGF-C is a trophic factor for neural progenitors in the vertebrate embryonic brain , 2006, Nature Neuroscience.

[38]  K. Jin,et al.  Vascular endothelial growth factor-B (VEGFB) stimulates neurogenesis: evidence from knockout mice and growth factor administration. , 2006, Developmental biology.

[39]  H. Scharfman,et al.  Depression of Synaptic Transmission by Vascular Endothelial Growth Factor in Adult Rat Hippocampus and Evidence for Increased Efficacy after Chronic Seizures , 2005, The Journal of Neuroscience.

[40]  C. Garner,et al.  Semaphorin 4B interacts with the post‐synaptic density protein PSD‐95/SAP90 and is recruited to synapses through a C‐terminal PDZ‐binding motif , 2005, FEBS letters.

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

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

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

[44]  J. Epstein,et al.  PlexinD1 and semaphorin signaling are required in endothelial cells for cardiovascular development. , 2004, Developmental cell.

[45]  J. Rosenstein,et al.  Neurotrophic Effects of Vascular Endothelial Growth Factor on Organotypic Cortical Explants and Primary Cortical Neurons , 2003, The Journal of Neuroscience.

[46]  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.

[47]  Yi Li,et al.  Statins induce angiogenesis, neurogenesis, and synaptogenesis after stroke , 2003, Annals of neurology.

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

[49]  C. Goodman,et al.  Bi-directional signaling by Semaphorin 1a during central synapse formation in Drosophila , 2002, Nature Neuroscience.

[50]  W. Stewart,et al.  Disrupted synaptic development in the hypoxic newborn brain , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[51]  Steven A. Goldman,et al.  Coordinated Interaction of Neurogenesis and Angiogenesis in the Adult Songbird Brain , 2002, Neuron.

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

[53]  E. Gundelfinger,et al.  Semaphorin4F interacts with the synapse‐associated protein SAP90/PSD‐95 , 2001, Journal of neurochemistry.

[54]  T. Furuyama,et al.  Sema4C, a Transmembrane Semaphorin, Interacts with a Post-synaptic Density Protein, PSD-95* , 2001, The Journal of Biological Chemistry.

[55]  G. Mckhann.  VEGF Links Hippocampal Activity with Neurogenesis, Learning, and Memory. , 2005, Neurosurgery.

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

[57]  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.

[58]  Till Acker,et al.  Deletion of the hypoxia-response element in the vascular endothelial growth factor promoter causes motor neuron degeneration , 2001, Nature Genetics.