Hoxa2 and Hoxb2 control dorsoventral patterns of neuronal development in the rostral hindbrain

Neuron

Volumn 22, Issue 4, 1999, Pages 677-691

  Davenne, Marc ^a   Maconochie, Mark K ^b   Neun, Rüdiger ^a   Pattyn, Alexandre ^c   Chambon, Pierre ^a   Krumlauf, Robb ^b   Rijli, Filippo M ^a  

^a INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^b NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^c AIX MARSEILLE UNIVERSITÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

HOMEODOMAIN PROTEIN; PROTEIN HOXA2; PROTEIN HOXB2; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; GENE EXPRESSION REGULATION; HOMEOBOX; MOUSE; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEUROMERE; NONHUMAN; PRIORITY JOURNAL; RHOMBENCEPHALON;

EID: 0033119868     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0896-6273(00)80728-X     Document Type: Article

References (60)

1. Auclair, F., Valdes, N., and 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.
2. Barrow, J.R., and Capecchi, M.R. (1996). Targeted disruption of the Hoxb-2 locus in mice interferes with expression of Hoxb-1 and Hoxb-4. Development 122, 3817-3828.
3. 1+ interneurons that require PAX6 for their development. Development 124, 4493-4503.
4. Carpenter, E.M., Goddard, J.M., Chisaka, O., Manley, N.R., and Capecchi, M.R. (1993). Loss of Hox-A1 (Hox-1.6) function results in the reorganization of the murine hindbrain. Development 118, 1063-1075.
5. Clarke, J.D., and Lumsden, A. (1993). Segmental repetition of neuronal phenotype sets in the chick embryo hindbrain. Development 118, 151-162.
6. Clarke, J.D., Erskine, L., and Lumsden, A. (1998). Differential progenitor dispersal and the spatial origin of early neurons can explain the predominance of single-phenotype clones in the chick hindbrain. Dev. Dyn. 212, 14-26.
7. Ensini, M., Tsuchida, T.N., Belting, H.G., and Jessell, T.M. (1998). The control of rostrocaudal pattern in the developing spinal cord: specification of motor neuron subtype identity is initiated by signals from paraxial mesoderm. Development 125, 969-982.
8. Ericson, J., Rashbass, P., Schedl, A., Brenner-Morton, S., Kawakami, A., van Heyningen, V., Jessell, T.M., and Briscoe, J. (1997). Pax6 controls progenitor cell identity and neuronal fate in response to graded Shh signaling. Cell 90, 169-180.
9. Fode, C., Gradwohl, G., Morin, X., Dierich, A., Le Meur, M., Goridis, C., and Guillemot, F. (1998). The bHLh protein NEUROGENIN 2 is a determination factor for epibranchial placode-derived sensory neurons. Neuron 20, 483-494.
10. Fraser, S., Keynes, R., and Lumsden, A. (1990). Segmentation in the chick embryo hindbrain is defined by cell lineage restrictions. Nature 344, 431-435.
11. Gavalas, A., Davenne, M., Lumsden, A., Chambon, P., and Rijli, F.M. (1997). Role of Hoxa-2 in axon pathfinding and rostral hindbrain patterning. Development 124, 3693-3702.
12. Gavalas, A., Studer, M., Lumsden, A., Rijli, F.M., Krumlauf, R., and Chambon, P. (1998). Hoxa1 and Hoxbl synergize in patterning the hindbrain, cranial nerves and second pharyngeal arch. Development 125, 1123-1136.
13. Goddard, J.M., Rossel, M., Manley, N.R., and Capecchi, M.R. (1996). Mice with targeted disruption of Hoxb-1 fail to form the motor nucleus of the vIIth nerve. Development 122, 3217-3228.
14. Gould, A., Itasaki, N., and Krumlauf, R. (1998). Initiation of rhombomeric Hoxb4 expression requires induction by somites and a retinoid pathway. Neuron 21, 39-51.
15. Goulding, M.D., Lumsden, A., and Gruss, P. (1993). Signals from the notochord and floor plate regulate the region-specific expression of two Pax genes in the developing spinal cord. Development 117, 1001-1016.
16. Gradwohl, G., Fode, C., and Guillemot, F. (1996). Restricted expression of a novel murine atonal-related bHLH protein in undifferentiated neural precursors. Dev. Biol. 180, 227-241.
17. Graham, A., Maden, M., and Krumlauf, R. (1991). The murine Hox-2 genes display dynamic D-V patterns of expression during central nervous system development. Development 112, 255-264.
18. Grapin-Botton, A., Bonnin, M.A., and Le Douarin, N.M. (1997). Hox gene induction in the neural tube depends on three parameters: competence, signal supply and paralogue group. Development 124, 849-859.
