Limits...
Semaphorin signaling in vertebrate neural circuit assembly.

Yoshida Y - Front Mol Neurosci (2012)

Bottom Line: The major semaphorin receptors are plexins and neuropilins, however other receptors and co-receptors also mediate signaling by semaphorins.Upon semaphorin binding to their receptors, downstream signaling molecules transduce this event within cells to mediate further events, including alteration of microtubule and actin cytoskeletal dynamics.Here, I review recent studies on semaphorin signaling in vertebrate neural circuit assembly, with the goal of highlighting how this diverse family of cues and receptors imparts exquisite specificity to neural complex connectivity.

View Article: PubMed Central - PubMed

Affiliation: Division of Developmental Biology, Cincinnati Children's Hospital Medical Center Cincinnati, OH, USA.

ABSTRACT
Neural circuit formation requires the coordination of many complex developmental processes. First, neurons project axons over long distances to find their final targets and then establish appropriate connectivity essential for the formation of neuronal circuitry. Growth cones, the leading edges of axons, navigate by interacting with a variety of attractive and repulsive axon guidance cues along their trajectories and at final target regions. In addition to guidance of axons, neuronal polarization, neuronal migration, and dendrite development must be precisely regulated during development to establish proper neural circuitry. Semaphorins consist of a large protein family, which includes secreted and cell surface proteins, and they play important roles in many steps of neural circuit formation. The major semaphorin receptors are plexins and neuropilins, however other receptors and co-receptors also mediate signaling by semaphorins. Upon semaphorin binding to their receptors, downstream signaling molecules transduce this event within cells to mediate further events, including alteration of microtubule and actin cytoskeletal dynamics. Here, I review recent studies on semaphorin signaling in vertebrate neural circuit assembly, with the goal of highlighting how this diverse family of cues and receptors imparts exquisite specificity to neural complex connectivity.

No MeSH data available.


Related in: MedlinePlus

Roles of semaphorin-plexin signaling in sensory-motor circuitry. (A) Cross-sectional diagrams depicting the dorsal spinal cords of wild-type, PlexA1, and Sema6D, and oligodendrocyte-deleted Sema6D mutant mice used in two studies (Yoshida et al., 2006; Leslie et al., 2011). Proprioceptive axons (red lines), oligodendrocytes (blue circles), cutaneous axons (green lines), cutaneous synapses (green wavy lines). Blue areas show Sema6D-expressing region. PlexA1 is expressed by proprioceptive sensory neurons but not cutaneous sensory neurons. Cutaneous synapses are disrupted when oligodendrocytes aberrantly enter the dorsal horn, whereas genetic deletion of oligodendrocytes from Sema6D mutants rescues these synaptic defects. (B) Cross-sectional diagrams depicting the spinal cords of wild-type, PlexD1, and Sema3E mutant mice as well as motor neuron-specific Sema3E-expressing mice (Pecho-Vrieseling et al., 2009). Motor neurons innervating triceps (Tri) muscle receive monosynaptic inputs from Tri sensory afferents, whereas cutaneous maximus (CM) motor neurons lack monosynaptic inputs from CM sensory afferents. Sema3E is expressed by CM motor neurons but not Tri motor neurons. PlexD1 is expressed by ∼80% of CM proprioceptive sensory neurons, and ∼50% of Tri proprioceptive sensory neurons. Absence of Sema3E-PlexD1 signaling causes aberrant monosynaptic sensory-motor connections between CM sensory and CM motor neurons. Ectopic expression of Sema3E in Tri motor neurons reduces monosynaptic connections between Tri afferents and Tri motor neurons.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC3368236&req=5

