Hoxb1 controls anteroposterior identity of vestibular projection neurons

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Chen, Yiju ^a   Takano Maruyama, Masumi ^a   Fritzsch, Bernd ^b   Gaufo, Gary O ^a  

^a UNIVERSITY OF TEXAS AT SAN ANTONIO   (United States)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN; HOXB 1 PROTEIN; PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR LBX1; TRANSCRIPTION FACTOR PHOX2A; UNCLASSIFIED DRUG; ASCL1 PROTEIN, MOUSE; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; HOMEODOMAIN PROTEIN; HOXB1 HOMEODOMAIN PROTEIN; HYBRID PROTEIN; LBX1H PROTEIN, MOUSE; MUSCLE PROTEIN; PHOX2A PROTEIN, MOUSE; TLX3 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL TISSUE; ANTERIOR POSTERIOR AXIS; ARTICLE; CONTROLLED STUDY; EMBRYO; EYE MOVEMENT; GENE; GENE TARGETING; HOXB 1 GENE; LATERAL VESTIBULAR NUCLEUS; MOUSE; NEUROANATOMY; NEUROMERE; NONHUMAN; PHENOTYPE; PROTEIN FUNCTION; RHOMBENCEPHALON; SPINAL CORD; SPINAL CORD MOTONEURON; STEREOTYPY; VESTIBULAR NERVOUS SYSTEM; ANIMAL; CYTOLOGY; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MORPHOGENESIS; MOUSE MUTANT; NERVE CELL; PHYSIOLOGY; PRENATAL DEVELOPMENT;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BODY PATTERNING; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GREEN FLUORESCENT PROTEINS; HOMEODOMAIN PROTEINS; MICE; MICE, KNOCKOUT; MUSCLE PROTEINS; NEURONS; RECOMBINANT FUSION PROTEINS; SPINAL CORD; VESTIBULAR NUCLEUS, LATERAL;

EID: 84859261049     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0034762     Document Type: Article

References (70)

