Neuronal defects in the hindbrain of Hoxa1, Hoxb1 and Hoxb2 mutants reflect regulatory interactions among these Hox genes

Development

Volumn 130, Issue 23, 2003, Pages 5663-5679

  Gavalas, Anthony ^a,d   Ruhrberg, Christiana ^a,e   Livet, Jean ^b   Henderson, Christopher E ^b   Krumlauf, Robb ^a,c  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^b INSERM   (France)

^c STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

^d KING'S COLLEGE LONDON   (United Kingdom)

^e UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Gene regulation; Hindbrain; Hox genes; Mouse; Neural development; Neurogenesis; Neuronal migration; Neuronal patterning; Segmentation

Indexed keywords

BIOLOGICAL MARKER; HOX PROTEIN; HOXA1 PROTEIN; HOXB1 PROTEIN; HOXB2 PROTEIN; MUTANT PROTEIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; APOPTOSIS; BRAIN DEVELOPMENT; BRAIN DISEASE; BRAIN NERVE CELL; CELL DIFFERENTIATION; CELL MIGRATION; CELL POPULATION; CELL SURVIVAL; CONTROLLED STUDY; DISEASE SEVERITY; EMBRYO PATTERN FORMATION; EMBRYO SEGMENTATION; FACIAL NERVE NUCLEUS; GENE ACTIVATION; GENE EXPRESSION; GENE INTERACTION; MOTONEURON; MOUSE; MOUSE MUTANT; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; RHOMBENCEPHALON; TRIGEMINAL NUCLEUS;

ANIMALS; APOPTOSIS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BCL-2-ASSOCIATED X PROTEIN; BODY PATTERNING; CELL DIFFERENTIATION; CELL MOVEMENT; DNA-BINDING PROTEINS; EMBRYO; GATA2 TRANSCRIPTION FACTOR; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GESTATIONAL AGE; HOMEODOMAIN PROTEINS; IN SITU HYBRIDIZATION; IN SITU NICK-END LABELING; MICE; NERVE TISSUE PROTEINS; NEURONS; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; RHOMBENCEPHALON; TRANSCRIPTION FACTORS;

ANIMALIA;

EID: 0346752186     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.00802     Document Type: Review

References (89)

