Muscle-selective RUNX3 dependence of sensorimotor circuit development

Yiqiao Wang; Haohao Wu; Pavel Zelenin; Paula Fontanet; Simone Wanderoy; Charles Petitpré; Glenda Comai; Carmelo Bellardita; Yongtao Xue-Franzén; Rosa Eva Huettl; Andrea B. Huber; Shahragim Tajbakhsh; Ole Kiehn; Patrik Ernfors; Tatiana G. Deliagina; François Lallemend; Saida Hadjab

doi:10.1242/dev.181750

Muscle-selective RUNX3 dependence of sensorimotor circuit development

Yiqiao Wang, Haohao Wu, Pavel Zelenin, Paula Fontanet, Simone Wanderoy, Charles Petitpré, Glenda Comai, Carmelo Bellardita, Yongtao Xue-Franzén, Rosa Eva Huettl, Andrea B. Huber, Shahragim Tajbakhsh, Ole Kiehn, Patrik Ernfors, Tatiana G. Deliagina, François Lallemend, Saida Hadjab

Motor Control

3 Citations (Scopus)

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Abstract

The control of all our motor outputs requires constant monitoring by proprioceptive sensory neurons (PSNs) that convey continuous muscle sensory inputs to the spinal motor network. Yet the molecular programs that control the establishment of this sensorimotor circuit remain largely unknown. The transcription factor RUNX3 is essential for the early steps of PSNs differentiation, making it difficult to study its role during later aspects of PSNs specification. Here, we conditionally inactivate Runx3 in PSNs after peripheral innervation and identify that RUNX3 is necessary for maintenance of cell identity of only a subgroup of PSNs, without discernable cell death. RUNX3 also controls the sensorimotor connection between PSNs and motor neurons at limb level, with muscle-by-muscle variable sensitivities to the loss of Runx3 that correlate with levels of RUNX3 in PSNs. Finally, we find that muscles and neurotrophin 3 signaling are necessary for maintenance of RUNX3 expression in PSNs. Hence, a transcriptional regulator that is crucial for specifying a generic PSN type identity after neurogenesis is later regulated by target muscle-derived signals to contribute to the specialized aspects of the sensorimotor connection selectivity.

Original language	English
Article number	dev181750
Journal	Development (Cambridge)
Volume	146
Issue number	20
Number of pages	10
ISSN	0950-1991
DOIs	https://doi.org/10.1242/dev.181750
Publication status	Published - 2019

Keywords

Dorsal root ganglia
Neuronal specification
Neurotrophins
Sensorimotor circuit
Sensory system

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10.1242/dev.181750Licence: CC BY

Muscle-selective RUNX3 dependence of sensorimotor circuit developmentFinal published version, 4.56 MBLicence: CC BY

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Wang, Y., Wu, H., Zelenin, P., Fontanet, P., Wanderoy, S., Petitpré, C., Comai, G., Bellardita, C., Xue-Franzén, Y., Huettl, R. E., Huber, A. B., Tajbakhsh, S., Kiehn, O., Ernfors, P., Deliagina, T. G., Lallemend, F., & Hadjab, S. (2019). Muscle-selective RUNX3 dependence of sensorimotor circuit development. Development (Cambridge), 146(20), [dev181750]. https://doi.org/10.1242/dev.181750

Wang, Y, Wu, H, Zelenin, P, Fontanet, P, Wanderoy, S, Petitpré, C, Comai, G, Bellardita, C, Xue-Franzén, Y, Huettl, RE, Huber, AB, Tajbakhsh, S, Kiehn, O, Ernfors, P, Deliagina, TG, Lallemend, F & Hadjab, S 2019, 'Muscle-selective RUNX3 dependence of sensorimotor circuit development', Development (Cambridge), vol. 146, no. 20, dev181750. https://doi.org/10.1242/dev.181750

