Hox genes and region-specific sensorimotor circuit formation in the hindbrain and spinal cord

Developmental Dynamics

Volumn 242, Issue 12, 2013, Pages 1348-1368

  Di Bonito, Maria ^a,b   Glover, Joel C ^c,d   Studer, Michèle ^a,b  

^a UNIVERSITÉ CÔTE D'AZUR   (France)

^b CENTRE DE BIOCHIMIE   (France)

^c UNIVERSITY OF OSLO   (Norway)

^d UNIVERSITY OF BERGEN   (Norway)

Author keywords

Hox genes; Neuronal differentiation, axon pathfinding, neuronal migration; Rhombomers; Sensorimotor circuits; Spinal cord

Indexed keywords

HOMEODOMAIN PROTEIN;

ARTICLE; AUDITORY NERVOUS SYSTEM; BRAIN REGION; CELL DIFFERENTIATION; CELL MIGRATION; DROSOPHILA; GENE CONTROL; GENE EXPRESSION; HOX GENE; NERVE CELL GROWTH; NERVE CELL NETWORK; NERVOUS SYSTEM DEVELOPMENT; NEUROMERE; NONHUMAN; PRIORITY JOURNAL; RHOMBENCEPHALON; SENSORIMOTOR FUNCTION; SPINAL CORD; TRIGEMINAL NUCLEUS; VESTIBULAR SYSTEM;

VERTEBRATA;

HOX GENES; NEURONAL DIFFERENTIATION, AXON PATHFINDING, NEURONAL MIGRATION; RHOMBOMERS; SENSORIMOTOR CIRCUITS; SPINAL CORD;

ANIMALS; CELL DIFFERENTIATION; CELL MOVEMENT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, HOMEOBOX; MODELS, BIOLOGICAL; MORPHOGENESIS; NEURAL PATHWAYS; RHOMBENCEPHALON; SPINAL CORD; VERTEBRATES;

EID: 84888034044     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.24055     Document Type: Article

References (155)

