How to build a vertebrate hindbrain. Lessons from genetics

Comptes Rendus de l'Academie des Sciences - Serie III

Volumn 321, Issue 10, 1998, Pages 819-834

  Schneider Maunoury, Sylvie ^a   Gilardi Hebenstreit, Pascale ^a   Charnay, Patrick ^a  

^a ECOLE NORMALE SUPÉRIEURE   (France)

Author keywords

Cell segregation; Gene regulation; Genetic interactions; Hindbrain development; Hox genes; Kreisler; Krox 20; Neurogenesis; Rhombomere

Indexed keywords

ANTERIOR POSTERIOR AXIS; ARTICLE; BRAIN DEVELOPMENT; DEVELOPMENTAL GENETICS; EMBRYO; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; EMBRYO SEGMENTATION; GENE CONTROL; MODEL; MOUSE; NEUROMERE; NONHUMAN; RHOMBENCEPHALON; VERTEBRATE;

VERTEBRATA;

EID: 0345363154     PISSN: 07644469     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0764-4469(99)80022-5     Document Type: Article

References (137)

1. [1] Ingham P.W., The molecular genetics of embryonic pattern formation in Drosophila, Nature 335 (1988) 25-34.
2. [2] Lawrence P.A., Morata G., Homeobox genes: their function in Drosophila segmentation and pattern formation, Cell 78 (1994) 181-189.
3. [3] Lumsden A., Keynes R., Segmental patterns of neuronal development in the chick hindbrain, Nature 337 (1989) 424-428.
4. [4] Clarke J.D., Lumsden A., Segmental repetition of neuronal phenotype sets in the chick embryo hindbrain, Development 118 (1993) 151-162.
5. [5] Marin F., Puelles L., Morphological fate of rhombomeres in quail/ chick chimeras: a segmental analysis of hindbrain nuclei, Eur. J. Neurosci. 7 (1995) 1714-1738.
6. [6] Wingate R.J., Lumsden A., Persistence of rhombomeric organisation in the postsegmental hindbrain, Development 122 (1996) 2143-2152.
7. [7] Le Douarin N., The Neural Crest, Cambridge University Press, Cambridge, 1983.
8. [8] Noden D.M., Interactions and fates of avian craniofacial mesenchyme, Development 103 (1988) 121-140.
9. [9] Lumsden A., Sprawson N., Graham A., Segmental origin and migration of neural crest cells in the hindbrain region of the chick embryo, Development 113 (1991) 1281-1291.
10. [10] Sechrist J., Serbedzija G.N., Scherson T., Fraser S.E., Bronner-Fraser M., Segmental migration of the hindbrain neural crest does not arise from its segmental generation, Development 118 (1993) 691-703.
11. [11] Fraser S., Keynes R., Lumsden A., Segmentation in the chick embryo hindbrain is defined by cell lineage restrictions, Nature 344 (1990) 431-435.
12. [12] Birgbauer E., Fraser S.E., Violation of cell lineage restriction compartments in the chick hindbrain, Development 120 (1994) 1347-1356.
13. [13] Guthrie S., Lumsden A., Formation and regeneration of rhombomere boundaries in the developing chick hindbrain, Development 112 (1991) 221-229.
14. [14] Guthre S., Prince V., Lumsden A., Selective dispersal of avian rhombomere cells in orthotopic and heterotopic grafts, Development 118 (1993) 527-538.
15. [15] Wizermann A., Lumsden A., Segregation of rhombomeres by differential chemoaffinity, Mol. Cell Neurosci. 9 (1997) 448-459.
16. [16] Lumsden A., Krumlauf R., Patterning the vertebrate neuraxis, Science 274 (1996) 1109-1115.
17. [17] Krumlauf R., Hox genes in vertebrate development, Cell 78 (1994) 191-201.
18. [18] Prince V.E., Joly L., Ekker M., Ho R.K., Zebrafish hox genes: genomic organization and modified colinear expression patterns in the trunk, Development 125 (1998) 407-420.
19. [19] Garcia-Fernandez J., Holland P.W., Archetypal organization of the amphioxus Hox gene cluster, Nature 370 (1994) 563-566.