Figure 4: Roles of semaphorin-plexin signaling in sensory-motor circuitry. (A) Cross-sectional diagrams depicting the dorsal spinal cords of wild-type, PlexA1, and Sema6D, and oligodendrocyte-deleted Sema6D mutant mice used in two studies (Yoshida et al., 2006; Leslie et al., 2011). Proprioceptive axons (red lines), oligodendrocytes (blue circles), cutaneous axons (green lines), cutaneous synapses (green wavy lines). Blue areas show Sema6D-expressing region. PlexA1 is expressed by proprioceptive sensory neurons but not cutaneous sensory neurons. Cutaneous synapses are disrupted when oligodendrocytes aberrantly enter the dorsal horn, whereas genetic deletion of oligodendrocytes from Sema6D mutants rescues these synaptic defects. (B) Cross-sectional diagrams depicting the spinal cords of wild-type, PlexD1, and Sema3E mutant mice as well as motor neuron-specific Sema3E-expressing mice (Pecho-Vrieseling et al., 2009). Motor neurons innervating triceps (Tri) muscle receive monosynaptic inputs from Tri sensory afferents, whereas cutaneous maximus (CM) motor neurons lack monosynaptic inputs from CM sensory afferents. Sema3E is expressed by CM motor neurons but not Tri motor neurons. PlexD1 is expressed by ∼80% of CM proprioceptive sensory neurons, and ∼50% of Tri proprioceptive sensory neurons. Absence of Sema3E-PlexD1 signaling causes aberrant monosynaptic sensory-motor connections between CM sensory and CM motor neurons. Ectopic expression of Sema3E in Tri motor neurons reduces monosynaptic connections between Tri afferents and Tri motor neurons.

Mentions: Two studies on the role of the PlexA1 receptor and its ligand Sema6D demonstrate that Sema6D-PlexA1 signaling controls axon positioning of proprioceptive sensory neurons in the dorsal spinal cord (Yoshida et al., 2006; Leslie et al., 2011; Figure 4A). PlexA1 is exclusively expressed by proprioceptive sensory neurons in the DRG, and Sema6D is expressed in the dorsal spinal cord (Yoshida et al., 2006). In PlexA1 or Sema6D mutants, proprioceptive axons ectopically invade the dorsal horn (Yoshida et al., 2006; Leslie et al., 2011; Figure 4A). Since proprioceptive axons are heavily myelinated, and most cutaneous axons are thinly myelinated if at all, oligodendrocytes associated with proprioceptive axons invade the dorsal spinal cord, and then inhibit synapse formation in the absence of Sema6D-PlexA1 signaling (Yoshida et al., 2006; Leslie et al., 2011; Figure 4A). Genetic deletion of oligodendrocytes demonstrates that it is the ectopic oligodendrocytes, not proprioceptive axons, in the dorsal spinal cord that inhibit synapse formation, but not axonal growth, in Sema6D mutants (Leslie et al., 2011; Figure 4A). Therefore, ectopic oligodendrocytes in the dorsal spinal cord inhibit synapse formation in the absence of Sema6D-PlexA1 signaling.


Semaphorin signaling in vertebrate neural circuit assembly.

Yoshida Y - Front Mol Neurosci (2012)

Roles of semaphorin-plexin signaling in sensory-motor circuitry. (A) Cross-sectional diagrams depicting the dorsal spinal cords of wild-type, PlexA1, and Sema6D, and oligodendrocyte-deleted Sema6D mutant mice used in two studies (Yoshida et al., 2006; Leslie et al., 2011). Proprioceptive axons (red lines), oligodendrocytes (blue circles), cutaneous axons (green lines), cutaneous synapses (green wavy lines). Blue areas show Sema6D-expressing region. PlexA1 is expressed by proprioceptive sensory neurons but not cutaneous sensory neurons. Cutaneous synapses are disrupted when oligodendrocytes aberrantly enter the dorsal horn, whereas genetic deletion of oligodendrocytes from Sema6D mutants rescues these synaptic defects. (B) Cross-sectional diagrams depicting the spinal cords of wild-type, PlexD1, and Sema3E mutant mice as well as motor neuron-specific Sema3E-expressing mice (Pecho-Vrieseling et al., 2009). Motor neurons innervating triceps (Tri) muscle receive monosynaptic inputs from Tri sensory afferents, whereas cutaneous maximus (CM) motor neurons lack monosynaptic inputs from CM sensory afferents. Sema3E is expressed by CM motor neurons but not Tri motor neurons. PlexD1 is expressed by ∼80% of CM proprioceptive sensory neurons, and ∼50% of Tri proprioceptive sensory neurons. Absence of Sema3E-PlexD1 signaling causes aberrant monosynaptic sensory-motor connections between CM sensory and CM motor neurons. Ectopic expression of Sema3E in Tri motor neurons reduces monosynaptic connections between Tri afferents and Tri motor neurons.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3368236&req=5