19. Guillemot, F., and Joyner, A.L. (1993). Dynamic expression of the murine Achaete-Scute homologue Mash-1 in the developing nervous system. Mech. Dev. 42, 171-185.
20. Guthrie, S., and Lumsden, A. (1991). Formation and regeneration of rhombomere boundaries in the developing chick hindbrain. DevelOpment 112, 221-229.
21. Hirsch, M.R., Tiveron, M.C., Guillemot, F., Brunet, J.F., and Goridis, C. (1998). Control of noradrenergic differentiation and Phox2a expression by MASH1 in the central and peripheral nervous system. Development 125, 599-608.
22. Irving, C., Nieto, M.A., Das Gupta, R., Charnay, P., and Wilkinson, D.G. (1996). Progressive spatial restriction of Sek-1 and Krox-20 gene expression during hindbrain segmentation. Dev. Biol. 173, 26-38.
23. Itasaki, N., Sharpe, J., Morrison, A., and Krumlauf, R. (1996). Reprogramming Hox expression in the vertebrate hindbrain: Influence of paraxial mesoderm and rhombomere transposition. Neuron 16, 487-500.
24. Kageyama, R., and Nakanishi, S. (1997). Helix-loop-helix factors in growth and differentiation of the vertebrate nervous system. Curr. Opin. Genet. Dev. 7, 659-665.
25. Lo, L.C., Johnson, J.E., Wuenschell, C.W., Saito, T., and Anderson, D.J. (1991). Mammalian achaete-scute homolog 1 is transiently expressed by spatially restricted subsets of early neuroepithelial and neural crest cells. Genes. Dev. 5, 1524-1537.
26. Lo, L., Tiveron, M.C., and Anderson, D.J. (1998). MASH1 activates expression of the paired homeodomain transcription factor Phox2a, and couples pan-neuronal and subtype-specific components of autonomic neuronal identity. Development 125, 609-620.
27. Lumsden, A., and Keynes, R. (1989). Segmental patterns of neuronal development in the chick hindbrain. Nature 337, 424-428.
28. Lumsden, A., and Krumlauf, R. (1996). Patterning the vertebrate neuraxis. Science 274, 1109-1115.
29. Lumsden, A., Clarke, J.D., Keynes, R., and Fraser, S. (1994). Early phenotypic choices by neuronal precursors, revealed by clonal analysis of the chick embryo hindbrain. Development 120, 1581-1589.
30. Ma, Q., Sommer, L., Cserjesi, P., and Anderson, D.J. (1997). Mash1 and neurogenin1 expression patterns define complementary domains of neuroepithelium in the developing CNS and are correlated with regions expressing notch ligands. J. Neurosci. 17, 3644-3652.
31. Maconochie, M.K., Nonchev, S., Studer, M., Chan, S.K., Popperl, H., Sham, M.H., Mann, R.S., and Krumlauf, R. (1997). Cross-regulation in the mouse Hoxb complex: The expression of Hoxb2 in rhombomere 4 is regulated by Hoxbl. Genes. Dev. 11, 1885-1895.
32. Marin, F., and Puelles, L. (1995). Morphological fate of rhombomeres in quail/chick chimeras: A segmental analysis of hindbrain nuclei. Eur. J. Neurosci. 7, 1714-1738.
33. Mark, M., Lufkin, T., Vonesch, J.L., Ruberte, E., Olivo, J.C., Dolle, P., Gorry, P., Lumsden, A., and Chambon, P. (1993). Two rhombomeres are altered in Hoxa-1 mutant mice. Development 119, 319-338.
34. Marshall, H., Nonchev, S., Sham, M.H., Muchamore, I., Lumsden, A., and Krumlauf, R. (1992). Retinoic acid alters hindbrain Hox code and induces transformation of rhombomeres 2/3 into a 4/5 identity. Nature 360, 737-741.
35. McKay, I.J., Lewis, J., and Lumsden, A. (1997). Organization and development of facial motor neurons in the kreisler mutant mouse. Eur. J. Neurosci. 9, 1499-1506.
36. Nonchev, S., Vesque, C., Maconochie, M., Seitanidou, T., Ariza-McNaughton, L., Frain, M., Marshall, H., Sham, M.H., Krumlauf, R., and Charnay, P. (1996). Segmental expression of Hoxa-2 in the hindbrain is directly regulated by Krox-20. Development 122, 543-554.
37. Osumi, N., Hirota, A., Ohuchi, H., Nakafuku, M., Iimura, T., Kuratani, S., Fujiwara, M., Noji, S., and Eto, K. (1997). Pax-6 is involved in the specification of hindbrain motor neuron subtype. Development 124, 2961-2972.
38. Pattyn, A., Morin, X., Cremer, H., Goridis, C., and Brunet, J.F. (1997). Expression and interactions of the two closely related homeobox genes Phox2a and Phox2b during neurogenesis. Development 124, 4065-4075.
39. Pfaff, S., and Kintner, C. (1998). Neuronal diversification: Development of motor neuron subtypes. Curr. Opin. Neurobiol. 8, 27-36.