20. [20] Garcia-Fernandez J., Holland P.W., Amphioxus Hox genes: insights into evolut on and development, Int. J. Dev. Biol. 1 (1996) 71S-72S.
21. [21] Duboule D., Morata G., Colinearity and functional hierarchy among genes of the homeotic complexes, Trends Genet. 10 (1994) 358-364.
22. [22] Krumauf R., Marshall H., Studer M., Nonchev S., Sham M.H., Lumsden A., Hox homeobox genes and regionalisation of the nervous system, J. Neurobiol. 24 (1993) 1328-1340.
23. [23] Hunt P., Gulisano M., Cook M., Sham M.H., Faiella A., Wilkinson D., Boncinelli E., Krumlauf R., A distinct Hox code for the branchial region of the vertebrate head, Nature 353 (1991) 861-864.
24. [24] Hunt P., Wilkinson D., Krumlauf R., Patterning the vertebrate head: murine Hox 2 genes mark distinct subpopulations of premigratory and migrating cranial neural crest, Development 112 (1991) 43-50.
25. [25] Hunt P., Krumlauf R., Deciphering the Hox code: clues to patterning branchial regions of the head, Cell 66 (1991) 1075-1078.
26. [26] Hunt P., Whiting J., Muchamore I., Marshall H., Krumlauf R., Homeobox genes and models for patterning the hindbrain and branchial arches, Dev. Suppl. 1 (1991) 187-196.
27. [27] Maconochie M., Nonchev S., Morrison A., Krumlauf R., Paralogous Hox genes: function and regulation, Annu. Rev. Genet. 30 (1996) 529-556.
28. [28] Goddard J.M., Rossel M., Manley N.R., Capecchi M.R., Mice with targeted disruption of Hoxb-1 fail to form the motor nucleus of the VIIth nerve, Development 122 (1996) 3217-3228.
29. [29] Studer M., Lumsden A., Ariza-McNaughton L., Bradley A., Krumlauf R., Altered segmental identity and abnormal migration of motor neurons in mice lacking Hoxb-1, Nature 384 (1996) 630-634.
30. [30] Barrow J.R., Capecchi M.R., Targeted disruption of the Hoxb-2 locus in mice interferes with expression of Hoxb-1 and Hoxb-4, Development 122 (1996) 3817-3828.
31. [31] Gendron-Maguire M., Mallo M., Zhang M., Gridley T., Hoxa-2 mutant mice exhibit homeotic transformation of skeletal elements derived from cranial neural crest, Cell 75 (1993) 1317-1331.
32. [32] Rijli F.M., Mark M., Lakkaraju S., Dierich A., Dolle P., Chambon P., 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 (1993) 1333-1349.
33. [33] Gavalas A., Davenne M., Lumsden A., Chambon P., Rijli F.M., Role of Hoxa-2 in axon pathfinding and rostral hindbrain patterning, Development 124 (1997) 3693-3702.
34. [34] Alexandre D., Clarke J.D., Oxtoby E., Van Y.L., Jowett T., Holder N., Ectopic expression of Hoxa-1 in the zebrafish alters the fate of the mandibular arch neural crest and phenocopies a retinoic acid-induced phenotype, Development 122 (1996) 735-746.
35. [35] Zhang M., Kim H.J., Marshall H., Gendron-Maguire M., Lucas D.A., Baron A., Gudas L.J., Gridley T., Krumlauf R., Grippo J.F., Ectopic Hoxa-1 induces rhombomere transformation in mouse hindbrain, Development 120 (1994) 2431-2442.
36. [36] Carpenter E.M., Goddard J.M., Chisaka O., Manley N.R., Capecchi M.R., Loss of Hox-A1 (Hox-1.6) function results in the reorganization of the murine hindbrain, Development 118 (1993) 1063-1075.
37. [37] Dolle P., Lufkin T., Krumlauf R., Mark M., Duboule D., Chambon P., Local alterations of Krox-20 and Hox gene expression in the hindbrain suggest lack of rhombomeres 4 and 5 in homozygote null Hoxa-1 (Hox-1.6) mutant embryos, Proc. Nat. Acad. Sci. USA 90 (1993) 7666-7670.
