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Erschienen in: Brain Structure and Function 8/2016

19.12.2015 | Original Article

Transcriptional regulation of mouse hypoglossal motor neuron somatotopic map formation

verfasst von: Xin Chen, Jae Woong Wang, Adele Salin-Cantegrel, Rola Dali, Stefano Stifani

Erschienen in: Brain Structure and Function | Ausgabe 8/2016

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Abstract

Somatic motor neurons in the hypoglossal nucleus innervate tongue muscles controlling vital functions such as chewing, swallowing and respiration. Formation of functional hypoglossal nerve circuits depends on the establishment of precise hypoglossal motor neuron maps correlating with specific tongue muscle innervations. Little is known about the molecular mechanisms controlling mammalian hypoglossal motor neuron topographic map formation. Here we show that combinatorial expression of transcription factors Runx1, SCIP and FoxP1 defines separate mouse hypoglossal motor neuron groups with different topological, neurotransmitter and calcium-buffering phenotypes. Runx1 and SCIP are coexpressed in ventromedial hypoglossal motor neurons involved in control of tongue protrusion whereas FoxP1 is expressed in dorsomedial motor neurons associated with tongue retraction. Establishment of separate hypoglossal motor neuron maps depends in part on Runx1-mediated suppression of ventrolateral and dorsomedial motor neuron phenotypes and regulation of FoxP1 expression pattern. These findings suggest that combinatorial actions of Runx1, SCIP and FoxP1 are important for mouse hypoglossal nucleus somatotopic map formation.
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Literatur
Zurück zum Zitat Aldes LD (1995) Subcompartmental organization of the ventral (protrusor) compartment in the hypoglossal nucleus of the rat. J Comp Neurol 353:89–108CrossRefPubMed Aldes LD (1995) Subcompartmental organization of the ventral (protrusor) compartment in the hypoglossal nucleus of the rat. J Comp Neurol 353:89–108CrossRefPubMed
Zurück zum Zitat Altschuler SM, Bao X, Miselis RR (1994) Dendritic architecture of hypoglossal motor neurons projecting to extrinsic tongue musculature in the rat. J Comp Neurol 342:538–550CrossRefPubMed Altschuler SM, Bao X, Miselis RR (1994) Dendritic architecture of hypoglossal motor neurons projecting to extrinsic tongue musculature in the rat. J Comp Neurol 342:538–550CrossRefPubMed
Zurück zum Zitat Arber S, Han B, Mendelsohn M, Smith M, Jessell TM, Sockanathan S (1999) Requirement for the homeobox gene HB9 in the consolidation of motor neuron identity. Neuron 23:659–674CrossRefPubMed Arber S, Han B, Mendelsohn M, Smith M, Jessell TM, Sockanathan S (1999) Requirement for the homeobox gene HB9 in the consolidation of motor neuron identity. Neuron 23:659–674CrossRefPubMed
Zurück zum Zitat Bruno L, Mazzarella L, Hoogenkamp M, Hertweck A, Cobb BS, Sauer S et al (2009) Runx proteins regulate Foxp3 expression. J Exp Med 206:2329–2337CrossRefPubMedPubMedCentral Bruno L, Mazzarella L, Hoogenkamp M, Hertweck A, Cobb BS, Sauer S et al (2009) Runx proteins regulate Foxp3 expression. J Exp Med 206:2329–2337CrossRefPubMedPubMedCentral
Zurück zum Zitat Chang IY, Kim SW, Lee KJ, Yoon SP (2008) Calbindin D-28 k, parvalbumin and calcitonin gene-related peptide immunoreactivity in the canine spinal cord. Anat Histol Embryol 37:446–451CrossRefPubMed Chang IY, Kim SW, Lee KJ, Yoon SP (2008) Calbindin D-28 k, parvalbumin and calcitonin gene-related peptide immunoreactivity in the canine spinal cord. Anat Histol Embryol 37:446–451CrossRefPubMed
Zurück zum Zitat Chen CL, Broom DC, Liu Y, de Nooij JC, Li Z, Cen C et al (2006) Runx1 determines nociceptive sensory neuron phenotype and is required for thermal and neuropathic pain. Neuron 49:365–377CrossRefPubMed Chen CL, Broom DC, Liu Y, de Nooij JC, Li Z, Cen C et al (2006) Runx1 determines nociceptive sensory neuron phenotype and is required for thermal and neuropathic pain. Neuron 49:365–377CrossRefPubMed