40. Rijli, F.M., Mark, M., Lakkaraju, S., Dierich, A., Dolle, P., and ChamBon, P. (1993). A homeotic transformation is generated in the rostral branchial region of the head by disruption of Hoxa-2, which acts as a selector gene. Cell 75, 1333-1349.
41. Rijli, F.M., Gavalas, A., and Chambon, P. (1998). Segmentation and specification in the branchial region of the head: The role of the Hox selector genes. Int. J. Dev. Biol. 42, 393-401.
42. Roztocil, T., Matter-Sadzinski, L., Alliod, C., Ballivet, M., and Matter, J.M. (1997). NeuroM, a neural helix-loop-helix transcription factor, defines a new transition stage in neurogenesis. Development 124, 3263-3272.
43. Schneider-Maunoury, S., Seitanidou, T., Charnay, P., and Lumsden, A. (1997). Segmental and neuronal architecture of the hindbrain of Krox-20 mouse mutants. Development 124, 1215-1226.
44. Sham, M.H., Vesque, C., Nonchev, S., Marshall, H., Frain, M., Gupta, R.D., Whiting, J., Wilkinson, D., Charnay, P., and Krumlauf, R. (1993). The zinc finger gene Krox20 regulates HoxB2 (Hox2.8) during hindbrain segmentation. Cell 72, 183-196.
45. Simon, H., and Lumsden, A. (1993). Rhombomere-specific origin of the contralateral vestibulo-acoustic efferent neurons and their migration across the embryonic midline. Neuron 11, 209-220.
46. Simon, H., Hornbruch, A., and Lumsden, A. (1995). Independent assignment of antero-posterior and dorso-ventral positional values in the developing chick hindbrain. Curr. Biol. 5, 205-214.
47. Sommer, L., Ma, Q., and Anderson, D.J. (1996). Neurogenins, a novel family of atonal-related bHLH transcription factors, are putative mammalian neuronal determination genes that reveal progenitor cell heterogeneity in the developing CNS and PNS. Mol. Cell. Neurosci. 8, 221-241.
48. Stoykova, A., Gotz, M., Gruss, P., and Price, J. (1997). Pax6-dependent regulation of adhesive patterning, R-cadherin expression and boundary formation in developing forebrain. Development 124, 3765-3777.
49. Stuart, E.T., Kioussi, C., and Gruss, P. (1994). Mammalian Pax genes. Annu. Rev. Genet. 28, 219-236.
50. Studer, M., Lumsden, A., Ariza-McNaughton, L., Bradley, A., and Krumlauf, R. (1996). Altered segmental identity and abnormal migration of motor neurons in mice lacking Hoxb-1. Nature 384, 630-634.
51. Studer, M., Gavalas, A., Marshall, H., Ariza-McNaughton, L., Rijli, F.M., Chambon, P., and Krumlauf, R. (1998). Genetic interactions between Hoxa1 and Hoxb1 reveal new roles in regulation of early hindbrain patterning. Development 125, 1025-1036.
52. Takebayashi, K., Takahashi, S., Yokota, C., Tsuda, H., Nakanishi, S., Asashima, M., and Kageyama, R. (1997). Conversion of ectoderm into a neural fate by ATH-3, a vertebrate basic helix-loop-helix gene homologous to Drosophila proneural gene atonal. EMBO J. 16, 384-395.
53. Tanabe, Y., and Jessell, T.M. (1996). Diversity and pattern in the developing spinal cord. Science 274, 1115-1123.
54. Theil, T., Frain, M., Gilardi-Hebenstreit, P., Flenniken, A., Charnay, P., and Wilkinson, D.G. (1998). Segmental expression of the EphA4 (Sek-1) receptor tyrosine kinase in the hindbrain is under direct transcriptional control of Krox-20. Development 125, 443-452.
55. Tiret, L., Le Mouellic, H., Maury, M., and Brulet, P. (1998). Increased apoptosis of motoneurons and altered somatotopic maps in the brachial spinal cord of Hoxc-8-deficient mice. Development 125, 279-291.
56. Wizenmann, A., and Lumsden, A. (1997). Segregation of rhombomeres by differential chemoaffinity. Mol. Cell. Neurosci. 9, 448-459.
57. Wolpert, L. (1969). Positional information and the spatial pattern of cellular differentiation. J. Theor. Biol. 25, 1-47.
58. Xu, Q., Alldus, G., Holder, N., and Wilkinson, D.G. (1995). Expression of truncated Sek-1 receptor tyrosine kinase disrupts the segmental restriction of gene expression in the xenopus and zebrafish hindbrain. Development 121, 4005-4016.
59. Ye, W., Shimamura, K., Rubenstein, J.L., Hynes, M.A., and RosenThal, A. (1998). FGF and Shh signals control dopaminergic and serotonergic cell fate in the anterior neural plate. Cell 93, 755-766.
60. Zhang, M., Kim, H.J., Marshall, H., Gendron-Maguire, M., Lucas, D.A., Baron, A., Gudas, L.J., Gridley, T., Krumlauf, R., and Grippo, J.F. (1994). Ectopic Hoxa-1 induces rhombomere transformation in mouse hindbrain. Development 120, 2431-2442.