38. [38] Mark M., Lufkin T., Vonesch J.L., Ruberte E., Olivo J.C., Dolle P., Gorry P., Lumsden A., Chambon P., Two rhombomeres are altered in Hoxa-1 mutant mice, Development 119 (1993) 319-338.
39. [39] Gavalas A., Studer M., Lumsden A., Rijli P., Chambon R., Hoxa1 and Hoxb1 synergize in patterning the hindbrain, cranial nerves and second pharyngeal arch, Development 125 (1998) 1123-1136.
40. [40] Chisaka O., Capecchi M.R., Regionally restricted developmental defects resulting from targeted disruption of the mouse homeobox gene hox-1.5, Nature 350 (1991) 473-479.
41. [41] Manley N.R., Capecchi M.R., The role of Hoxa-3 in mouse thymus and thyroid development, Development 121 (1995) 1989-2003.
42. [42] Condie B.G., Capecchi M.R., Mice with targeted disruptions in the paralogous genes hoxa-3 and hoxd-3 reveal synergistic interactions, Nature 370 (1994) 304-307.
43. [43] Davis A.P., Witte D.P., Hsieh-Li H.M., Potter S.S., Capecchi M.R., Absence of radius and ulna in mice lacking hoxa-11 and hoxd-11, Nature 375 (1995) 791-795.
44. [44] Horan G.S., Kovacs E.N., Behringer R.R., Featherstone M.S., Mutations in paralogous Hox genes result in overlapping homeotic transformations of the axial skeleton: evidence for unique and redundant function, Dev. Biol. 169 (1995) 359-372.
45. [45] Horan G.S., Ramirez-Solis R., Featherstone M.S., Wolgemuth D.J., Bradley A., Behringer R.R., Compound mutants for the paralogous hoxa-4, hoxb-4, and hoxd-4 genes show more complete homeotic transformations and a dose-dependent increase in the number of vertebrae transformed, Genes Dev. 9 (1995) 1667-1677.
46. [46] Favier B., Rijli F.M., Fromental-Ramain C., Fraulob V., Chambon P., Dolle P., Functional cooperation between the non-paralogous genes Hoxa-10 and Hoxd-11 in the developing forelimb and axial skeleton, Development 122 (1996) 449-460.
47. [47] Zakany J., Gerard M., Favier B., Potter S.S., Duboule D., Functional equivalence and rescue among group 11 Hox gene products in vertebral patterning, Dev. Biol. 176 (1996) 325-328.
48. [48] Manley N.R., Capecchi M.R., Hox group 3 paralogous genes act synergistically in the formation of somitic and neural crest-derived structures, Dev. Biol. 192 (1997) 274-288.
49. [49] Chavrier P., Vesque C., Galliot B., Vigneron M., Dolle P., Duboule D., Charnay P., The segment-specific gene Krox-20 encodes a transcription factor with binding sites in the promoter region of the Hox-1.4 gene, Embo J. 9 (1990) 1209-1218.
50. [50] Wilkinson D.G., Bhatt S., Chavrier P., Bravo R., Charnay P., Segment-specific expression of a zinc-finger gene in the developing nervous system of the mouse, Nature 337 (1989) 461-464.
51. [51] Schneider-Maunoury S., Topilko P., Seitandou T., Levi G., Cohen-Tannoudji M., Pournin S., Babinet C., Charnay P., Disruption of Krox-20 results in alteration of rhombomeres 3 and 5 in the developing hindbrain, Cell 75 (1993) 1199-1214.
52. [52] Swiatek P.J., Gridley T., Perinatal lethality and defects in hindbrain development in mice homozygous for a targeted mutation of the zinc finger gene Krox20, Genes Dev. 7 (1993) 2071-2084.
53. [53] Schneider-Maunoury S., Seitanidou T., Charnay P., Lumsden A., Segmentai and neuronal architecture of the hindbrain of Krox-20 mouse mutants, Development 124 (1997) 1215-1226.
54. [54] Cordes S.P., Barsh G.S., The mouse segmentation gene kr encodes a novel basic domain-leucine zipper transcription factor, Cell 79 (1994) 1025-1034.
