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Expression of the immunoglobulin superfamily cell adhesion molecules in the developing spinal cord and dorsal root ganglion.

Gu Z, Imai F, Kim IJ, Fujita H, Katayama Ki, Mori K, Yoshihara Y, Yoshida Y - PLoS ONE (2015)

Bottom Line: Further analyses show that Ocam is expressed by obturator but not quadriceps motor neurons, suggesting that Ocam may regulate sensory-motor specificity in these sensory-motor reflex arcs.Since a subset of Ocam+ motor neurons also express Alcam, Alcam or other functionally redundant IgSF molecules may compensate for Ocam in controlling sensory-motor specificity.Taken together, these results reveal that IgSF molecules are broadly expressed by sensory and motor neurons during development, and that Ocam and other IgSF molecules may have redundant functions in controlling the specificity of sensory-motor circuits.

View Article: PubMed Central - PubMed

Affiliation: Division of Developmental Biology, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio, United States of America.

ABSTRACT
Cell adhesion molecules belonging to the immunoglobulin superfamily (IgSF) control synaptic specificity through hetero- or homophilic interactions in different regions of the nervous system. In the developing spinal cord, monosynaptic connections of exquisite specificity form between proprioceptive sensory neurons and motor neurons, however, it is not known whether IgSF molecules participate in regulating this process. To determine whether IgSF molecules influence the establishment of synaptic specificity in sensory-motor circuits, we examined the expression of 157 IgSF genes in the developing dorsal root ganglion (DRG) and spinal cord by in situ hybridization assays. We find that many IgSF genes are expressed by sensory and motor neurons in the mouse developing DRG and spinal cord. For instance, Alcam, Mcam, and Ocam are expressed by a subset of motor neurons in the ventral spinal cord. Further analyses show that Ocam is expressed by obturator but not quadriceps motor neurons, suggesting that Ocam may regulate sensory-motor specificity in these sensory-motor reflex arcs. Electrophysiological analysis shows no obvious defects in synaptic specificity of monosynaptic sensory-motor connections involving obturator and quadriceps motor neurons in Ocam mutant mice. Since a subset of Ocam+ motor neurons also express Alcam, Alcam or other functionally redundant IgSF molecules may compensate for Ocam in controlling sensory-motor specificity. Taken together, these results reveal that IgSF molecules are broadly expressed by sensory and motor neurons during development, and that Ocam and other IgSF molecules may have redundant functions in controlling the specificity of sensory-motor circuits.

No MeSH data available.


Related in: MedlinePlus

Expression of Alcam in the developing DRG and spinal cor.(A-I) In situ hybridizations for Alcam on lumbar spinal cord sections from E16.5 (A-C), P0 (D-F), and P4 (G-I) wild-type mice. Alcam was strongly expressed by a subset of sensory and motor neurons at E16.5. Alcam was ubiquitously expressed in the spinal cord at P0 and P4.
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pone.0121550.g002: Expression of Alcam in the developing DRG and spinal cor.(A-I) In situ hybridizations for Alcam on lumbar spinal cord sections from E16.5 (A-C), P0 (D-F), and P4 (G-I) wild-type mice. Alcam was strongly expressed by a subset of sensory and motor neurons at E16.5. Alcam was ubiquitously expressed in the spinal cord at P0 and P4.