1. Altman, J. and Bayer, S. (1982). Development of the Cranial Nerve Ganglia and Related Nuclei in the Rat. Berlin: Springer-Verlag.
2. Arber, S., Ladle, D. R., Lin, J. H., Frank, E. and Jessell, T. M. (2000). ETS gene Er81 controls the formation of functional connections between group Ia sensory afferents and motor neurons. Cell 101, 485-498.
3. 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.
4. Bell, E., Wingate, R. and Lumsden, A. (1999). Homeotic transformation of rhombomere identity after localized Hoxb1 misexpression. Science 284, 2168-2171.
5. Bloch-Gallego, E., Ezan, F., Tessier-Lavigne, M. and Sotelo, C. (1999). Floor plate and netrin-1 are involved in the migration and survival of inferior olivary neurons. J. Neurosci. 19, 4407-4420.
6. Brose, K. and Tessier-Lavigne, M. (2000). Slit proteins: key regulators of axon guidance, axonal branching, and cell migration. Curr. Opin. Neurobiol. 10, 95-102.
7. Carpenter, E. M., Goddard, J. M., Chisaka, O., Manley, N. R. and Capecchi, M. R. (1993). Loss of Hoxa-1 (Hox-1.6) function results in the reorganization of the murine hindbrain. Development 118, 1063-1075.
8. Caton, A., Hacker, A., Naeem, A., Livet, J., Maina, F., Bladt, E., Klein, R., Birchmeier, C. and Guthrie, S. (2000). The branchial arches and HGF are growth-promoting and chemoattractant for cranial motor axons. Development 127, 1751-1766.
9. Chisaka, O., Musci, T. and Capecchi, M. (1992). Developmental defects of the ear, cranial nerves and hindbrain resulting from targeted disruption of the mouse homeobox gene Hox-1.6. Nature 355, 516-520.
10. Cordes, S. P. and Barsh, G. S. (1994). The Mouse segmentation gene kr encodes a novel basic domain-leucine zipper transcription factor. Cell 79, 1025-1034.
11. Covell, D. A., Jr and Noden, D. M. (1989). Embryonic development of the chick primary trigeminal sensory-motor complex. J. Comp. Neurol. 286, 488-503.
12. Davenne, M., Maconochie, M., Neun, R., Brunet, J.-F., Chambon, P., Krumlauf, R. and Rijli, E. (1999). Hoxa2 and Hoxb2 control dorsoventral patterns of neuronal development in the rostral hindbrain. Neuron 22, 677-691.
13. Deckwerth, T. L., Easton, R. M., Knudson, C. M., Korsmeyer, S. J. and Johnson, E. M., Jr (1998). Placement of the BCL2 family member BAX in the death pathway of sympathetic neurons activated by trophic factor deprivation. Exp. Neurol. 152, 150-162.
14. del Toro, E. D., Borday, V., Davenne, M., Neun, R., Rijli, F. M. and Champagnat, J. (2001). Generation of a novel functional neuronal circuit in Hoxa1 mutant mice. J. Neurosci. 21, 5637-5642.
15. deLapeyriere, O. and Henderson, C. E. (1997). Motoneuron differentiation, survival and synaptogenesis. Curr. Opin. Genet. Dev. 7, 642-650.
16. Di Rocco, G., Mavilio, F. and Zappavigna, V. (1997). Functional dissection of a transcriptionally active, target-specific Hox-Pbx complex. EMBO J. 16, 3644-3654.
17. Di Rocco, G., Gavalas, A., Popperl, H., Krumlauf, R., Mavilio, F. and Zappavigna, V. (2001a). The recruitment of SOX/OCT complexes and the differential activity of HOXA1 and HOXB1 modulate the Hoxb1 auto-regulatory enhancer function. J. Biol. Chem. 276, 20506-20515.
18. Di Rocco, G., Gavalas, A., Popperl, H., Krumlauf, R., Mavilio, F. and Zappavigna, V. (2001b). The recruitment of SOX/OCT complexes and the differential activity of HOXA1 and HOXB1 modulate the Hoxb1 auto-regulatory enhancer function. J. Biol. Chem. 1, 1.
19. Dollé, P., Lufkin, T., Krumlauf, R., Mark, M., Duboule, D. and Chambon, P. (1993). Local alterations of Krox-20 ahd Hox gene expression in the hindbrain suggest lack of rhombomeres 4 and 5 in homozygote null Hoxa-1 (Hox-1.6) mutant embryos. Proc. Natl. Acad. Sci. USA 90, 7666-7670.
20. Dubreuil, V., Hirsch, M., Pattyn, A., Brunet, J. and Goridis, C. (2000). The Phox2b transcription factor coordinately regulates neuronal cell cycle exit and identity. Development 127, 5191-5201.