55. [55] Moens C.B., Van Y.L., Appel B., Force A.G., Kimmel C.B., valentino: a zebrafish gene required for normal hindbrain segmentation, Development 122 (1996) 3981-3990.
56. [56] Moens C.B., Cordes S.P., Giorgianni M.W., Barsh G.S., Kimmel C.B., Equivalence in the genetic control of hindbrain segmentation in fish and mouse [In Process Citation], Development 125 (1998) 381-391.
57. [57] Frehman M.A., Martin G.R., Cordes S.P., Halamek L.P., Barsh G.S., Altered rhombomere-specific gene expression and hyoid bone differentiation in the mouse segmentation mutant, kreisler (kr), Development 117 (1993) 925-936.
58. [58] McKay I.J., Muchamore I., Krumlauf R., Maden M., Lumsden A., Lewis J., The kreisler mouse: a hindbrain segmentation mutant that lacks two rhombomeres, Development 120 (1994) 2199-2211.
59. [59] Prince V.E., Moens C.B., Kimmel C.B., Ho R.K., Zebrafish hox genes: expression in the hindbrain region of wild-type and mutants of the segmentation gene, valentino, Development 125 (1998) 393-406.
60. [60] Wassarman K.M., Lewandoski M., Campbell K., Joyner A.L., Rubenstein J.L., Martinez S., Martin G.R., Specification of the anterior hindbrain and establishment of a normal mid/hindbrain organizer is dependent on Gbx2 gene function, Development 124 (1997) 2923-2934.
61. [61] Lufkin T., Dierich A., LeMeur M., Mark M., Chambon P., Disruption of the Hox-1.6 homeobox gene results in defects in a region corresponding to its rostral domain of expression, Cell 66 (1991) 1105-1119.
62. [62] Chisaka O., Musci T.S., Capecchi M.R., Developmental defects of the ear, cranial nerves and hindbrain resulting from targeted disruption of the mouse homeobox gene Hox-1.6, Nature 355 (1992) 516-520.
63. [63] Inoue T., Chisaka O., Matsunami H., Takeichi M., Cadherin-6 express on transiently delineates specific rhombomeres, other neural tube subdivisions, and neural crest subpopulations in mouse embryos, Dev. Biol. 183 (1997) 183-194.
64. [64] Murphy P., Hill R.E., Expression of the mouse labial-like homeobox-containng genes, Hox 2.9 and Hox 1.6, during segmentation of the hindbrain, development 111 (1991) 61-74.
65. [65] Gilardi-Hebenstreit P., Nieto M.A., Frain M., Mattei M.G., Chestier A., Wilkinson D.G., Charnay P., An Eph-related receptor protein tyrosine kinase gene segmentally expressed in the developing mouse hindbrain, Oncogene 7 (1992) 2499-2506.
66. [66] Nieto M.A., Gilardi-Hebenstreit P., Charnay P., Wilkinson D.G., A receptor protein tyrosine kinase implicated in the segmental patterning of the hindbrain and mesoderm, Development 116 (1992) 1137-1150.
67. [67] Xu Q., Alldus G., Holder N., Wilkinson D.G., Expression of truncated Sek-1 receptor tyrosine kinase disrupts the segmental restriction of gene expression in the Xenopus and zebrafish hindbrain, Development 121 (1995) 4005-4016.
68. [68] Smith A., Robinson V., Patel K., Wilkinson D.G., The EphA4 and EphB1 receptor tyrosine kinases and ephrin-B2 ligand regulate targeted migration of branchial neural crest cells, Curr. Biol. 7 (1997) 561-570.
69. [69] Sham M.H., Vesque C., Nonchev S., Marshall H., Frain M., Gupta R.D., Whiting J., Wilkinson D., Charnay P., Krumlauf R., The zinc finger gene Krox20 regulates HoxB2 (Hox2.8) during hindbrain segmentation, Cell 72 (1993) 183-196.
70. [70] Vesque C., Maconochie M., Nonchev S., Ariza-McNaughton L., Kuroiwa A., Charnay P., Krumlauf R., Hoxb-2 transcriptional activation in rhombomeres 3 and 5 requires an evolutionary conserved cis-acting element in addition to the Krox-20 binding site, Embo J. 15 (1996) 5383-5396.