Zurück zum Zitat Chibuzo GA, Cummings JF (1982) An enzyme tracer study of the organization of the somatic motor center for the innervation of different muscles of the tongue: evidence for two sources. J Comp Neurol 205:273–281CrossRefPubMed Chibuzo GA, Cummings JF (1982) An enzyme tracer study of the organization of the somatic motor center for the innervation of different muscles of the tongue: evidence for two sources. J Comp Neurol 205:273–281CrossRefPubMed
Zurück zum Zitat Dasen JS, Tice BC, Brenner-Morton S, Jessell TM (2005) A Hox regulatory network establishes motor neuron pool identity and target-muscle connectivity. Cell 123:477–491CrossRefPubMed Dasen JS, Tice BC, Brenner-Morton S, Jessell TM (2005) A Hox regulatory network establishes motor neuron pool identity and target-muscle connectivity. Cell 123:477–491CrossRefPubMed
Zurück zum Zitat Dasen JS, De Camilli A, Wang B, Tucker PW, Jessell TM (2008) Hox repertoires for motor neuron diversity and connectivity gated by a single accessory factor, FoxP1. Cell 134:304–316CrossRefPubMed Dasen JS, De Camilli A, Wang B, Tucker PW, Jessell TM (2008) Hox repertoires for motor neuron diversity and connectivity gated by a single accessory factor, FoxP1. Cell 134:304–316CrossRefPubMed
Zurück zum Zitat de Souza E, Coveñas R, Yi P, Aguilar LA, Lerma L, Andrade R et al (2008) Mapping of CGRP in the alpaca (Lama pacos) brainstem. J Chem Neuroanat 35:346–355CrossRefPubMed de Souza E, Coveñas R, Yi P, Aguilar LA, Lerma L, Andrade R et al (2008) Mapping of CGRP in the alpaca (Lama pacos) brainstem. J Chem Neuroanat 35:346–355CrossRefPubMed
Zurück zum Zitat Dunham I, Kundaje A, Aldred SF, Collins PJ, Davis CA, Doyle F et al (2012) An integrated encyclopedia of DNA elements in the human genome. Nature 489:57–74CrossRef Dunham I, Kundaje A, Aldred SF, Collins PJ, Davis CA, Doyle F et al (2012) An integrated encyclopedia of DNA elements in the human genome. Nature 489:57–74CrossRef
Zurück zum Zitat Francius C, Clotman F (2014) Generating spinal motor neuron diversity: a long quest for neuronal identity. Cell Mol Life Sci 71:813–829CrossRefPubMed Francius C, Clotman F (2014) Generating spinal motor neuron diversity: a long quest for neuronal identity. Cell Mol Life Sci 71:813–829CrossRefPubMed
Zurück zum Zitat Kanning KC, Kaplan A, Henderson CE (2010) Motor neuron diversity in development and disease. Annu Rev Neurosci 33:409–440CrossRefPubMed Kanning KC, Kaplan A, Henderson CE (2010) Motor neuron diversity in development and disease. Annu Rev Neurosci 33:409–440CrossRefPubMed
Zurück zum Zitat Kitoh A, Ono M, Naoe Y, Ohkura N, Yamaguchi T, Yaguchi H et al (2009) Indispensable role of the Runx1-Cbfbeta transcription complex for in vivo-suppressive function of FoxP3 + regulatory T cells. Immunity 31:609–620CrossRefPubMed Kitoh A, Ono M, Naoe Y, Ohkura N, Yamaguchi T, Yaguchi H et al (2009) Indispensable role of the Runx1-Cbfbeta transcription complex for in vivo-suppressive function of FoxP3 + regulatory T cells. Immunity 31:609–620CrossRefPubMed
Zurück zum Zitat Kramer I, Sigrist M, de Nooij JC, Taniuchi I, Jessell TM, Arber S (2006) A role for Runx1 transcription factor signaling in dorsal root ganglion sensory neuron diversification. Neuron 49:379–393CrossRefPubMed Kramer I, Sigrist M, de Nooij JC, Taniuchi I, Jessell TM, Arber S (2006) A role for Runx1 transcription factor signaling in dorsal root ganglion sensory neuron diversification. Neuron 49:379–393CrossRefPubMed
Zurück zum Zitat Krammer EB, Rath T, Lischka MF (1979) Somatotopic organization of the hypoglossal nucleus: a HRP study in the rat. Brain Res 170:533–537CrossRefPubMed Krammer EB, Rath T, Lischka MF (1979) Somatotopic organization of the hypoglossal nucleus: a HRP study in the rat. Brain Res 170:533–537CrossRefPubMed