21. Dupé, V., Davenne, M., Brocard, J., Dollé, P., Mark, M., Dietrich, A., Chambon, P. and Rijli, E. (1997). In vivo functional analysis of the Hoxa1 3′ retinoid response element (3′ RARE). Development 124, 399-410.
22. Ensini, M., Tsuchida, T., Belting, H.-G. and Jessell, T. (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.
23. Ericson, J., Thor, S., Edlund, T., Jessell, T. M. and Yamada, T. (1992). Early stages of motor neuron differentiation revealed by expression of homeobox gene Islet-1. Science 256, 1555-1560.
24. 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.
25. Ferretti, E., Marshall, H., Pöpperl, H., Maconochie, M., Krumlauf, R. and Blasi, F. (2000). Segmental expression of Hoxb2 in r4 requires two distinct sites that facilitate co-operative interactions and ternary complex formation between Perp, Pbx and Hox proteins. Development 127, 155-166.
26. Fraser, S., Keynes, R. and Lumsden, A. (1990). Segmentation in the chick embryo hindbrain is defined by cell lineage restrictions. Nature 344, 431-435.
27. Frohman, M. A., Boyle, M. and Martin, G. R. (1990). Isolation of the mouse Hox-2.9 gene; analysis of embryonic expression suggests that positional information along the anterior-posterior axis is specified by mesoderm. Development 110, 589-607.
28. Garel, S., Garcia-Dominguez, M. and Charnay, P. (2000). Control of the migratory pathway of facial branchiomotor neurones. Development 127, 5297-5307.
29. Gaufo, G. O., Flodby, P. and Capecchi, M. R. (2000). Hoxb1 controls effectors of sonic hedgehog and Mash1 signaling pathways. Development 127, 5343-5354.
30. Gavalas, A., Davenne, M., Lumsden, A., Chambon, P. and Rijli, F. (1997). Role of Hoxa-2 in axon pathfinding and rostral hindbrain patterning. Development 124, 3693-3702.
31. Gavalas, A., Studer, M., Lumsden, A., Rijli, E., Krumlauf, R. and Chambon, P. (1998). Hoxa1 and Hoxb1 synergize in patterning the hindbrain, cranial nerves and second pharyngeal arch. Development 125, 1123-1136.
32. Gendron-Maguire, M., Mallo, M., Zhang, M. and Gridley, T. (1993). Hoxa2 mutant mice exhibit homeotic transformation of skeletal elements derived from cranial neural crest. Cell 75, 1317-1331.
33. Goddard, J., Rossel, M., Manley, N. and Capecchi, M. (1996). Mice with targeted disruption of Hoxb1 fail to form the motor nucleus of the VIIth nerve. Development 122, 3217-3228.
34. Gould, A., Morrison, A., Sproat, G., White, R. and Krumlauf, R. (1997). Positive cross-regulation and enhancer sharing: two mechanisms for specifying overlapping Hox expression patterns. Genes Dev. 11, 900-913.
35. Graham, A., Maden, M. and Krumlauf, R. (1991). The murine Hox-2 genes display dynamic dorsoventral patterns of expression during central nervous system development. Development 112, 255-264.
36. Helmbacher, F., Pujades, C., Desmarquet, C., Frain, M., Rijli, F., Chambon, P. and Charnay, P. (1998). Hoxa1 and Krox20 synergize to control the development of rhombomere 3. Development 125, 4739-4748.
37. Jacob, J. and Guthrie, S. (2000). Facial visceral motor neurons display specific rhombomere origin and axon pathfinding behavior in the chick. J. Neurosci. 20, 7664-7671.
38. Jacob, J., Tiveron, M. C., Brunet, J. F. and Guthrie, S. (2000). Role of the target in the pathfinding of facial visceral motor axons. Mol. Cell. Neurosci. 16, 14-26.
39. Jessell, T. M. (2000). Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat. Rev. Genet. 1, 20-29.
40. Jessen, J. R., Topczewski, J., Bingham, S., Sepich, D. S., Marlow, F., Chandrasekhar, A. and Solnica-Krezel, L. (2002). Zebrafish trilobite identifies new roles for Strabismus in gastrulation and neuronal movements. Nat. Cell Biol. 4, 610-615.
41. Jungbluth, S., Bell, E. and Lumsden, A. (1999). Specification of distinct motor neuron identities by the singular activities of individual Hox genes. Development 126, 2751-2758.
42. Karlsson, O., Thor, S., Norberg, T., Ohlsson, H. and Edlund, T. (1990). Insulin gene enhancer binding protein Isl-1 is a member of a novel class of proteins containing both a homeo- and a Cys-His domain. Nature 344, 879-882.