71. [71] Nonchev S., Vesque C., Maconochie M., Seitanidou T., Ariza-McNaughton L., Frain M., Marshall H., Sham M.H., Krumlauf R., Charnay P., Segmental expression of Hoxa-2 in the hindbrain is directly regulated by Krox-20, Development 122 (1996) 543-554.
72. [72] Theil T., Frain M., Gilardi-Hebenstreit P., Flenniken A., Charnay P., Wilkinson D.G., Segmental expression of the EphA4 (Sek-1) receptor tyrosine kinase in the hindbrain is under direct transcriptional control of Krox-20, Development 125 (1998) 443-452.
73. [73] Seitanidou T., Schneider-Maunoury S., Desmarquet C., Wilkinson D.C., Charnay P., Krox-20 is a key regulator of rhombomere-specific gene expression in the developing hindbrain, Mech. Dev. 65 (1997) 31-42.
74. [74] Manzanares M., Cordes S., Kwan C.T., Sham M.H., Barsh G.S., Krumlauf R., Segmental regulation of Hoxb-3 by kreisler, Nature 387 (1997) 191-195.
75. [75] Morriss-Kay G., Retinoic acid and craniofacial development: molecules and morphogenesis, Bioessays 15 (1993) 9-15.
76. [76] Conlon R.A., Retinoic acid and pattern formation in vertebrates, Trends Genet. 11 (1995) 314-319.
77. [77] Morriss-Kay G.M., Murphy P., Hill R.E., Davidson D.R., Effects of retinoic acid excess on expression of Hox-2.9 and Krox-20 and on morphological segmentation in the hindbrain of mouse embryos, Embo J. 10 (1991) 2985-2995.
78. [78] Papalopulu N., Clarke J.D., Bradley L., Wilkinson D., Krumlauf R., Holder N., Retinoic acid causes abnormal development and segmental patterning of the anterior hindbrain in Xenopus embryos, Development 113 (1991) 1145-1158.
79. [79] Conlon R.A., Rossant J., Exogenous retinoic acid rapidly induces anterior ectopic expression of murine Hox-2 genes in vivo, Development 116 (1992) 357-368.
80. [80] Marshall H., Nonchev S., Sham M.H., Muchamore I., Lumsden A., Krumlauf R., Retinoic acid alters hindbrain Hox code and induces transformation of rhombomeres 2/3 into a 4/5 identity, Nature 360 (1992) 737-741.
81. [81] Wood H., Pall G., Morriss-Kay G., Exposure to retinoic acid before or after the onset of somitogenesis reveals separate effects on rhombomeric segmentation and 3′ HoxB gene expression domains, Development 120 (1994) 2279-2285.
82. [82] Hill J., Clarke J.D., Vargesson N., Jowett T., Holder N., Exogenous retinoic acid causes specific alterations in the development of the mid-brain and hindbrain of the zebrafish embryo including positional respecification of the Mauthner neuron, Mech. Dev. 50 (1995) 3-16.
83. [83] Maden M., Gale E., Kostetskii I., Zile M., Vitamin A-deficient quail embryos have half a hindbrain and other neural defects, Curr. Biol. 6 (1996) 417-426.
84. [84] Maden M., Graham A., Gale E., Rollinson C., Zile M., Positional apoptosis during vertebrate CNS development in the absence of endogenous retinoids, Development 124 (1997) 2799-2805.
85. [85] Kolm P.J., Apekin V., Sive H., Xenopus hindbrain patterning requires retinoid signaling, Dev. Biol. 192 (1997) 1-16.
86. [86] van der Wees J., Schilthuis J.G., Koster C.H., Diesveld-Schipper H., Folkers G.E., van der Saag P.T., Dawson M.I., Shudo K., van der Burg B., Durston A.J., Inhibition of retinoic acid receptor-mediated signalling alters positional identity in the developing hindbrain [In Process Citation], Development 125 (1998) 545-556.
87. [87] Simeone A., Acampora D., Arcioni L., Andrews P.W., Boncinelli E., Mavilio F., Sequential activation of HOX2 homeobox genes by retinoic acid in human embryonal carcinoma cells, Nature 346 (1990) 763-766.