1. Altman J, Bayer SA. 1987a. Development of the precerebellar nuclei in the rat. I. The precerebellar neuroepithelium of the rhombencephalon. J Comp Neurol 257:477-489.
2. Altman J, Bayer SA. 1987b. Development of the precerebellar nuclei in the rat. II. The intramural olivary migratory stream and the neurogenetic organization of the inferior olive. J Comp Neurol 257:490-512.
3. Altman J, Bayer SA. 1987c. Development of the precerebellar nuclei in the rat. III. The posterior precerebellar extramural migratory stream and the lateral reticular and external cuneate nuclei. J Comp Neurol 257:513-528.
4. Altman J, Bayer SA. 1987d. Development of the precerebellar nuclei in the rat. IV. The anterior precerebellar extramural migratory stream and the nucleus reticularis tegmenti pontis and the basal pontine gray. J Comp Neurol 257:529-552.
5. Angelaki DE, Cullen KE. 2008. Vestibular system: the many facets of a multimodal sense. Annu Rev Neurosci 31:125-150.
6. Auclair F, Marchand R, Glover JC. 1999. Regional patterning of reticulospinal and vestibulospinal neurons in the hindbrain of mouse and rat embryos. J Comp Neurol 411:288-300.
7. Auclair F, Valdes N, Marchand R. 1996. Rhombomere-specific origin of branchial and visceral motoneurons of the facial nerve in the rat embryo. J Comp Neurol 369:451-461.
8. Azuara V, Perry P, Sauer S, Spivakov M, Jorgensen HF, John RM, Gouti M, Casanova M, Warnes G, Merkenschlager M, Fisher AG. 2006. Chromatin signatures of pluripotent cell lines. Nat Cell Biol 8:532-538.
9. Barrow JR, Capecchi MR. 1996. Targeted disruption of the Hoxb-2 locus in mice interferes with expression of Hoxb-1 and Hoxb-4. Development 122:3817-3828.
10. Batini C, Compoint C, Buisseret-Delmas C, Daniel H, Guegan M. 1992. Cerebellar nuclei and the nucleocortical projections in the rat: retrograde tracing coupled to GABA and glutamate immunohistochemistry. J Comp Neurol 315:74-84.
11. Beckmann J, Vitobello A, Ferralli J, Broz DK, Rijli FM, Chiquet-Ehrismann R. 2011. Human teneurin-1 is a direct target of the homeobox transcription factor EMX2 at a novel alternate promoter. BMC Dev Biol 11:35.
12. Ben-Arie N, Bellen HJ, Armstrong DL, McCall AE, Gordadze PR, Guo Q, Matzuk MM, Zoghbi HY. 1997. Math1 is essential for genesis of cerebellar granule neurons. Nature 390:169-172.
13. Ben-Arie N, Hassan BA, Bermingham NA, Malicki DM, Armstrong D, Matzuk M, Bellen HJ, Zoghbi HY. 2000. Functional conservation of atonal and Math1 in the CNS and PNS. Development 127:1039-1048.
14. Bermingham NA, Hassan BA, Price SD, Vollrath MA, Ben-Arie N, Eatock RA, Bellen HJ, Lysakowski A, Zoghbi HY. 1999. Math1: an essential gene for the generation of inner ear hair cells. Science 284:1837-1841.
15. Bermingham NA, Hassan BA, Wang VY, Fernandez M, Banfi S, Bellen HJ, Fritzsch B, Zoghbi HY. 2001. Proprioceptor pathway development is dependent on Math1. Neuron 30:411-422.
16. Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, Fry B, Meissner A, Wernig M, Plath K, Jaenisch R, Wagschal A, Feil R, Schreiber SL, Lander ES. 2006. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125:315-326.
17. Berretta S, Perciavalle V, Poppele RE. 1991. Origin of cuneate projections to the anterior and posterior lobes of the rat cerebellum. Brain Res 556:297-302.
18. Bourrat F, Sotelo C. 1988. Migratory pathways and neuritic differentiation of inferior olivary neurons in the rat embryo. Axonal tracing study using the in vitro slab technique. Brain Res 467:19-37.
19. Bourrat F, Sotelo C. 1990. Migratory pathways and selective aggregation of the lateral reticular neurons in the rat embryo: a horseradish peroxidase in vitro study, with special reference to migration patterns of the precerebellar nuclei. J Comp Neurol 294:1-13.
20. Brose K, Tessier-Lavigne M. 2000. Slit proteins: key regulators of axon guidance, axonal branching, and cell migration. Curr Opin Neurobiol 10:95-102.
21. Brown MC, de Venecia RK, Guinan JJ Jr. 2003. Responses of medial olivocochlear neurons. Specifying the central pathways of the medial olivocochlear reflex. Exp Brain Res 153:491-498.