43. Korematsu, K. and Redies, C. (1997). Restricted expression of cadherin-8 in segmental and functional subdivisions of the embryonic mouse brain. Dev. Dyn. 208, 178-189.
44. Kusumi, K., Dunwoodie, S. L. and Krumlauf, R. (2001). Dynamic expression patterns of the pudgy/spondylocostal dysostosis gene Dll3 in the developing nervous system. Mech. Dev. 100, 141-144.
45. Lee, K. and Jessell, T. (1999). The specification of dorsal cell fates in the vertebrate central nervous system. Annu. Rev. Neurosci. 22, 261-294.
46. Liem, K. F., Jr, Tremml, G. and Jessell, T. M. (1997). A role for the roof plate and its resident TGFbeta-related proteins in neuronal patterning in the dorsal spinal cord. Cell 91, 127-138.
47. Lumsden, A. and Keynes, R. (1989). Segmental patterns of neuronal development in the chick hindbrain. Nature 337, 424-428.
48. Lumsden, A. and Krumlauf, R. (1996). Patterning the vertebrate neuraxis. Science 274, 1109-1115.
49. Maconochie, M., Nonchev, S., Studer, M., Chan, S.-K., Pöpperl, H., Sham, M.-H., Mann, R. and Krumlauf, R. (1997). Cross-regulation in the mouse HoxB complex: the expression of Hoxb2 in rhombomere 4 is regulated by Hoxb1. Genes Dev. 11, 1885-1896.
50. Maden, M., Graham, A., Gale, E., Rollinson, C. and Zile, M. (1997). Positional apoptosis during vertebrate CNS development in the absence of endogenous retinoids. Development 124, 2799-2805.
51. Maina, F. and Klein, R. (1999). Hepatocyte growth factor, a versatile signal for developing neurons. Nat. Neurosci. 2, 213-217.
52. Manzanares, M., Trainor, P., Nonchev, S., Ariza-McNaughton, L., Brodie, J., Gould, A., Marshall, H., Morrison, A., Kwan, C.-T., Sham, M.-H. et al. (1999). The role of kreisler in segmentation during hindbrain development. Dev. Biol. 211, 220-237.
53. Manzanares, M., Bel-Vialer, S., Ariza-McNaughton, L., Ferretti, E., Marshall, H., Maconochie, M. K., Blasi, F. and Krumlauf, R. (2001). Independent regulation of initiation and maintenance phases of Hoxa3 expression in the vertebrate hindbrain involves auto and cross-regulatory mechanisms. Development 128, 3595-3607.
54. Mark, M., Lufkin, T., Vonesch, J.-L., Ruberte, E., Olivo, J.-C., Dollé, P., Gorry, P., Lumsden, A. and Chambon, P. (1993). Two rhombomeres are altered in Hoxa-1 mutant mice. Development 119, 319-338.
55. Marshall, H., Studer, M., Pöpperl, H., Aparicio, S., Kuroiwa, A., Brenner, S. and Krumlauf, R. (1994). A conserved retinoic acid response element required for early expression of the homeobox gene Hoxb-1. Nature 370, 567-571.
56. Maves, L., Jackman, W. and Kimmel, C. B. (2002). FGF3 and FGF8 mediate a rhombomere 4 signaling activity in the zebrafish hindbrain. Development 129, 3825-3837.
57. McKay, I., Lewis, J. and Lumsden, A. (1997). Organization and development of facial motor neurons in the kreisler mutant mouse. Eur J. Neurosci. 9, 1499-1506.
58. Megason, S. G. and McMahon, A. P. (2002). A mitogen gradient of dorsal midline Wnts organizes growth in the CNS. Development 129, 2087-2098.
59. Muroyama, Y., Fujihara, M., Ikeya, M., Kondoh, H. and Takada, S. (2002). Wnt signaling plays an essential role in neuronal specification of the dorsal spinal cord. Genes Dev. 16, 548-553.
60. Murphy, P. and Hill, R. E. (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.
61. Murphy, P., Davidson, D. R. and Hill, R. E. (1989). Segment-specific expression of a homeobox-containing gene in the mouse hindbrain. Nature 341, 156-159.
62. Nardelli, J., Thiesson, D., Fujiwara, Y., Tsai, F. Y. and Orkin, S. H. (1999). Expression and genetic interaction of transcription factors GATA-2 and GATA-3 during development of the mouse central nervous system. Dev. Biol. 210, 305-321.
63. Ohshima, T., Ogawa, M., Takeuchi, K., Takahashi, S., Kulkarni, A. B. and Mikoshiba, K. (2002). Cyclin-dependent kinase 5/p35 contributes synergistically with Reelin/Dab1 to the positioning of facial branchiomotor and inferior olive neurons in the developing mouse hindbrain. J. Neurosci. 22, 4036-4044.