88. [88] Papalopulu N., Lovell-Badge R., Krumlauf R., The expression of murine Hox-2 genes is dependent on the differentiation pathway and displays a collinear sensitivity to retinoic acid in F9 cells and Xenopus embryos, Nucleic Acids Res. 19 (1991) 5497-5506.
89. [89] Simeone A., Acampora D., Nigro V., Faiella A., D'Esposito M., Stornaiuolo A., Mavilio F., Boncinelli E., Differential regulation by retinoic acid of the homeobox genes of the four HOX loci in human embryonal carcinoma cells, Mech. Dev. 33 (1991) 215-227.
90. [90] Marshall H., Morrison A., Studer M., Popperl H., Krumlauf R., Retinoids and Hox genes, Faseb J. 10 (1996) 969-978.
91. [91] Marshall H., Studer M., Popperl H., Aparicio S., Kuroiwa A., Brenner S., Krumlauf R., A conserved retinoic acid response element required for early expression of the homeobox gene Hoxb-1, Nature 370 (1994) 567-571.
92. [92] Langston A.W., Gudas L.J., Identification of a retinoic acid responsive enhancer 3′ of the murine homeobox gene Hox-1.6, Mech. Dev. 38 (1992) 217-227.
93. [93] Frasch M., Chen X., Lufkin T., Evolutionary-conserved enhancers direct region-specific expression of the murine Hoxa-1 and Hoxa-2 loci in both mice and Drosophila, Development 121 (1995) 957-974.
94. [94] Dupe V., Davenne M., Brocard J., Dolle P., Mark M., Dierich A., Chambon P., Rijli F.M., In vivo functional analysis of the Hoxa-1 3′ retinoic acid response element (3′RARE), Development 124 (1997) 399-410.
95. [95] Studer M., Popperl H., Marshall H., Kuroiwa A., Krumlauf R., Role of a conserved retinoic acid response element in rhombomere restriction of Hoxb-1, Science 265 (1994) 1728-1732.
96. [96] Popperl H., Bienz M., Studer M., Chan S.K., Aparicio S., Brenner S., Mann R.S., Krumlauf R., Segmental expression of Hoxb-1 is controlled by a highly conserved autoregulatory loop dependent upon exd/pbx, Cell 81 (1995) 1031-1042.
97. [97] Studer M., Cavalas A., Marshall H., Ariza-McNaughton L., Rijli F., Chambon P., Krumlauf R., Genetic interactions between Hoxa1 and Hoxb1 reveal new roles in regulation of early hindbrain patterning, Development 125 (1998) 1025-1036.
98. [98] Maconochie M.K., Nonchev S., Studer M., Chan S.K., Popperl H., Sham M.H., Mann R.S., Krumlauf R., Cross-regulation in the mouse HoxB complex: the expression of Hoxb2 in rhombomere 4 is regulated by Hoxb1, Genes Dev. 11 (1997) 1885-1895.
99. [99] Gould A., Morrison A., Sproat G., White R.A., Krumlauf R., Positive cross-regulation and enhancer sharing: two mechanisms for specifying overlapping Hox expression patterns, Genes Dev. 11 (1997) 900-913.
100. [100] Guthrie S., Muchamore I., Kuroiwa A., Marshall H., Krumlauf R., Lumsden A., Neuroectodermal autonomy of Hox-2.9 expression revealed by rhombomere transpositions, Nature 356 (1992) 157-159.
101. [101] Kuratani S.C., Eichele G., Rhombomere transplantation repatterns the segmental organization of cranial nerves and reveals cell-autonomous expression of a homeodomain protein, Development 117 (1993) 105-117.
102. [102] Grapin-Botton A., Bonnin M.A., McNaughton L.A., Krumlauf R., Le Douarin N.M., Plasticity of transposed rhombomeres: Hox gene induction is correlated with phenotypic modifications, Development 121 (1995) 2707-2721.
103. [103] Itasaki N., Sharpe J., Morrison A., Krumlauf R., Reprogramming Hox expression in the vertebrate hindbrain: influence of paraxial mesoderm and rhombomere transposition, Neuron 16 (1996) 487-500.
