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Developmental waves of mechanosensitivity acquisition in sensory neuron subtypes during embryonic development.

Lechner SG, Frenzel H, Wang R, Lewin GR - EMBO J. (2009)

Bottom Line: Sensory neurons that are mechanoreceptors or proprioceptors acquire mature mechanotransduction indistinguishable from the adult already at E13.In contrast, most nociceptive (pain sensing) sensory neurons acquire mechanosensitive competence as a result of exposure to target-derived nerve growth factor.The highly regulated process of mechanosensory acquisition unveiled here, reveals new strategies to identify molecules required for sensory neuron mechanotransduction.

View Article: PubMed Central - PubMed

Affiliation: Department of Neuroscience, Max-Delbrück Center for Molecular Medicine, Berlin-Buch, Germany.

ABSTRACT
Somatic sensation relies on the transduction of physical stimuli into electrical signals by sensory neurons of the dorsal root ganglia. Little is known about how and when during development different types of sensory neurons acquire transduction competence. We directly investigated the emergence of electrical excitability and mechanosensitivity of embryonic and postnatal mouse sensory neurons. We show that sensory neurons acquire mechanotransduction competence coincident with peripheral target innervation. Mechanotransduction competence arises in different sensory lineages in waves, coordinated by distinct developmental mechanisms. Sensory neurons that are mechanoreceptors or proprioceptors acquire mature mechanotransduction indistinguishable from the adult already at E13. This process is independent of neurotrophin-3 and may be driven by a genetic program. In contrast, most nociceptive (pain sensing) sensory neurons acquire mechanosensitive competence as a result of exposure to target-derived nerve growth factor. The highly regulated process of mechanosensory acquisition unveiled here, reveals new strategies to identify molecules required for sensory neuron mechanotransduction.

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Correlation between Trk-receptor expression and cell size. (A) Photomicrograph and size frequency distribution of acutely dissociated E13.5 DRGs in culture. Note, only large neurons are mechanosensitive at this stage (blue arrows). (B–D) TrkA, TrkB and TrkC receptor expression in E13.5 whole mount DRGs was examined using in situ hybridization. Size frequency distribution of TrkC, TrkB and trkA-expressing neurons reveals that the subpopulation of large cells is almost exclusively TrkB and/or TrkC-positive (blue bars), whereas TrkA expression is primarily found in small cells (red bars).
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f3: Correlation between Trk-receptor expression and cell size. (A) Photomicrograph and size frequency distribution of acutely dissociated E13.5 DRGs in culture. Note, only large neurons are mechanosensitive at this stage (blue arrows). (B–D) TrkA, TrkB and TrkC receptor expression in E13.5 whole mount DRGs was examined using in situ hybridization. Size frequency distribution of TrkC, TrkB and trkA-expressing neurons reveals that the subpopulation of large cells is almost exclusively TrkB and/or TrkC-positive (blue bars), whereas TrkA expression is primarily found in small cells (red bars).

Mentions: Large sensory neurons with the electrophysiological properties of early born mechanoreceptors acquire mechanosensitivity during target innervation at E13.5 (Figure 2A). Using in situ hybridization, we showed that the distinctive population of neurons with large cell diameters that emerge at E13.5 are almost all TrkC+ or TrkB+, whereas small diameter neurons do not express TrkC or TrkB (Figure 3B–D). In contrast, almost all small sensory neurons express TrkA, but the TrkA receptor message was not detected in larger mechanosensitive neurons (Figure 3). Single-cell PCR experiments confirmed these results (Figure 2E).


Developmental waves of mechanosensitivity acquisition in sensory neuron subtypes during embryonic development.

Lechner SG, Frenzel H, Wang R, Lewin GR - EMBO J. (2009)

Correlation between Trk-receptor expression and cell size. (A) Photomicrograph and size frequency distribution of acutely dissociated E13.5 DRGs in culture. Note, only large neurons are mechanosensitive at this stage (blue arrows). (B–D) TrkA, TrkB and TrkC receptor expression in E13.5 whole mount DRGs was examined using in situ hybridization. Size frequency distribution of TrkC, TrkB and trkA-expressing neurons reveals that the subpopulation of large cells is almost exclusively TrkB and/or TrkC-positive (blue bars), whereas TrkA expression is primarily found in small cells (red bars).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2664657&req=5

f3: Correlation between Trk-receptor expression and cell size. (A) Photomicrograph and size frequency distribution of acutely dissociated E13.5 DRGs in culture. Note, only large neurons are mechanosensitive at this stage (blue arrows). (B–D) TrkA, TrkB and TrkC receptor expression in E13.5 whole mount DRGs was examined using in situ hybridization. Size frequency distribution of TrkC, TrkB and trkA-expressing neurons reveals that the subpopulation of large cells is almost exclusively TrkB and/or TrkC-positive (blue bars), whereas TrkA expression is primarily found in small cells (red bars).
Mentions: Large sensory neurons with the electrophysiological properties of early born mechanoreceptors acquire mechanosensitivity during target innervation at E13.5 (Figure 2A). Using in situ hybridization, we showed that the distinctive population of neurons with large cell diameters that emerge at E13.5 are almost all TrkC+ or TrkB+, whereas small diameter neurons do not express TrkC or TrkB (Figure 3B–D). In contrast, almost all small sensory neurons express TrkA, but the TrkA receptor message was not detected in larger mechanosensitive neurons (Figure 3). Single-cell PCR experiments confirmed these results (Figure 2E).

Bottom Line: Sensory neurons that are mechanoreceptors or proprioceptors acquire mature mechanotransduction indistinguishable from the adult already at E13.In contrast, most nociceptive (pain sensing) sensory neurons acquire mechanosensitive competence as a result of exposure to target-derived nerve growth factor.The highly regulated process of mechanosensory acquisition unveiled here, reveals new strategies to identify molecules required for sensory neuron mechanotransduction.

View Article: PubMed Central - PubMed

Affiliation: Department of Neuroscience, Max-Delbrück Center for Molecular Medicine, Berlin-Buch, Germany.

ABSTRACT
Somatic sensation relies on the transduction of physical stimuli into electrical signals by sensory neurons of the dorsal root ganglia. Little is known about how and when during development different types of sensory neurons acquire transduction competence. We directly investigated the emergence of electrical excitability and mechanosensitivity of embryonic and postnatal mouse sensory neurons. We show that sensory neurons acquire mechanotransduction competence coincident with peripheral target innervation. Mechanotransduction competence arises in different sensory lineages in waves, coordinated by distinct developmental mechanisms. Sensory neurons that are mechanoreceptors or proprioceptors acquire mature mechanotransduction indistinguishable from the adult already at E13. This process is independent of neurotrophin-3 and may be driven by a genetic program. In contrast, most nociceptive (pain sensing) sensory neurons acquire mechanosensitive competence as a result of exposure to target-derived nerve growth factor. The highly regulated process of mechanosensory acquisition unveiled here, reveals new strategies to identify molecules required for sensory neuron mechanotransduction.

Show MeSH
Related in: MedlinePlus