22. Bruce LL, Kingsley J, Nichols DH, Fritzsch B. 1997. The development of vestibulocochlear efferents and cochlear afferents in mice. Int J Dev Neurosci 15:671-692.
23. Bumsted-O'Brien KM, Hendrickson A, Haverkamp S, Ashery-Padan R, Schulte D. 2007. Expression of the homeodomain transcription factor Meis2 in the embryonic and postnatal retina. J Comp Neurol 505:58-72.
24. Cambronero F, Puelles L. 2000. Rostrocaudal nuclear relationships in the avian medulla oblongata: a fate map with quail chick chimeras. J Comp Neurol 427:522-545.
25. Carpenter EM. 2002. Hox genes and spinal cord development. Dev Neurosci 24:24-34.
26. Causeret F, Danne F, Ezan F, Sotelo C, Bloch-Gallego E. 2002. Slit antagonizes netrin-1 attractive effects during the migration of inferior olivary neurons. Dev Biol 246:429-440.
27. Chambers D, Wilson LJ, Alfonsi F, Hunter E, Saxena U, Blanc E, Lumsden A. 2009. Rhombomere-specific analysis reveals the repertoire of genetic cues expressed across the developing hindbrain. Neural Dev 4:6.
28. Chen Y, Takano-Maruyama M, Fritzsch B, Gaufo GO. 2012. Hoxb1 controls anteroposterior identity of vestibular projection neurons. PLoS One 7:e34762.
29. Cramer KS, Fraser SE, Rubel EW. 2000. Embryonic origins of auditory brain-stem nuclei in the chick hindbrain. Dev Biol 224:138-151.
30. Dallos P. 2008. Cochlear amplification, outer hair cells and prestin. Curr Opin Neurobiol 18:370-376.
31. Darrow KN, Maison SF, Liberman MC. 2007. Selective removal of lateral olivocochlear efferents increases vulnerability to acute acoustic injury. J Neurophysiol 97:1775-1785.
32. Dasen JS, Liu JP, Jessell TM. 2003. Motor neuron columnar fate imposed by sequential phases of Hox-c activity. Nature 425:926-933.
33. Dasen JS, Tice BC, Brenner-Morton S, Jessell TM. 2005. A Hox regulatory network establishes motor neuron pool identity and target-muscle connectivity. Cell 123:477-491.
34. Davenne M, Maconochie MK, Neun R, Pattyn A, Chambon P, Krumlauf R, Rijli FM. 1999. Hoxa2 and Hoxb2 control dorsoventral patterns of neuronal development in the rostral hindbrain. Neuron 22:677-691.
35. de Venecia RK, Liberman MC, Guinan JJ Jr, Brown MC. 2005. Medial olivocochlear reflex interneurons are located in the posteroventral cochlear nucleus: a kainic acid lesion study in guinea pigs. J Comp Neurol 487:345-360.
36. Di Bonito M, Narita Y, Avallone B, Sequino L, Mancuso M, Andolfi G, Franze AM, Puelles L, Rijli FM, Studer M. 2013. Assembly of the auditory circuitry by a Hox genetic network in the mouse brainstem. PLoS Genet 9:e1003249.
37. Di Meglio T, Kratochwil CF, Vilain N, Loche A, Vitobello A, Yonehara K, Hrycaj SM, Roska B, Peters AH, Eichmann A, Wellik D, Ducret S, Rijli FM. 2013. Ezh2 orchestrates topographic migration and connectivity of mouse precerebellar neurons. Science 339:204-207.
38. Diaz C, Glover JC. 2002. Comparative aspects of the hodological organization of the vestibular nuclear complex and related neuron populations. Brain Res Bull 57:307-312.
39. Diaz C, Glover JC, Puelles L, Bjaalie JG. 2003. The relationship between hodological and cytoarchitectonic organization in the vestibular complex of the 11-day chicken embryo. J Comp Neurol 457:87-105.
40. Diaz C, Puelles L, Marin F, Glover JC. 1998. The relationship between rhombomeres and vestibular neuron populations as assessed in quail-chicken chimeras. Dev Biol 202:14-28.
41. Duboule D. 1991. Patterning in the vertebrate limb. Curr Opin Genet Dev 1:211-216.
42. Dymecki SM, Ray RS, Kim JC. 2010. Mapping cell fate and function using recombinase-based intersectional strategies. Methods Enzymol 477:183-213.
43. Erzurumlu RS, Killackey HP. 1983. Development of order in the rat trigeminal system. J Comp Neurol 213:365-380.
44. Erzurumlu RS, Murakami Y, Rijli FM. 2010. Mapping the face in the somatosensory brainstem. Nat Rev Neurosci 11:252-263.
45. Farago AF, Awatramani RB, Dymecki SM. 2006. Assembly of the brainstem cochlear nuclear complex is revealed by intersectional and subtractive genetic fate maps. Neuron 50:205-218.