Figure 4: Roles of semaphorin-plexin signaling in sensory-motor circuitry. (A) Cross-sectional diagrams depicting the dorsal spinal cords of wild-type, PlexA1, and Sema6D, and oligodendrocyte-deleted Sema6D mutant mice used in two studies (Yoshida et al., 2006; Leslie et al., 2011). Proprioceptive axons (red lines), oligodendrocytes (blue circles), cutaneous axons (green lines), cutaneous synapses (green wavy lines). Blue areas show Sema6D-expressing region. PlexA1 is expressed by proprioceptive sensory neurons but not cutaneous sensory neurons. Cutaneous synapses are disrupted when oligodendrocytes aberrantly enter the dorsal horn, whereas genetic deletion of oligodendrocytes from Sema6D mutants rescues these synaptic defects. (B) Cross-sectional diagrams depicting the spinal cords of wild-type, PlexD1, and Sema3E mutant mice as well as motor neuron-specific Sema3E-expressing mice (Pecho-Vrieseling et al., 2009). Motor neurons innervating triceps (Tri) muscle receive monosynaptic inputs from Tri sensory afferents, whereas cutaneous maximus (CM) motor neurons lack monosynaptic inputs from CM sensory afferents. Sema3E is expressed by CM motor neurons but not Tri motor neurons. PlexD1 is expressed by ∼80% of CM proprioceptive sensory neurons, and ∼50% of Tri proprioceptive sensory neurons. Absence of Sema3E-PlexD1 signaling causes aberrant monosynaptic sensory-motor connections between CM sensory and CM motor neurons. Ectopic expression of Sema3E in Tri motor neurons reduces monosynaptic connections between Tri afferents and Tri motor neurons.
Mentions: Two studies on the role of the PlexA1 receptor and its ligand Sema6D demonstrate that Sema6D-PlexA1 signaling controls axon positioning of proprioceptive sensory neurons in the dorsal spinal cord (Yoshida et al., 2006; Leslie et al., 2011; Figure 4A). PlexA1 is exclusively expressed by proprioceptive sensory neurons in the DRG, and Sema6D is expressed in the dorsal spinal cord (Yoshida et al., 2006). In PlexA1 or Sema6D mutants, proprioceptive axons ectopically invade the dorsal horn (Yoshida et al., 2006; Leslie et al., 2011; Figure 4A). Since proprioceptive axons are heavily myelinated, and most cutaneous axons are thinly myelinated if at all, oligodendrocytes associated with proprioceptive axons invade the dorsal spinal cord, and then inhibit synapse formation in the absence of Sema6D-PlexA1 signaling (Yoshida et al., 2006; Leslie et al., 2011; Figure 4A). Genetic deletion of oligodendrocytes demonstrates that it is the ectopic oligodendrocytes, not proprioceptive axons, in the dorsal spinal cord that inhibit synapse formation, but not axonal growth, in Sema6D mutants (Leslie et al., 2011; Figure 4A). Therefore, ectopic oligodendrocytes in the dorsal spinal cord inhibit synapse formation in the absence of Sema6D-PlexA1 signaling.

Bottom Line: The major semaphorin receptors are plexins and neuropilins, however other receptors and co-receptors also mediate signaling by semaphorins.Upon semaphorin binding to their receptors, downstream signaling molecules transduce this event within cells to mediate further events, including alteration of microtubule and actin cytoskeletal dynamics.Here, I review recent studies on semaphorin signaling in vertebrate neural circuit assembly, with the goal of highlighting how this diverse family of cues and receptors imparts exquisite specificity to neural complex connectivity.

View Article: PubMed Central - PubMed

Affiliation: Division of Developmental Biology, Cincinnati Children's Hospital Medical Center Cincinnati, OH, USA.

ABSTRACT
Neural circuit formation requires the coordination of many complex developmental processes. First, neurons project axons over long distances to find their final targets and then establish appropriate connectivity essential for the formation of neuronal circuitry. Growth cones, the leading edges of axons, navigate by interacting with a variety of attractive and repulsive axon guidance cues along their trajectories and at final target regions. In addition to guidance of axons, neuronal polarization, neuronal migration, and dendrite development must be precisely regulated during development to establish proper neural circuitry. Semaphorins consist of a large protein family, which includes secreted and cell surface proteins, and they play important roles in many steps of neural circuit formation. The major semaphorin receptors are plexins and neuropilins, however other receptors and co-receptors also mediate signaling by semaphorins. Upon semaphorin binding to their receptors, downstream signaling molecules transduce this event within cells to mediate further events, including alteration of microtubule and actin cytoskeletal dynamics. Here, I review recent studies on semaphorin signaling in vertebrate neural circuit assembly, with the goal of highlighting how this diverse family of cues and receptors imparts exquisite specificity to neural complex connectivity.

No MeSH data available.


Related in: MedlinePlus