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title = "Muscle-selective RUNX3 dependence of sensorimotor circuit development",

abstract = "The control of all our motor outputs requires constant monitoring by proprioceptive sensory neurons (PSNs) that convey continuous muscle sensory inputs to the spinal motor network. Yet the molecular programs that control the establishment of this sensorimotor circuit remain largely unknown. The transcription factor RUNX3 is essential for the early steps of PSNs differentiation, making it difficult to study its role during later aspects of PSNs specification. Here, we conditionally inactivate Runx3 in PSNs after peripheral innervation and identify that RUNX3 is necessary for maintenance of cell identity of only a subgroup of PSNs, without discernable cell death. RUNX3 also controls the sensorimotor connection between PSNs and motor neurons at limb level, with muscle-by-muscle variable sensitivities to the loss of Runx3 that correlate with levels of RUNX3 in PSNs. Finally, we find that muscles and neurotrophin 3 signaling are necessary for maintenance of RUNX3 expression in PSNs. Hence, a transcriptional regulator that is crucial for specifying a generic PSN type identity after neurogenesis is later regulated by target muscle-derived signals to contribute to the specialized aspects of the sensorimotor connection selectivity.",

keywords = "Dorsal root ganglia, Neuronal specification, Neurotrophins, Sensorimotor circuit, Sensory system",

author = "Yiqiao Wang and Haohao Wu and Pavel Zelenin and Paula Fontanet and Simone Wanderoy and Charles Petitpr{\'e} and Glenda Comai and Carmelo Bellardita and Yongtao Xue-Franz{\'e}n and Huettl, {Rosa Eva} and Huber, {Andrea B.} and Shahragim Tajbakhsh and Ole Kiehn and Patrik Ernfors and Deliagina, {Tatiana G.} and Fran{\c c}ois Lallemend and Saida Hadjab",

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AU - Wang, Yiqiao

AU - Wu, Haohao

AU - Zelenin, Pavel

AU - Fontanet, Paula

AU - Wanderoy, Simone

AU - Petitpré, Charles

AU - Comai, Glenda

AU - Bellardita, Carmelo

AU - Xue-Franzén, Yongtao

AU - Huettl, Rosa Eva

AU - Huber, Andrea B.

AU - Tajbakhsh, Shahragim

AU - Kiehn, Ole

AU - Ernfors, Patrik

AU - Deliagina, Tatiana G.

AU - Lallemend, François

AU - Hadjab, Saida

PY - 2019

Y1 - 2019

N2 - The control of all our motor outputs requires constant monitoring by proprioceptive sensory neurons (PSNs) that convey continuous muscle sensory inputs to the spinal motor network. Yet the molecular programs that control the establishment of this sensorimotor circuit remain largely unknown. The transcription factor RUNX3 is essential for the early steps of PSNs differentiation, making it difficult to study its role during later aspects of PSNs specification. Here, we conditionally inactivate Runx3 in PSNs after peripheral innervation and identify that RUNX3 is necessary for maintenance of cell identity of only a subgroup of PSNs, without discernable cell death. RUNX3 also controls the sensorimotor connection between PSNs and motor neurons at limb level, with muscle-by-muscle variable sensitivities to the loss of Runx3 that correlate with levels of RUNX3 in PSNs. Finally, we find that muscles and neurotrophin 3 signaling are necessary for maintenance of RUNX3 expression in PSNs. Hence, a transcriptional regulator that is crucial for specifying a generic PSN type identity after neurogenesis is later regulated by target muscle-derived signals to contribute to the specialized aspects of the sensorimotor connection selectivity.

AB - The control of all our motor outputs requires constant monitoring by proprioceptive sensory neurons (PSNs) that convey continuous muscle sensory inputs to the spinal motor network. Yet the molecular programs that control the establishment of this sensorimotor circuit remain largely unknown. The transcription factor RUNX3 is essential for the early steps of PSNs differentiation, making it difficult to study its role during later aspects of PSNs specification. Here, we conditionally inactivate Runx3 in PSNs after peripheral innervation and identify that RUNX3 is necessary for maintenance of cell identity of only a subgroup of PSNs, without discernable cell death. RUNX3 also controls the sensorimotor connection between PSNs and motor neurons at limb level, with muscle-by-muscle variable sensitivities to the loss of Runx3 that correlate with levels of RUNX3 in PSNs. Finally, we find that muscles and neurotrophin 3 signaling are necessary for maintenance of RUNX3 expression in PSNs. Hence, a transcriptional regulator that is crucial for specifying a generic PSN type identity after neurogenesis is later regulated by target muscle-derived signals to contribute to the specialized aspects of the sensorimotor connection selectivity.

KW - Dorsal root ganglia

KW - Neuronal specification

KW - Neurotrophins

KW - Sensorimotor circuit

KW - Sensory system

U2 - 10.1242/dev.181750

DO - 10.1242/dev.181750

M3 - Journal article

C2 - 31575648

AN - SCOPUS:85074118017

SN - 0950-1991

VL - 146

JO - Development

JF - Development

IS - 20

M1 - dev181750

ER -

Muscle-selective RUNX3 dependence of sensorimotor circuit development

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