46. Fazeli A, Dickinson SL, Hermiston ML, Tighe RV, Steen RG, Small CG, Stoeckli ET, Keino-Masu K, Masu M, Rayburn H, Simons J, Bronson RT, Gordon JI, Tessier-Lavigne M, Weinberg RA. 1997. Phenotype of mice lacking functional Deleted in colorectal cancer (Dcc) gene. Nature 386:796-804.
47. Fettiplace R, Hackney CM. 2006. The sensory and motor roles of auditory hair cells. Nat Rev Neurosci 7:19-29.
48. Forehand CJ, Ezerman EB, Goldblatt JP, Skidmore DL, Glover JC. 1998. Segment-specific pattern of sympathetic preganglionic projections in the chicken embryo spinal cord is altered by retinoids. Proc Natl Acad Sci U S A 95:10878-10883.
49. Forehand CJ, Ezerman EB, Rubin E, Glover JC. 1994. Segmental patterning of rat and chicken sympathetic preganglionic neurons: correlation between soma position and axon projection pathway. J Neurosci 14:231-241.
50. Fraser S, Keynes R, Lumsden A. 1990. Segmentation in the chick embryo hindbrain is defined by cell lineage restrictions. Nature 344:431-435.
51. Fu J, Ivy Yu HM, Maruyama T, Mirando AJ, Hsu W. 2011. Gpr177/mouse Wntless is essential for Wnt-mediated craniofacial and brain development. Dev Dyn 240:365-371.
52. Fujiyama T, Yamada M, Terao M, Terashima T, Hioki H, Inoue YU, Inoue T, Masuyama N, Obata K, Yanagawa Y, Kawaguchi Y, Nabeshima Y, Hoshino M. 2009. Inhibitory and excitatory subtypes of cochlear nucleus neurons are defined by distinct bHLH transcription factors, Ptf1a and Atoh1. Development 136:2049-2058.
53. Gaufo GO, Flodby P, Capecchi MR. 2000. Hoxb1 controls effectors of sonic hedgehog and Mash1 signaling pathways. Development 127:5343-5354.
54. Gaufo GO, Thomas KR, Capecchi MR. 2003. Hox3 genes coordinate mechanisms of genetic suppression and activation in the generation of branchial and somatic motoneurons. Development 130:5191-5201.
55. Gavalas A, Davenne M, Lumsden A, Chambon P, Rijli FM. 1997. Role of Hoxa-2 in axon pathfinding and rostral hindbrain patterning. Development 124:3693-3702.
56. Gavalas A, Ruhrberg C, Livet J, Henderson CE, Krumlauf R. 2003. Neuronal defects in the hindbrain of Hoxa1, Hoxb1 and Hoxb2 mutants reflect regulatory interactions among these Hox genes. Development 130:5663-5679.
57. Geisen MJ, Di Meglio T, Pasqualetti M, Ducret S, Brunet JF, Chedotal A, Rijli FM. 2008. Hox paralog group 2 genes control the migration of mouse pontine neurons through slit-robo signaling. PLoS Biol 6:e142.
58. Glasgow SM, Henke RM, Macdonald RJ, Wright CV, Johnson JE. 2005. Ptf1a determines GABAergic over glutamatergic neuronal cell fate in the spinal cord dorsal horn. Development 132:5461-5469.
59. Glover JC. 1989. Rhombomeres and longitudinal boundaries in the chicken embryo brainstem subdivide vestibular neurons according to axonal pathway. Soc Neurosci Abstr 15:959.
60. Glover JC. 1994. The organization of vestibulo-ocular and vestibulospinal projections in the chicken embryo. Eur J Morphol 32:193-200.
61. Glover JC. 1996. Development of second-order vestibular projections in the chicken embryo. Ann N Y Acad Sci 781:13-20.
62. Glover JC. 2000. Neuroepithelial 'compartments' and the specification of vestibular projections. Prog Brain Res 124:3-21.
63. Glover JC. 2001. Correlated patterns of neuron differentiation and Hox gene expression in the hindbrain: a comparative analysis. Brain Res Bull 55:683-693.
64. Glover JC. 2003. The development of vestibulo-ocular circuitry in the chicken embryo. J Physiol Paris 97:17-25.
65. Glover JC. 2007. The vestibular system. Encyclopedia of neuroscience. Amsterdam: Elsevier.
66. Glover JC, Petursdottir G. 1991. Regional specificity of developing reticulospinal, vestibulospinal, and vestibulo-ocular projections in the chicken embryo. J Neurobiol 22:353-376.
67. Golden MG, Dasen JS. 2012. Polycomb repressive complex 1 activities determine the columnar organization of motor neurons. Genes Dev 26:2236-2250.
68. Guinan JJ Jr. 2006. Olivocochlear efferents: anatomy, physiology, function, and the measurement of efferent effects in humans. Ear Hear 27:589-607.