64. Oppenheim, R. W. (1996). Neurotrophic survival molecules for motoneurons: an embarrassment of riches. Neuron 17, 195-197.
65. 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.
66. Pata, I., Studer, M., van Doorninck, J. H., Briscoe, J., Kuuse, S., Engel, J. D., Grosveld, F. and Karis, A. (1999). The transcription factor GATA3 is a downstream effector of Hoxb1 specification in rhombomere 4. Development 126, 5523-5531.
67. 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.
68. Pattyn, A., Hirsch, M., Goridis, C. and Brunet, J. F. (2000). Control of hindbrain motor neuron differentiation by the homeobox gene Phox2b. Development 127, 1349-1358.
69. Pettmann, B. and Henderson, C. E. (1998). Neuronal cell death. Neuron 20, 633-647.
70. Pierani, A., Brenner-Morton, S., Chiang, C. and Jessell, T. (1999). A sonic hedgehog-independent, retinoid activated pathway of neurogenesis in the ventral spinal cord. Cell 97, 903-915.
71. Pöpperl, H., Bienz, M., Studer, M., Chan, S., Aparicio, S., Brenner, S., Mann, R. and Krumlauf, R. (1995). Segmental expression of Hoxb1 is controlled by a highly conserved autoregulatory loop dependent upon exd/Pbx. Cell 81, 1031-1042.
72. 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.
73. 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.
74. Sharma, K., Sheng, H. Z., Lettieri, K., Li, H., Karavanov, A., Potter, S., Westphal, H. and Pfaff, S. L. (1998). LIM homeodomain factors Lhx3 and Lhx4 assign subtype identities for motor neurons. Cell 95, 817-828.
75. 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.
76. Studer, M. (2001). Initiation of facial motoneurone migration is dependent on rhombomeres 5 and 6. Development 128, 3707-3716.
77. 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, 630-635.
78. Studer, M., Gavalas, A., Marshall, H., Ariza-McNaughton, L., Rijli, F., Chambon, P. and Krumlauf, R. (1998). Genetic interaction between Hoxa1 and Hoxb1 reveal new roles in regulation of early hindbrain patterning. Development 125, 1025-1036.
79. Takahashi, M. and Osumi, N. (2002). Pax6 regulates specification of ventral neurone subtypes in the hindbrain by establishing progenitor domains. Development 129, 1327-1338.
80. 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.
81. Takeichi, M., Uemura, T., Iwai, Y., Uchida, N., Inoue, T., Tanaka, T. and Suzuki, S. C. (1997). Cadherins in brain patterning and neural network formation. Cold Spring Harb. Symp. Quant. Biol. 62, 505-510.
82. Tanabe, Y. and Jessell, T. (1997). Diversity and patterning inthe developing spinal cord. Science 274, 1115-1123.
83. Trainor, P. and Krumlauf, R. (2000). Patterning the cranial neural crest: Hindbrain segmentation and Hox gene plasticity. Nat. Rev. Neurosci. 1, 116-124.
84. Tsuchida, T., Ensini, M., Morton, S. B., Baldassare, M., Edlund, T., Jessell, T. M. and Pfaff, S. L. (1994). Topographic organization of embryonic motor neurons defined by expression of LIM homeobox genes. Cell 79, 957-970.
85. Varela-Echavarria, A., Pfaff, S. L. and Guthrie, S. (1996). Differential expression of LIM homeobox genes among motor neuron subpopulations in the developing chick brain stem. Mol. Cell. Neurosci. 8, 242-257.
86. Vesque, C., Maconochie, M., Nonchev, S., Ariza-McNaughton, L., Kuroiwa, A., Charnay, P. and Krumlauf, R. (1996). Hoxb-2 transcriptional activation by Krox-20 in vertebrate hindbrain requires an evolutionary conserved cis-acting element in addition to the Krox-20 site. EMBO J. 15, 5383-5896.
87. Walshe, J., Maroon, H., McGonnell, I. M., Dickson, C. and Mason, I. (2002). Establishment of hindbrain segmental identity requires signaling by FGF3 and FGF8. Curr. Biol. 12, 1117-1123.
88. Wilkinson, D. G., Bhatt, S., Cook, M., Boncinelli, E. and Krumlauf, R. (1989). Segmental expression of Hox-2 homeobox-containing genes in the developing mouse hindbrain. Nature 341, 405-409.
89. Zhou, Y., Yamamoto, M. and Engel, J. D. (2000). GATA2 is required for the generation of V2 interneurons. Development 127, 3829-3838.