104. [104] Grapin-Botton A., Bonnin M.A., Le Douarin N.M., Hox gene induction in the neural tube depends on three parameters: competence, signal supply and paralogue group, Development 124 (1997) 849-859.
105. [105] Grapin-Botton A., Bonnin M.A., Sieweke M., Douarin N., Defined concentrations of a posteriorizing signal are critical for MafB/Kreisler segmentai expression in the hindbrain, Development 125 (1998) 1173-1181.
106. [106] Graham A., Heyman I., Lumsden A., Even-numbered rhombomeres control the apoptotic elimination of neural crest cells from odd-numbered rhombomeres in the chick hindbrain, Development 119 (1993) 233-245.
107. [107] Graham A., Lumsden A., Interactions between rhombomeres modulate Krox-20 and follistatin expression in the chick embryo hindbrain, Development 122 (1996) 473-480.
108. [108] Gilbert S.F., Saxen L., Spemann's organizer: models and molecules, Mech. Dev. 41 (1993) 73-89.
109. [109] McCrew L.L., Lai C.J., Moon R.T., Specification of the anteroposterior neural axis through synergistic interaction of the Wnt signaling cascade with noggin and follistatin, Dev. Biol. 172 (1995) 337-342.
110. [110] McGrew L.L., Hoppler S., Moon R.T., Wnt and FGF pathways cooperatively pattern anteroposterior neural ectoderm in Xenopus [In Process Citation], Mech. Dev. 69 (1997) 105-114.
111. [111] Irving C., Nieto M.A., DasGupta R., Charnay P., Wilkinson D.G., Progressive spatial restriction of Sek-1 and Krox-20 gene expression during hindbrain segmentation, Dev. Biol. 173 (1996) 26-38.
112. [112] Wilkinson D.G., Genetic control of segmentation in the vertebrate hindbrain, Perspect. Dev. Neurobiol. 3 (1995) 29-38.
113. [113] Gurdon J.B., A community effect in animal development, Nature 336 (1988) 772-774.
114. [114] Gale N.W., Flenniken A., Compton D.C., Jenkins N., Copeland N.G., Gilbert D.J., Davis S., Wilkinson D.G., Yancopoulos G.D., Elk-L3, a novel transmembrane ligand for the Eph family of receptor tyrosine kinases, expressed in embryonic floor plate, roof plate and hindbrain segments, Oncogene 13 (1996) 1343-1352.
115. [115] Guthrie S., Butcher M., Lumsden A., Patterns of cell division and interkinetic nuclear migration in the chick embryo hindbrain, J. Neurobiol. 22 (1991) 742-754.
116. [116] Heyman I., Kent A., Lumsden A., Cellular morphology and extracellular space at rhombomere boundaries in the chick embryo hindbrain, Dev. Dyn. 198 (1993) 241-253.
117. [117] Heyman I., Faissner A., Lumsden A., Cell and matrix specialisations of rhombomere boundaries, Dev. Dyn. 204 (1995) 301-315.
118. [118] Martinez S., Marin F., Nieto M.A., Puelles L., Induction of ectopic engrailed expression and fate change in avian rhombomeres: intersegmental boundaries as barriers, Mech. Dev. 51 (1995) 289-303.
119. [119] Lawrence P.A., Struhl, G., Morphogens, compartments and pattern: lessons from Drosophila?, Cell 85 (1996) 951-961.
120. [120] Taneja R., Thisse B., Rijli F.M., Thisse C., Bouillet P., Dolle P., Chambon P., The expression pattern of the mouse receptor tyrosine kinase gene MDK1 is conserved through evolution and requires Hoxa-2 for rhombomere- specific expression in mouse embryos. Dev. Biol. 177 (1996) 397-412.
121. [121] Murphy P., Davidson D.R., Hill R.E., Segment-specific expression of a homoeobox-containing gene in the mouse hindbrain, Nature 341 (1989) 156-159.
122. [122] Wilkinson D.G., Bhatt S., Cook M., Boncinelli E., Krumlauf R., Segmental expression of Hox-2 homoeobox-containing genes in the developing mouse hindbrain, Nature 341 (1989) 405-409.