69. Hidalgo-Sanchez M, Backer S, Puelles L, Bloch-Gallego E. 2012. Origin and plasticity of the subdivisions of the inferior olivary complex. Dev Biol 371:215-226.
70. Hori K, Hoshino M. 2012. GABAergic neuron specification in the spinal cord, the cerebellum, and the cochlear nucleus. Neural Plast 2012:921732.
71. Hoshino M, Nakamura S, Mori K, Kawauchi T, Terao M, Nishimura YV, Fukuda A, Fuse T, Matsuo N, Sone M, Watanabe M, Bito H, Terashima T, Wright CV, Kawaguchi Y, Nakao K, Nabeshima Y. 2005. Ptf1a, a bHLH transcriptional gene, defines GABAergic neuronal fates in cerebellum. Neuron 47:201-213.
72. Huber L, Ferdin M, Holzmann J, Stubbusch J, Rohrer H. 2012. HoxB8 in noradrenergic specification and differentiation of the autonomic nervous system. Dev Biol 363:219-233.
73. Hunt P, Gulisano M, Cook M, Sham MH, Faiella A, Wilkinson D, Boncinelli E, Krumlauf R. 1991. A distinct Hox code for the branchial region of the vertebrate head. Nature 353:861-864.
74. Jacob J, Ferri AL, Milton C, Prin F, Pla P, Lin W, Gavalas A, Ang SL, Briscoe J. 2007. Transcriptional repression coordinates the temporal switch from motor to serotonergic neurogenesis. Nat Neurosci 10:1433-1439.
75. Jessell TM. 2000. Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat Rev Genet 1:20-29.
76. Jung H, Lacombe J, Mazzoni EO, Liem KF Jr, Grinstein J, Mahony S, Mukhopadhyay D, Gifford DK, Young RA, Anderson KV, Wichterle H, Dasen JS. 2010. Global control of motor neuron topography mediated by the repressive actions of a single hox gene. Neuron 67:781-796.
77. Kasumacic N, Glover JC, Perreault MC. 2010. Segmental patterns of vestibular-mediated synaptic inputs to axial and limb motoneurons in the neonatal mouse assessed by optical recording. J Physiol 588:4905-4925.
78. Kasumacic N, Glover JC, Perreault MC. 2012. Vestibular-mediated synaptic inputs and pathways to sympathetic preganglionic neurons in the neonatal mouse. J Physiol 590:5809-5826.
79. Keynes RJ, Stern CD. 1984. Segmentation in the vertebrate nervous system. Nature 310:786-789.
80. Kiecker C, Lumsden A. 2005. Compartments and their boundaries in vertebrate brain development. Nat Rev Neurosci 6:553-564.
81. Kim EJ, Battiste J, Nakagawa Y, Johnson JE. 2008. Ascl1 (Mash1) lineage cells contribute to discrete cell populations in CNS architecture. Mol Cell Neurosci 38:595-606.
82. Krumlauf R. 1994. Hox genes in vertebrate development. Cell 78:191-201.
83. Krumlauf R, Marshall H, Studer M, Nonchev S, Sham MH, Lumsden A. 1993. Hox homeobox genes and regionalisation of the nervous system. J Neurobiol 24:1328-1340.
84. Kuan CY, Tannahill D, Cook GM, Keynes RJ. 2004. Somite polarity and segmental patterning of the peripheral nervous system. Mech Dev 121:1055-1068.
85. Kujawa SG, Liberman MC. 1997. Conditioning-related protection from acoustic injury: effects of chronic deefferentation and sham surgery. J Neurophysiol 78:3095-3106.
86. Lacombe J, Hanley O, Jung H, Philippidou P, Surmeli G, Grinstein J, Dasen JS. 2013. Genetic and functional modularity of Hox activities in the specification of limb-innervating motor neurons. PLoS Genet 9:e1003184.
87. Lance-Jones C, Omelchenko N, Bailis A, Lynch S, Sharma K. 2001. Hoxd10 induction and regionalization in the developing lumbosacral spinal cord. Development 128:2255-2268.
88. Landsberg RL, Awatramani RB, Hunter NL, Farago AF, DiPietrantonio HJ, Rodriguez CI, Dymecki SM. 2005. Hindbrain rhombic lip is comprised of discrete progenitor cell populations allocated by Pax6. Neuron 48:933-947.
89. Lebel M, Mo R, Shimamura K, Hui CC. 2007. Gli2 and Gli3 play distinct roles in the dorsoventral patterning of the mouse hindbrain. Dev Biol 302:345-355.
90. Lee DJ, de Venecia RK, Guinan JJ Jr, Brown MC. 2006. Central auditory pathways mediating the rat middle ear muscle reflexes. Anat Rec A Discov Mol Cell Evol Biol 288:358-369.
91. Leonardo ED, Hinck L, Masu M, Keino-Masu K, Ackerman SL, Tessier-Lavigne M. 1997. Vertebrate homologues of C. elegans UNC-5 are candidate netrin receptors. Nature 386:833-838.