Zurück zum Zitat Levanon D, Bettoun D, Harris-Cerruti C, Woolf E, Negreanu V, Eilam R et al (2002) The Runx3 transcription factor regulates development and survival of TrkC dorsal root ganglia neurons. EMBO J 21:3454–3463CrossRefPubMedPubMedCentral Levanon D, Bettoun D, Harris-Cerruti C, Woolf E, Negreanu V, Eilam R et al (2002) The Runx3 transcription factor regulates development and survival of TrkC dorsal root ganglia neurons. EMBO J 21:3454–3463CrossRefPubMedPubMedCentral
Zurück zum Zitat Lewis PR, Flumerfelt BA, Shute CCD (1971) The use of cholinesterase techniques to study topographical localization in the hypoglossal nucleus of the rat. J Anat (London) 110:203–213 Lewis PR, Flumerfelt BA, Shute CCD (1971) The use of cholinesterase techniques to study topographical localization in the hypoglossal nucleus of the rat. J Anat (London) 110:203–213
Zurück zum Zitat Lowe AA (1981) The neural regulation of tongue movements. Prog Neurol 15:295–344CrossRef Lowe AA (1981) The neural regulation of tongue movements. Prog Neurol 15:295–344CrossRef
Zurück zum Zitat Lowe AA (1984) Tongue movements-brainstem mechanisms and clinical postulates. Brain Behav Evol 25:128–137CrossRefPubMed Lowe AA (1984) Tongue movements-brainstem mechanisms and clinical postulates. Brain Behav Evol 25:128–137CrossRefPubMed
Zurück zum Zitat Machado CB, Kanning KC, Kreis P, Stevenson D, Crossley M, Nowak M et al (2014) Reconstruction of phrenic neuron identity in embryonic stem cell-derived motor neurons. Development 141:784–794CrossRefPubMedPubMedCentral Machado CB, Kanning KC, Kreis P, Stevenson D, Crossley M, Nowak M et al (2014) Reconstruction of phrenic neuron identity in embryonic stem cell-derived motor neurons. Development 141:784–794CrossRefPubMedPubMedCentral
Zurück zum Zitat McClung JR, Goldberg SJ (1999) Organization of motoneurons in the dorsal hypoglossal nucleus that innervate the retrusor muscles of the tongue in the rat. Anat Rec 254:222–230CrossRefPubMed McClung JR, Goldberg SJ (1999) Organization of motoneurons in the dorsal hypoglossal nucleus that innervate the retrusor muscles of the tongue in the rat. Anat Rec 254:222–230CrossRefPubMed
Zurück zum Zitat McClung JR, Goldberg SJ (2000) Functional anatomy of the hypoglossal innervated muscles of the rat tongue: a model for elongation and protrusion of the mammalian tongue. Anat Rec 260:378–386CrossRefPubMed McClung JR, Goldberg SJ (2000) Functional anatomy of the hypoglossal innervated muscles of the rat tongue: a model for elongation and protrusion of the mammalian tongue. Anat Rec 260:378–386CrossRefPubMed
Zurück zum Zitat Murthy M, Bocking S, Verginelli F, Stifani S (2014) Transcription factor Runx1 inhibits proliferation and promotes developmental maturation in a selected population of inner olfactory nerve layer olfactory ensheathing cells. Gene 540:191–200CrossRefPubMed Murthy M, Bocking S, Verginelli F, Stifani S (2014) Transcription factor Runx1 inhibits proliferation and promotes developmental maturation in a selected population of inner olfactory nerve layer olfactory ensheathing cells. Gene 540:191–200CrossRefPubMed
Zurück zum Zitat North T, Gu TL, Stacy T, Wang Q, Howard L, Binder M et al (1999) Cbfa2 is required for the formation of intra-aortic hematopoietic clusters. Development 126:2563–2575PubMed North T, Gu TL, Stacy T, Wang Q, Howard L, Binder M et al (1999) Cbfa2 is required for the formation of intra-aortic hematopoietic clusters. Development 126:2563–2575PubMed
Zurück zum Zitat Odutola AB (1976) Cell grouping and Golgi architecture of the hypoglossal nucleus in the rat. Exp Neurol 52:356–371CrossRefPubMed Odutola AB (1976) Cell grouping and Golgi architecture of the hypoglossal nucleus in the rat. Exp Neurol 52:356–371CrossRefPubMed