Mentions: To identify the IgSF molecules that regulate sensory-motor specificity, we examined 157 genes encoding IgSF cell adhesion molecules [14] for their expression profiles in embryonic day (E) 14.5-E16.5 DRGs and spinal cords at lumbar levels. We used E14.5-16.5 embryos since sensory-motor connections are already detected in the lumbar region as early as E17.5 [9,15] suggesting that molecules involved in sensory-motor specificity would be expressed earlier by proprioceptive sensory and/or motor neurons. Sensory-motor circuits are formed between presynaptic proprioceptive sensory neurons (marked by the expression of Pv, a specific proprioceptive marker [16,17]) (Fig. 1A, 1C), and postsynaptic motor neurons in the ventral spinal cord (identified by Islet-1) (Fig. 1A-1B). Fig. 1, S1, and S2 showed the expression patterns of representative IgSF genes at E15.5. CD83 was expressed by a subset of motor neurons in the ventral spinal cord as well as a subset of DRG sensory neurons (Fig. 1D-1E). Neurotractin was expressed by most spinal cord neurons, with particularly strong expression in motor neurons within the ventral spinal cord (Fig. 1F). Neurotractin was also strongly expressed by a subset of sensory neurons (Fig. 1F-1G). Lrrn 2 was expressed by a subset of sensory and motor neurons (Fig. 1H-1I), while expression of Lrrn 3 was restricted to a subset of motor neurons (Fig. 1J). Expression of Vstm5 was detected in the ventral spinal cord, with strong expression in a subset of motor neurons (Fig. 1L). Vstm5 was also expressed by a subset of sensory neurons (Fig. 1L-1M). Basigin was expressed by most spinal cord neurons, with motor neurons exhibiting the strongest expression (Fig. 1N). In addition, Basigin was expressed in tubular structures (likely endothelial cells) (Fig. 1N) and some DRG sensory neurons (Fig. 1N-1O). There was a gradient of SDR-1 expression in the spinal cord (Fig. 1P). SDR-1 was strongly expressed in the ventral spinal cord, and weakly expressed in the dorsal spinal cord (Fig. 1P). SDR-1 was also strongly expressed by a subset of DRG neurons and weakly expressed by other DRG neurons (Fig. 1P-1Q). Other IgSF genes (Camd4, Chl1, Dscaml1, Iglon5) were expressed in both the DRG and the spinal cord (S1 FigA-1L) while Pvrl3 and Bcam were expressed by a subset of sensory and motor neurons (S1 FigM–S1O and S2). Moreover, since Alcam, Mcam and Ocam displayed more specific expression patterns in the spinal cord than other genes, we performed more detailed examinations of these genes at different developmental stages (see Fig.2–7). In summary, many IgSF genes are expressed by sensory and motor neurons at E15.5, a time just prior to the formation of sensory-motor connections, suggesting that IgSF proteins may participate in establishing these circuits.


Expression of the immunoglobulin superfamily cell adhesion molecules in the developing spinal cord and dorsal root ganglion.

Gu Z, Imai F, Kim IJ, Fujita H, Katayama Ki, Mori K, Yoshihara Y, Yoshida Y - PLoS ONE (2015)

Expression of Alcam in the developing DRG and spinal cor.(A-I) In situ hybridizations for Alcam on lumbar spinal cord sections from E16.5 (A-C), P0 (D-F), and P4 (G-I) wild-type mice. Alcam was strongly expressed by a subset of sensory and motor neurons at E16.5. Alcam was ubiquitously expressed in the spinal cord at P0 and P4.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4380438&req=5