92. Liberman MC, Guinan JJ Jr. 1998. Feedback control of the auditory periphery: anti-masking effects of middle ear muscles vs. olivocochlear efferents. J Commun Disord 31:471-482; quiz 483; 553.
93. Lints R, Emmons SW. 1999. Patterning of dopaminergic neurotransmitter identity among Caenorhabditis elegans ray sensory neurons by a TGFbeta family signaling pathway and a Hox gene. Development 126:5819-5831.
94. Louvi A, Yoshida M, Grove EA. 2007. The derivatives of the Wnt3a lineage in the central nervous system. J Comp Neurol 504:550-569.
95. Lumsden A, Keynes R. 1989. Segmental patterns of neuronal development in the chick hindbrain. Nature 337:424-428.
96. Lumsden A, Krumlauf R. 1996. Patterning the vertebrate neuraxis. Science 274:1109-1115.
97. Machold R, Fishell G. 2005. Math1 is expressed in temporally discrete pools of cerebellar rhombic-lip neural progenitors. Neuron 48:17-24.
98. Maconochie MK, Nonchev S, Studer M, Chan SK, Popperl H, Sham MH, Mann RS, Krumlauf R. 1997. Cross-regulation in the mouse HoxB complex: the expression of Hoxb2 in rhombomere 4 is regulated by Hoxb1. Genes Dev 11:1885-1895.
99. Maison SF, Luebke AE, Liberman MC, Zuo J. 2002. Efferent protection from acoustic injury is mediated via alpha9 nicotinic acetylcholine receptors on outer hair cells. J Neurosci 22:10838-10846.
100. Mann RS. 1995. The specificity of homeotic gene function. Bioessays 17:855-863.
101. Maricich SM, Xia A, Mathes EL, Wang VY, Oghalai JS, Fritzsch B, Zoghbi HY. 2009. Atoh1-lineal neurons are required for hearing and for the survival of neurons in the spiral ganglion and brainstem accessory auditory nuclei. J Neurosci 29:11123-11133.
102. Marillat V, Sabatier C, Failli V, Matsunaga E, Sotelo C, Tessier-Lavigne M, Chedotal A. 2004. The slit receptor Rig-1/Robo3 controls midline crossing by hindbrain precerebellar neurons and axons. Neuron 43:69-79.
103. Marin F, Puelles L. 1995. Morphological fate of rhombomeres in quail/chick chimeras: a segmental analysis of hindbrain nuclei. Eur J Neurosci 7:1714-1738.
104. Marin F, Aroca P, Puelles L. 2008. Hox gene colinear expression in the avian medulla oblongata is correlated with pseudorhombomeric domains. Dev Biol 323:230-247.
105. Marrs GS, Morgan WJ, Howell DM, Spirou GA, Mathers PH. 2013. Embryonic origins of the mouse superior olivary complex. Dev Neurobiol 73:384-398.
106. Mazzoni EO, Mahony S, Closser M, Morrison CA, Nedelec S, Williams DJ, An D, Gifford DK, Wichterle H. 2013. Synergistic binding of transcription factors to cell-specific enhancers programs motor neuron identity. Nat Neurosci 16:1219-1227.
107. Miguez A, Ducret S, Di Meglio T, Parras C, Hmidan H, Haton C, Sekizar S, Mannioui A, Vidal M, Kerever A, Nyabi O, Haigh J, Zalc B, Rijli FM, Thomas JL. 2012. Opposing roles for Hoxa2 and Hoxb2 in hindbrain oligodendrocyte patterning. J Neurosci 32:17172-17185.
108. Misra M, Sours E, Lance-Jones C. 2012. Hox transcription factors influence motoneuron identity through the integrated actions of both homeodomain and non-homeodomain regions. Dev Dyn 241:718-731.
109. Moens CB, Selleri L. 2006. Hox cofactors in vertebrate development. Dev Biol 291:193-206.
110. Moreno-Bravo JA, Perez-Balaguer A, Martinez-Lopez JE, Aroca P, Puelles L, Martinez S, Puelles E. 2013. Role of Shh in the development of molecularly characterized tegmental nuclei in mouse rhombomere 1. Brain Struct Funct [Epub ahead of print].
111. Murphy P, Hill RE. 1991. Expression of the mouse labial-like homeobox-containing genes, Hox 2.9 and Hox 1.6, during segmentation of the hindbrain. Development 111:61-74.
112. Narita Y, Rijli FM. 2009. Hox genes in neural patterning and circuit formation in the mouse hindbrain. Curr Top Dev Biol 88:139-167.
113. Nolte C, and Krumlauf R. 2006. Expression of Hox genes in the nervous system of vertebrates. In HOX Gene Expression, S. Papageorgiou, ed. (Austin, TX, Landes Bioscience and Springer), pp. 14-41.
114. Oury F, Murakami Y, Renaud JS, Pasqualetti M, Charnay P, Ren SY, Rijli FM. 2006. Hoxa2- and rhombomere-dependent development of the mouse facial somatosensory map. Science 313:1408-1413.