Zurück zum Zitat Palmesino E, Rousso DL, Kao T-J, Klar A, Laufer E, Uemura O et al (2010) Foxp1 and Lhx1 Coordinate Motor Neuron Migration with Axon Trajectory Choice by Gating Reelin Signalling. PLoS Biol 8(8):e1000446CrossRefPubMedPubMedCentral Palmesino E, Rousso DL, Kao T-J, Klar A, Laufer E, Uemura O et al (2010) Foxp1 and Lhx1 Coordinate Motor Neuron Migration with Axon Trajectory Choice by Gating Reelin Signalling. PLoS Biol 8(8):e1000446CrossRefPubMedPubMedCentral
Zurück zum Zitat Philippidou P, Walsh CM, Aubin J, Jeannotte L, Dasen JS (2012) Sustained Hox5 gene activity is required for respiratory motor neuron development. Nature Neurosci 15:1636–1644CrossRefPubMedPubMedCentral Philippidou P, Walsh CM, Aubin J, Jeannotte L, Dasen JS (2012) Sustained Hox5 gene activity is required for respiratory motor neuron development. Nature Neurosci 15:1636–1644CrossRefPubMedPubMedCentral
Zurück zum Zitat Rousso DL, Gaber ZB, Wellik D, Morrisey EE, Novitch BG (2008) Coordinated actions of the forkhead protein Foxp1 and Hox proteins in the columnar organization of spinal motor neurons. Neuron 59:226–240CrossRefPubMedPubMedCentral Rousso DL, Gaber ZB, Wellik D, Morrisey EE, Novitch BG (2008) Coordinated actions of the forkhead protein Foxp1 and Hox proteins in the columnar organization of spinal motor neurons. Neuron 59:226–240CrossRefPubMedPubMedCentral
Zurück zum Zitat Rudra D, Egawa T, Chong MM, Treuting P, Littman DR, Rudensky AY (2009) Runx-CBFbeta complexes control expression of the transcription factor Foxp3 in regulatory T cells. Nat Immunol 10:1170–1177CrossRefPubMedPubMedCentral Rudra D, Egawa T, Chong MM, Treuting P, Littman DR, Rudensky AY (2009) Runx-CBFbeta complexes control expression of the transcription factor Foxp3 in regulatory T cells. Nat Immunol 10:1170–1177CrossRefPubMedPubMedCentral
Zurück zum Zitat Sienkiewicz W, Dudek A, Kaleczyc J, Chrószcz A (2010) Immunohistochemical characterization of neurones in the hypoglossal nucleus of the pig. Anat Histol Embryol 39:152–159CrossRefPubMed Sienkiewicz W, Dudek A, Kaleczyc J, Chrószcz A (2010) Immunohistochemical characterization of neurones in the hypoglossal nucleus of the pig. Anat Histol Embryol 39:152–159CrossRefPubMed
Zurück zum Zitat Smith JC, Goldberg SJ, Shall MS (2005) Phenotype and contractile properties of mammalian tongue muscles innervated by the hypoglossal nerve. Respir Physiol Neurobiol 147:253–262CrossRefPubMed Smith JC, Goldberg SJ, Shall MS (2005) Phenotype and contractile properties of mammalian tongue muscles innervated by the hypoglossal nerve. Respir Physiol Neurobiol 147:253–262CrossRefPubMed
Zurück zum Zitat Stifani N, Freitas AR, Liakhovitskaia A, Medvinsky A, Kania A, Stifani S (2008) Suppression of interneuron programs and maintenance of selected spinal motor neuron fates by the transcription factor AML1/Runx1. Proc Natl Acad Sci USA 105:6451–6456CrossRefPubMedPubMedCentral Stifani N, Freitas AR, Liakhovitskaia A, Medvinsky A, Kania A, Stifani S (2008) Suppression of interneuron programs and maintenance of selected spinal motor neuron fates by the transcription factor AML1/Runx1. Proc Natl Acad Sci USA 105:6451–6456CrossRefPubMedPubMedCentral
Zurück zum Zitat Sürmeli G, Akay T, Ippolito GC, Tucker PW, Jessell TM (2011) Patterns of spinal sensory-motor connectivity prescribed by a dorsoventral positional template. Cell 147:653–665CrossRefPubMedPubMedCentral Sürmeli G, Akay T, Ippolito GC, Tucker PW, Jessell TM (2011) Patterns of spinal sensory-motor connectivity prescribed by a dorsoventral positional template. Cell 147:653–665CrossRefPubMedPubMedCentral