pone.0121550.g002: Expression of Alcam in the developing DRG and spinal cor.(A-I) In situ hybridizations for Alcam on lumbar spinal cord sections from E16.5 (A-C), P0 (D-F), and P4 (G-I) wild-type mice. Alcam was strongly expressed by a subset of sensory and motor neurons at E16.5. Alcam was ubiquitously expressed in the spinal cord at P0 and P4.
Mentions: To identify the IgSF molecules that regulate sensory-motor specificity, we examined 157 genes encoding IgSF cell adhesion molecules [14] for their expression profiles in embryonic day (E) 14.5-E16.5 DRGs and spinal cords at lumbar levels. We used E14.5-16.5 embryos since sensory-motor connections are already detected in the lumbar region as early as E17.5 [9,15] suggesting that molecules involved in sensory-motor specificity would be expressed earlier by proprioceptive sensory and/or motor neurons. Sensory-motor circuits are formed between presynaptic proprioceptive sensory neurons (marked by the expression of Pv, a specific proprioceptive marker [16,17]) (Fig. 1A, 1C), and postsynaptic motor neurons in the ventral spinal cord (identified by Islet-1) (Fig. 1A-1B). Fig. 1, S1, and S2 showed the expression patterns of representative IgSF genes at E15.5. CD83 was expressed by a subset of motor neurons in the ventral spinal cord as well as a subset of DRG sensory neurons (Fig. 1D-1E). Neurotractin was expressed by most spinal cord neurons, with particularly strong expression in motor neurons within the ventral spinal cord (Fig. 1F). Neurotractin was also strongly expressed by a subset of sensory neurons (Fig. 1F-1G). Lrrn 2 was expressed by a subset of sensory and motor neurons (Fig. 1H-1I), while expression of Lrrn 3 was restricted to a subset of motor neurons (Fig. 1J). Expression of Vstm5 was detected in the ventral spinal cord, with strong expression in a subset of motor neurons (Fig. 1L). Vstm5 was also expressed by a subset of sensory neurons (Fig. 1L-1M). Basigin was expressed by most spinal cord neurons, with motor neurons exhibiting the strongest expression (Fig. 1N). In addition, Basigin was expressed in tubular structures (likely endothelial cells) (Fig. 1N) and some DRG sensory neurons (Fig. 1N-1O). There was a gradient of SDR-1 expression in the spinal cord (Fig. 1P). SDR-1 was strongly expressed in the ventral spinal cord, and weakly expressed in the dorsal spinal cord (Fig. 1P). SDR-1 was also strongly expressed by a subset of DRG neurons and weakly expressed by other DRG neurons (Fig. 1P-1Q). Other IgSF genes (Camd4, Chl1, Dscaml1, Iglon5) were expressed in both the DRG and the spinal cord (S1 FigA-1L) while Pvrl3 and Bcam were expressed by a subset of sensory and motor neurons (S1 FigM–S1O and S2). Moreover, since Alcam, Mcam and Ocam displayed more specific expression patterns in the spinal cord than other genes, we performed more detailed examinations of these genes at different developmental stages (see Fig.2–7). In summary, many IgSF genes are expressed by sensory and motor neurons at E15.5, a time just prior to the formation of sensory-motor connections, suggesting that IgSF proteins may participate in establishing these circuits.

Bottom Line: Further analyses show that Ocam is expressed by obturator but not quadriceps motor neurons, suggesting that Ocam may regulate sensory-motor specificity in these sensory-motor reflex arcs.Since a subset of Ocam+ motor neurons also express Alcam, Alcam or other functionally redundant IgSF molecules may compensate for Ocam in controlling sensory-motor specificity.Taken together, these results reveal that IgSF molecules are broadly expressed by sensory and motor neurons during development, and that Ocam and other IgSF molecules may have redundant functions in controlling the specificity of sensory-motor circuits.

View Article: PubMed Central - PubMed

Affiliation: Division of Developmental Biology, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio, United States of America.

ABSTRACT
Cell adhesion molecules belonging to the immunoglobulin superfamily (IgSF) control synaptic specificity through hetero- or homophilic interactions in different regions of the nervous system. In the developing spinal cord, monosynaptic connections of exquisite specificity form between proprioceptive sensory neurons and motor neurons, however, it is not known whether IgSF molecules participate in regulating this process. To determine whether IgSF molecules influence the establishment of synaptic specificity in sensory-motor circuits, we examined the expression of 157 IgSF genes in the developing dorsal root ganglion (DRG) and spinal cord by in situ hybridization assays. We find that many IgSF genes are expressed by sensory and motor neurons in the mouse developing DRG and spinal cord. For instance, Alcam, Mcam, and Ocam are expressed by a subset of motor neurons in the ventral spinal cord. Further analyses show that Ocam is expressed by obturator but not quadriceps motor neurons, suggesting that Ocam may regulate sensory-motor specificity in these sensory-motor reflex arcs. Electrophysiological analysis shows no obvious defects in synaptic specificity of monosynaptic sensory-motor connections involving obturator and quadriceps motor neurons in Ocam mutant mice. Since a subset of Ocam+ motor neurons also express Alcam, Alcam or other functionally redundant IgSF molecules may compensate for Ocam in controlling sensory-motor specificity. Taken together, these results reveal that IgSF molecules are broadly expressed by sensory and motor neurons during development, and that Ocam and other IgSF molecules may have redundant functions in controlling the specificity of sensory-motor circuits.

No MeSH data available.


Related in: MedlinePlus