115. Pascual M, Abasolo I, Mingorance-Le Meur A, Martinez A, Del Rio JA, Wright CV, Real FX, Soriano E. 2007. Cerebellar GABAergic progenitors adopt an external granule cell-like phenotype in the absence of Ptf1a transcription factor expression. Proc Natl Acad Sci U S A 104:5193-5198.
116. Pasqualetti M, Diaz C, Renaud JS, Rijli FM, Glover JC. 2007. Fate-mapping the mammalian hindbrain: segmental origins of vestibular projection neurons assessed using rhombomere-specific Hoxa2 enhancer elements in the mouse embryo. J Neurosci 27:9670-9681.
117. Pattyn A, Vallstedt A, Dias JM, Samad OA, Krumlauf R, Rijli FM, Brunet JF, Ericson J. 2003. Coordinated temporal and spatial control of motor neuron and serotonergic neuron generation from a common pool of CNS progenitors. Genes Dev 17:729-737.
118. Philippidou P, Walsh CM, Aubin J, Jeannotte L, Dasen JS. 2012. Sustained Hox5 gene activity is required for respiratory motor neuron development. Nat Neurosci 15:1636-1644.
119. Popperl H, Bienz M, Studer M, Chan SK, Aparicio S, Brenner S, Mann RS, Krumlauf R. 1995. Segmental expression of Hoxb-1 is controlled by a highly conserved autoregulatory loop dependent upon exd/pbx. Cell 81:1031-1042.
120. Pouchelon G, Frangeul L, Rijli FM, Jabaudon D. 2012. Patterning of pre-thalamic somatosensory pathways. Eur J Neurosci 35:1533-1539.
121. Prince V, Lumsden A. 1994. Hoxa-2 expression in normal and transposed rhombomeres: independent regulation in the neural tube and neural crest. Development 120:911-923.
122. Przyborski SA, Knowles BB, Ackerman SL. 1998. Embryonic phenotype of Unc5h3 mutant mice suggests chemorepulsion during the formation of the rostral cerebellar boundary. Development 125:41-50.
123. Ray RS, Dymecki SM. 2009. Rautenlippe Redux -- toward a unified view of the precerebellar rhombic lip. Curr Opin Cell Biol 21:741-747.
124. Renier N, Schonewille M, Giraudet F, Badura A, Tessier-Lavigne M, Avan P, De Zeeuw CI, Chedotal A. 2010. Genetic dissection of the function of hindbrain axonal commissures. PLoS Biol 8:e1000325.
125. Rodriguez CI, Dymecki SM. 2000. Origin of the precerebellar system. Neuron 27:475-486.
126. Rohrschneider MR, Elsen GE, Prince VE. 2007. Zebrafish Hoxb1a regulates multiple downstream genes including prickle1b. Dev Biol 309:358-372.
127. Rose MF, Ahmad KA, Thaller C, Zoghbi HY. 2009a. Excitatory neurons of the proprioceptive, interoceptive, and arousal hindbrain networks share a developmental requirement for Math1. Proc Natl Acad Sci U S A 106:22462-22467.
128. Rose MF, Ren J, Ahmad KA, Chao HT, Klisch TJ, Flora A, Greer JJ, Zoghbi HY. 2009b. Math1 is essential for the development of hindbrain neurons critical for perinatal breathing. Neuron 64:341-354.
129. Sabatier C, Plump AS, Le M, Brose K, Tamada A, Murakami F, Lee EY, Tessier-Lavigne M. 2004. The divergent Robo family protein rig-1/Robo3 is a negative regulator of slit responsiveness required for midline crossing by commissural axons. Cell 117:157-169.
130. Samad OA, Geisen MJ, Caronia G, Varlet I, Zappavigna V, Ericson J, Goridis C, Rijli FM. 2004. Integration of anteroposterior and dorsoventral regulation of Phox2b transcription in cranial motoneuron progenitors by homeodomain proteins. Development 131:4071-4083.
131. Sander M, Paydar S, Ericson J, Briscoe J, Berber E, German M, Jessell TM, Rubenstein JL. 2000. Ventral neural patterning by Nkx homeobox genes: Nkx6.1 controls somatic motor neuron and ventral interneuron fates. Genes Dev 14:2134-2139.
132. Saul SM, Brzezinski JAt, Altschuler RA, Shore SE, Rudolph DD, Kabara LL, Halsey KE, Hufnagel RB, Zhou J, Dolan DF, Glaser T. 2008. Math5 expression and function in the central auditory system. Mol Cell Neurosci 37:153-169.
133. Serafini T, Colamarino SA, Leonardo ED, Wang H, Beddington R, Skarnes WC, Tessier-Lavigne M. 1996. Netrin-1 is required for commissural axon guidance in the developing vertebrate nervous system. Cell 87:1001-1014.
134. Simmons DD. 2002. Development of the inner ear efferent system across vertebrate species. J Neurobiol 53:228-250.