1. Jessell TM, (2000) Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat Rev Genet 1: 20-29.
2. Lumsden A, Krumlauf R, (1996) Patterning the vertebrate neuraxis. Science 274: 1109-1115.
3. Gaufo GO, Wu S, Capecchi MR, (2004) Contribution of Hox genes to the diversity of the hindbrain sensory system. Development 131: 1259-1266.
4. Lee KJ, Dietrich P, Jessell TM, (2000) Genetic ablation reveals that the roof plate is essential for dorsal interneuron specification. Nature 403: 734-740.
5. Muller T, Brohmann H, Pierani A, Heppenstall PA, Lewin GR, et al. (2002) The homeodomain factor lbx1 distinguishes two major programs of neuronal differentiation in the dorsal spinal cord. Neuron 34: 551-562.
6. Oury F, Murakami Y, Renaud JS, Pasqualetti M, Charnay P, et al. (2006) Hoxa2- and rhombomere-dependent development of the mouse facial somatosensory map. Science 313: 1408-1413.
7. Sieber MA, Storm R, Martinez-de-la-Torre M, Muller T, Wende H, et al. (2007) Lbx1 acts as a selector gene in the fate determination of somatosensory and viscerosensory relay neurons in the hindbrain. J Neurosci 27: 4902-4909.
8. Fritzsch B, Pauley S, Feng F, Matei V, Nichols DH, (2006) The evolution of the vertebrate auditory system: transformations of vestibular mechanosensory cells for sound processing is combined with newly generated central processing neurons. Int J Comp Psychol 19.
9. Maklad A, Fritzsch B, (2003) Development of vestibular afferent projections into the hindbrain and their central targets. Brain Res Bull 60: 497-510.
10. Bermingham NA, Hassan BA, Wang VY, Fernandez M, Banfi S, et al. (2001) Proprioceptor pathway development is dependent on Math1. Neuron 30: 411-422.
11. 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.
12. Gross MK, Dottori M, Goulding M, (2002) Lbx1 specifies somatosensory association interneurons in the dorsal spinal cord. Neuron 34: 535-549.
13. Helms AW, Battiste J, Henke RM, Nakada Y, Simplicio N, et al. (2005) Sequential roles for Mash1 and Ngn2 in the generation of dorsal spinal cord interneurons. Development 132: 2709-2719.
14. Pattyn A, Goridis C, Brunet JF, (2000) Specification of the central noradrenergic phenotype by the homeobox gene Phox2b. Mol Cell Neurosci 15: 235-243.
15. Pillai A, Mansouri A, Behringer R, Westphal H, Goulding M, (2007) Lhx1 and Lhx5 maintain the inhibitory-neurotransmitter status of interneurons in the dorsal spinal cord. Development 134: 357-366.
16. Qian Y, Shirasawa S, Chen CL, Cheng L, Ma Q, (2002) Proper development of relay somatic sensory neurons and D2/D4 interneurons requires homeobox genes Rnx/Tlx-3 and Tlx-1. Genes Dev 16: 1220-1233.
17. 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.
18. Lee KJ, Jessell TM, (1999) The specification of dorsal cell fates in the vertebrate central nervous system. Annu Rev Neurosci 22: 261-294.
19. Cheng L, Arata A, Mizuguchi R, Qian Y, Karunaratne A, et al. (2004) Tlx3 and Tlx1 are post-mitotic selector genes determining glutamatergic over GABAergic cell fates. Nat Neurosci 7: 510-517.
20. Cheng L, Samad OA, Xu Y, Mizuguchi R, Luo P, et al. (2005) Lbx1 and Tlx3 are opposing switches in determining GABAergic versus glutamatergic transmitter phenotypes. Nat Neurosci 8: 1510-1515.
21. Mizuguchi R, Kriks S, Cordes R, Gossler A, Ma Q, et al. (2006) Ascl1 and Gsh1/2 control inhibitory and excitatory cell fate in spinal sensory interneurons. Nat Neurosci 9: 770-778.
22. Carpenter MB, (1985) Core text of neuroanatomy Baltimore Williams & Wilkins pp. xiv 473.
23. Kandel ER, Schwartz JH, Jessell TM, (2000) Principles of neural science New York McGraw-Hill, Health Professions Division pp. xli 1414.
24. 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.
25. 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.
26. 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.
27. 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.
28. Glover JC, (1994) The organization of vestibulo-ocular and vestibulospinal projections in the chicken embryo. Eur J Morphol 32: 193-200.
29. Glover JC, (1995) Rhombomeres and innervation fields. Trends Neurosci 18: 486-487; author reply 487-488.
30. Glover JC, (2000) Neuroepithelial 'compartments' and the specification of vestibular projections. Prog Brain Res 124: 3-21.
31. Glover JC, (2001) Correlated patterns of neuron differentiation and Hox gene expression in the hindbrain: a comparative analysis. Brain Res Bull 55: 683-693.
32. Glover JC, Petursdottir G, (1988) Pathway specificity of reticulospinal and vestibulospinal projections in the 11-day chicken embryo. J Comp Neurol 270: 25-38 60-21.
33. Glover JC, Petursdottir G, (1991) Regional specificity of developing reticulospinal, vestibulospinal, and vestibulo-ocular projections in the chicken embryo. J Neurobiol 22: 353-376.
34. Oury F, Rijli FM, (2007) [Hoxa2: a key gene for the facial somatosensory map]. Med Sci (Paris) 23: 247-249.
35. Dasen JS, Liu JP, Jessell TM, (2003) Motor neuron columnar fate imposed by sequential phases of Hox-c activity. Nature 425: 926-933.
36. 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.