Zurück zum Zitat Theriault FM, Roy P, Stifani S (2004) AML1/RUNX1 is important for the development of hindbrain cholinergic branchiovisceral motor neurons and selected cranial sensory neurons. Proc Natl Acad Sci USA 101:10343–10348CrossRefPubMedPubMedCentral Theriault FM, Roy P, Stifani S (2004) AML1/RUNX1 is important for the development of hindbrain cholinergic branchiovisceral motor neurons and selected cranial sensory neurons. Proc Natl Acad Sci USA 101:10343–10348CrossRefPubMedPubMedCentral
Zurück zum Zitat Theriault FM, Nuthall HN, Dong Z, Lo R, Barnabe-Heider F, Miller FD et al (2005) Role for Runx1 in the proliferation and neuronal differentiation of selected progenitor cells in the mammalian nervous system. J Neurosci 25:2050–2061CrossRefPubMed Theriault FM, Nuthall HN, Dong Z, Lo R, Barnabe-Heider F, Miller FD et al (2005) Role for Runx1 in the proliferation and neuronal differentiation of selected progenitor cells in the mammalian nervous system. J Neurosci 25:2050–2061CrossRefPubMed
Zurück zum Zitat Uemura-Sumi M, Mizuno N, Nomura S, Iwahori N, Takeuchi Y, Matshushima R (1981) Topographical representation of the hypoglossal nerve branches in the hypoglossal nucleus of the Macaque monkeys. Neurosci Lett 22:31–35CrossRefPubMed Uemura-Sumi M, Mizuno N, Nomura S, Iwahori N, Takeuchi Y, Matshushima R (1981) Topographical representation of the hypoglossal nerve branches in the hypoglossal nucleus of the Macaque monkeys. Neurosci Lett 22:31–35CrossRefPubMed
Zurück zum Zitat Yang X, Arber S, William C, Li L, Tanabe Y, Jessell TM et al (2001) Patterning of muscle acetylcholine receptor gene expression in the absence of motor innervation. Neuron 30:399–410CrossRefPubMed Yang X, Arber S, William C, Li L, Tanabe Y, Jessell TM et al (2001) Patterning of muscle acetylcholine receptor gene expression in the absence of motor innervation. Neuron 30:399–410CrossRefPubMed
Zurück zum Zitat Yoshikawa M, Hirabayashi M, Ito R, Ozaki S, Aizawa S, Masuda T et al (2015) Contribution of the Runx1 transcription factor to axonal pathfinding and muscle innervation by hypoglossal motoneurons. Dev Neurobiol 75:1295−1314 CrossRefPubMed Yoshikawa M, Hirabayashi M, Ito R, Ozaki S, Aizawa S, Masuda T et al (2015) Contribution of the Runx1 transcription factor to axonal pathfinding and muscle innervation by hypoglossal motoneurons. Dev Neurobiol 75:1295−1314 CrossRefPubMed
Zurück zum Zitat Zagami CJ, Stifani S (2010) Molecular characterization of the mouse superior lateral parabrachial nucleus through expression of the transcription factor Runx1. PLoS One 5(11):e13944CrossRefPubMedPubMedCentral Zagami CJ, Stifani S (2010) Molecular characterization of the mouse superior lateral parabrachial nucleus through expression of the transcription factor Runx1. PLoS One 5(11):e13944CrossRefPubMedPubMedCentral
Zurück zum Zitat Zhao H, Zhou W, Yao Z, Wan Y, Cao J, Zhang L et al (2015) Foxp1/2/4 regulate endochondral ossification as a suppressor complex. Dev Biol 398:242–252CrossRefPubMed Zhao H, Zhou W, Yao Z, Wan Y, Cao J, Zhang L et al (2015) Foxp1/2/4 regulate endochondral ossification as a suppressor complex. Dev Biol 398:242–252CrossRefPubMed
Zurück zum Zitat Zusso M, Methot L, Lo R, Grenhalgh AD, David S, Stifani S (2012) Regulation of postnatal forebrain amoeboid microglial cell proliferation and development by the transcription factor Runx1. J Neurosci 32:11285–11298CrossRefPubMed Zusso M, Methot L, Lo R, Grenhalgh AD, David S, Stifani S (2012) Regulation of postnatal forebrain amoeboid microglial cell proliferation and development by the transcription factor Runx1. J Neurosci 32:11285–11298CrossRefPubMed
Metadaten
Titel
Transcriptional regulation of mouse hypoglossal motor neuron somatotopic map formation
verfasst von
Xin Chen
Jae Woong Wang
Adele Salin-Cantegrel
Rola Dali
Stefano Stifani
Publikationsdatum
19.12.2015
Verlag
Springer Berlin Heidelberg
Erschienen in
Brain Structure and Function / Ausgabe 8/2016
Print ISSN: 1863-2653
Elektronische ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-015-1160-2

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