135. Soshnikova N. 2013. Hox genes regulation in vertebrates. Dev Dyn [Epub ahead of print].
136. Stein E, Tessier-Lavigne M. 2001. Hierarchical organization of guidance receptors: silencing of netrin attraction by slit through a Robo/DCC receptor complex. Science 291:1928-1938.
137. Storm R, Cholewa-Waclaw J, Reuter K, Brohl D, Sieber M, Treier M, Muller T, Birchmeier C. 2009. The bHLH transcription factor Olig3 marks the dorsal neuroepithelium of the hindbrain and is essential for the development of brainstem nuclei. Development 136:295-305.
138. Studer M, Gavalas A, Marshall H, Ariza-McNaughton L, Rijli FM, Chambon P, Krumlauf R. 1998. Genetic interactions between Hoxa1 and Hoxb1 reveal new roles in regulation of early hindbrain patterning. Development 125:1025-1036.
139. Studer M, Lumsden A, Ariza-McNaughton L, Bradley A, Krumlauf R. 1996. Altered segmental identity and abnormal migration of motor neurons in mice lacking Hoxb-1. Nature 384:630-634.
140. Tan K, Le Douarin NM. 1991. Development of the nuclei and cell migration in the medulla oblongata. Application of the quail-chick chimera system. Anat Embryol (Berl) 183:321-343.
141. Tsuchida T, Ensini M, Morton SB, Baldassare M, Edlund T, Jessell TM, Pfaff SL. 1994. Topographic organization of embryonic motor neurons defined by expression of LIM homeobox genes. Cell 79:957-970.
142. Tumpel S, Cambronero F, Ferretti E, Blasi F, Wiedemann LM, Krumlauf R. 2007. Expression of Hoxa2 in rhombomere 4 is regulated by a conserved cross-regulatory mechanism dependent upon Hoxb1. Dev Biol 302:646-660.
143. Tumpel S, Wiedemann LM, Krumlauf R. 2009. Hox genes and segmentation of the vertebrate hindbrain. Curr Top Dev Biol 88:103-137.
144. Vaage S. 1969. The segmentation of the primitive neural tube in chick embryos (Gallus domesticus). A morphological, histochemical and autoradiographical investigation. Ergeb Anat Entwicklungsgesch 41:3-87.
145. Walsh EJ, McGee J, McFadden SL, Liberman MC. 1998. Long-term effects of sectioning the olivocochlear bundle in neonatal cats. J Neurosci 18:3859-3869.
146. Wang VY, Rose MF, Zoghbi HY. 2005. Math1 expression redefines the rhombic lip derivatives and reveals novel lineages within the brainstem and cerebellum. Neuron 48:31-43.
147. Wassef M, Cholley B, Heizmann CW, Sotelo C. 1992. Development of the olivocerebellar projection in the rat. II. Matching of the developmental compartmentations of the cerebellum and inferior olive through the projection map. J Comp Neurol 323:537-550.
148. Webb BD, Shaaban S, Gaspar H, Cunha LF, Schubert CR, Hao K, Robson CD, Chan WM, Andrews C, MacKinnon S, Oystreck DT, Hunter DG, Iacovelli AJ, Ye X, Camminady A, Engle EC, Jabs EW. 2012. HOXB1 founder mutation in humans recapitulates the phenotype of Hoxb1-/- mice. Am J Hum Genet 91:171-179.
149. Wilkinson DG, Bhatt S, Cook M, Boncinelli E, Krumlauf R. 1989. Segmental expression of Hox-2 homoeobox-containing genes in the developing mouse hindbrain. Nature 341:405-409.
150. Willott J. 2001. Handbook of mouse auditory research: from behavior to molecular biology. Boca Raton: CRC Press.
151. Wingate RJ. 2001. The rhombic lip and early cerebellar development. Curr Opin Neurobiol 11:82-88.
152. Wylie CJ, Hendricks TJ, Zhang B, Wang L, Lu P, Leahy P, Fox S, Maeno H, Deneris ES. 2010. Distinct transcriptomes define rostral and caudal serotonin neurons. J Neurosci 30:670-684.
153. Yamada M, Terao M, Terashima T, Fujiyama T, Kawaguchi Y, Nabeshima Y, Hoshino M. 2007. Origin of climbing fiber neurons and their developmental dependence on Ptf1a. J Neurosci 27:10924-10934.
154. Yee KT, Simon HH, Tessier-Lavigne M, O'Leary DM. 1999. Extension of long leading processes and neuronal migration in the mammalian brain directed by the chemoattractant netrin-1. Neuron 24:607-622.
155. Zhao XD, Han X, Chew JL, Liu J, Chiu KP, Choo A, Orlov YL, Sung WK, Shahab A, Kuznetsov VA, Bourque G, Oh S, Ruan Y, Ng HH, Wei CL. 2007. Whole-genome mapping of histone H3 Lys4 and 27 trimethylations reveals distinct genomic compartments in human embryonic stem cells. Cell Stem Cell 1:286-298.