37. Davenne M, Maconochie MK, Neun R, Pattyn A, Chambon P, et al. (1999) Hoxa2 and Hoxb2 control dorsoventral patterns of neuronal development in the rostral hindbrain. Neuron 22: 677-691.
38. Gaufo GO, Flodby P, Capecchi MR, (2000) Hoxb1 controls effectors of sonic hedgehog and Mash1 signaling pathways. Development 127: 5343-5354.
39. 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.
40. Maricich SM, Xia A, Mathes EL, Wang VY, Oghalai JS, et al. (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.
41. 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.
42. Goddard JM, Rossel M, Manley NR, Capecchi MR, (1996) Mice with targeted disruption of Hoxb-1 fail to form the motor nucleus of the VIIth nerve. Development 122: 3217-3228.
43. McClintock JM, Kheirbek MA, Prince VE, (2002) Knockdown of duplicated zebrafish hoxb1 genes reveals distinct roles in hindbrain patterning and a novel mechanism of duplicate gene retention. Development 129: 2339-2354.
44. Popperl H, Bienz M, Studer M, Chan SK, Aparicio S, et al. (1995) Segmental expression of Hoxb-1 is controlled by a highly conserved autoregulatory loop dependent upon exd/pbx. Cell 81: 1031-1042.
45. 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.
46. 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.
47. Marshall H, Studer M, Popperl H, Aparicio S, Kuroiwa A, et al. (1994) A conserved retinoic acid response element required for early expression of the homeobox gene Hoxb-1. Nature 370: 567-571.
48. Straka H, Baker R, Gilland E, (2001) Rhombomeric organization of vestibular pathways in larval frogs. J Comp Neurol 437: 42-55.
49. Fritzsch B, Dillard M, Lavado A, Harvey NL, Jahan I, (2010) Canal cristae growth and fiber extension to the outer hair cells of the mouse ear require prox1 activity. PLoS One 5: e9377.
50. Carpenter MB, Sutin J, Strong OS, (1983) Human neuroanatomy: (formerly Strong and Elwyn's Human neuroanatomy) Baltimore Williams & Wilkins pp. xiv 872.
51. Altman J, Bayer SA, (1980) Development of the brain stem in the rat. III. Thymidine-radiographic study of the time of origin of neurons of the vestibular and auditory nuclei of the upper medulla. J Comp Neurol 194: 877-904.
52. Pattyn A, Morin X, Cremer H, Goridis C, Brunet JF, (1997) Expression and interactions of the two closely related homeobox genes Phox2a and Phox2b during neurogenesis. Development 124: 4065-4075.
53. Briscoe J, Pierani A, Jessell TM, Ericson J, (2000) A homeodomain protein code specifies progenitor cell identity and neuronal fate in the ventral neural tube. Cell 101: 435-445.
54. Bell E, Wingate RJ, Lumsden A, (1999) Homeotic transformation of rhombomere identity after localized Hoxb1 misexpression. Science 284: 2168-2171.
55. Hafen E, Levine M, Gehring WJ, (1984) Regulation of Antennapedia transcript distribution by the bithorax complex in Drosophila. Nature 307: 287-289.
56. Lewis EB, (1978) A gene complex controlling segmentation in Drosophila. Nature 276: 565-570.
57. Waskiewicz AJ, Rikhof HA, Moens CB, (2002) Eliminating zebrafish pbx proteins reveals a hindbrain ground state. Dev Cell 3: 723-733.
58. Samad OA, Geisen MJ, Caronia G, Varlet I, Zappavigna V, et al. (2004) Integration of anteroposterior and dorsoventral regulation of Phox2b transcription in cranial motoneuron progenitors by homeodomain proteins. Development 131: 4071-4083.
59. Fritzsch B, (1998) Evolution of the vestibulo-ocular system. Otolaryngol Head Neck Surg 119: 182-192.
60. Paxinos G, Ashwell KWS, Tèork I, (1994) Atlas of the developing rat nervous system San Diego Academic Press 1 v. (unpaged) p.
61. Paxinos G, Franklin KBJ, (2001) The mouse brain in stereotaxic coordinates San Diego Academic Press 1 v. (various pagings) p.
62. Straka H, Baker R, Gilland E, (2002) The frog as a unique vertebrate model for studying the rhombomeric organization of functionally identified hindbrain neurons. Brain Res Bull 57: 301-305.
63. Straka H, Vibert N, Vidal PP, Moore LE, Dutia MB, (2005) Intrinsic membrane properties of vertebrate vestibular neurons: function, development and plasticity. Prog Neurobiol 76: 349-392.
64. Landwehr S, Dicke U, (2005) Distribution of GABA, glycine, and glutamate in neurons of the medulla oblongata and their projections to the midbrain tectum in plethodontid salamanders. J Comp Neurol 490: 145-162.
65. Lumsden A, Keynes R, (1989) Segmental patterns of neuronal development in the chick hindbrain. Nature 337: 424-428.
66. Manns M, Fritzsch B, (1992) Retinoic acid affects the organization of reticulospinal neurons in developing Xenopus. Neurosci Lett 139: 253-256.
67. Papalopulu N, Clarke JD, Bradley L, Wilkinson D, Krumlauf R, et al. (1991) Retinoic acid causes abnormal development and segmental patterning of the anterior hindbrain in Xenopus embryos. Development 113: 1145-1158.
68. Helms AW, Johnson JE, (1998) Progenitors of dorsal commissural interneurons are defined by MATH1 expression. Development 125: 919-928.
69. Müller T, Anlag K, Wildner H, Britsch S, Treier M, et al. (2005) The bHLH factor Olig3 coordinates the specification of dorsal neurons in the spinal cord. Genes Dev 19: 733-743.
70. Storm R, Cholewa-Waclaw J, Reuter K, Bröhl D, Sieber M, et al. (2008) 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.