123. [123] Becker N., Seitanidou T., Murphy P., Mattei M.G., Topilko P., Nieto M.A., Wilkinson D.G., Charnay P., Gilardi-Hebenstreit P., Several receptor tyrosine kinase genes of the Eph family are segmentally expressed in the developing hindbrain, Mech. Dev, 47 (1994) 3-17.
124. [124] Ganju P., Shigemoto K., Brennan J., Entwistle A., Reith A.D., The Eck receptor tyrosine kinase is implicated in pattern formation during gastrulation, hindbrain segmentation and limb development, Oncogene 9 (1994) 1613-1624.
125. [125] Henkemeyer M., Marengere L.E., McGlade J., Olivier J.P., Conlon R.A., Holmyard D.P., Letwin K., Pawson T., Immunolocalization of the Nuk receptor tyrosine kinase suggests roles in segmental patterning of the brain and axonogenesis, Oncogene 9 (1994) 1001-1014.
126. [126] Ruiz J.C., Robertson E.J., The expression of the receptor-protein tyrosine kinase gene, eck, is highly restricted during early mouse development, Mech. Dev. 46 (1994) 87-100.
127. [127] Ellis J., Liu Q., Breitman M., Jenkins N.A., Gilbert D.J., Copeland N.G., Tempest H.V., Warren S., Muir E., Schilling H. et al., Embryo brain kinase: a novel gene of the eph/elk receptor tyrosine kinase family, Mech. Dev. 52 (1995) 319-341.
128. [128] Bergemann A.D., Cheng H.J., Brambilla R., Klein R., Flanagan J.G., ELF-2, a new member of the Eph ligand family, is segmentally expressed in mouse embryos in the region of the hindbrain and newly forming somites, Mol. Cell Biol. 15 (1995) 4921-4929.
129. [129] Flenniken A.M., Gale N.W., Yancopoulos G.D., Wilkinson D.G., Distinct and overlapping expression patterns of ligands for Eph-related receptor tyrosine kinases during mouse embryogenesis, Dev. Biol. 179 (1996) 382-401.
130. [130] Ruberte L., Dolle P., Chambon P., Morriss-Kay G., Retinoic acid receptors and cellular retinoid binding proteins. II. Their differential pattern of transcription during early morphogenesis in mouse embryos, Development 111 (1991) 45-60.
131. [131] Maden M., Horton C., Graham A., Leonard L., Pizzey J., Siegenthaler G., Lumsden A., Eriksson U., Domains of cellular retinoic acid-binding protein 1 (CRABP 1) expression in the hindbrain and neural crest of the mouse embryo, Mech. Dev. 37 (1992) 13-23.
132. [132] Ruberte E., Friederich V., Morriss-Kay G., Chambon P., Differential distribution patterns of CRABP 1 and CRABP 11 transcripts during mouse embryogenesis, Development 115 (1992) 973-987.
133. [133] Wilkinson D.G., Peters G., Dickson C., McMahon A.P., Expression of the FGF-related proto-oncogene int-2 during gastrulation and neurulation in the mouse, Embo J. 7 (1988) 691-695.
134. [134] Albano R.M., Arkell R., Beddington R.S., Smith J.C., Expression of inhibin subunits and follistatin during postimplantation mouse development: decidual expression of activin and expression of follistatin in primitive streak, somites and hindbrain, Development 120 (1994) 803-813.
135. [135] Bouillet P., Oulad-Abdelghani M., Ward S.J., Bronner S., Chambon P., Dolle P., A new mouse member of the Wnt gene family, mWnt-8, is expressed during early embryogenesis and is ectopically induced by retinoic acid, Mech. Dev. 58 (1996) 141-152.
136. [136] Mahmood R., Mason I.J., Morriss-Kay G.M., Expression of Fgf-3 in relation to hindbrain segmentation, otic pit position and pharyngeal arch morphology in normal and retinoic acid-exposed mouse embryos, Anat. Embryol. 194 (1996) 13-22.
137. [137] Committee E.N., Unified nomenclature for EPH family receptors and their ligands, the ephrins, Cell 90 (1997) 403-404.