Initiating Hox gene expression: In the early chick neural tube differential sensitivity to FGF and RA signaling subdivides the HoxB genes in two distinct groups

Development

Volumn 129, Issue 22, 2002, Pages 5103-5115

  Bel Vialar, Sophie ^a,c   Itasaki, Nobue ^a   Krumlauf, Robb ^a,b  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^b STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

^c Centre de Biologie du Developpement Toulouse   (France)

Author keywords

AP patterning; Caudal; Cdx; Chick development; Electroporation; FGF signaling; Gene regulation; Hox genes; Nueural development; Retinoids

Indexed keywords

FIBROBLAST GROWTH FACTOR; HOX PROTEIN; RETINOIC ACID; RETINOIC ACID RECEPTOR; TRANSCRIPTION FACTOR;

ANIMAL CELL; CHICKEN; CONTROLLED STUDY; ELECTROPORATION; EMBRYO; EMBRYO DEVELOPMENT; GENE ACTIVATION; GENE EXPRESSION REGULATION; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL TUBE; NONHUMAN; PRIORITY JOURNAL; REVIEW; RHOMBENCEPHALON; SENSITIVITY ANALYSIS;

ANIMALS; AVIAN PROTEINS; CENTRAL NERVOUS SYSTEM; CHICK EMBRYO; FIBROBLAST GROWTH FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; MESODERM; MULTIGENE FAMILY; NEURAL CREST; RHOMBENCEPHALON; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRETINOIN; XENOPUS PROTEINS;

ANIMALIA; GALLUS GALLUS;

EID: 0036862406     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (100)

1. Affolter, M. and Mann, R. (2001). Development. Legs, eyes, or wings - selectors and signals make the difference. Science 292, 1080-1081.
2. Allan, D., Houle, M., Bouchard, N., Meyer, B. I., Gruss, P. and Lohnes, D. (2001). RARgamma and Cdx1 interactions in vertebral patterning. Dev. Biol. 240, 46-60.
3. Amaya, E., Musci, T. J. and Kirschner, M. W. (1991). Expression of a dominant negative mutant of the FGF receptor disrupts mesoderm formation in Xenopus embryos. Cell 66, 257-270.
4. Bel, S., Coré, N., Djabali, M., Kieboom, K., van der Lugt, N., Alkema, M. and van Lohuizen, M. (1998). Genetic interactions and dosage effects of Polycomb group genes in mice. Development 125, 3543-3551.
5. Bel-Vialar, S., Core, N., Terranova, R., Goudot, V., Boned, A. and Djabali, M. (2000). Altered retinoic acid sensitivity and temporal expression of Hox genes in polycomb-M33-deficient mice. Dev. Biol. 224, 238-249.
6. Blumberg, B., Bolado, J., Moreno, T., Kintner, C., Evans, R. and Papalopulu, N. (1997). An essential role for retinoid signaling in anteroposterior neural patterning. Development 124, 373-379.
7. Charité, J., de Graaff, W., Consten, D., Reijnen, M., Korving, J. and Deschamps, J. (1998). Transducing positional information to the Hox henes: critical interaction of cdx gene products with position-sensitive regulatory elements. Development 125, 4349-4358.
8. Conlon, R. A. (1995). Retinoic acid and pattern formation in vertebrates. Trends Genet. 11, 314-319.
9. Conlon, R. A. and Rossant, J. (1992). Exogenous retinoic acid rapidly induces anterior ectopic expression of murine Hox-2 genes in vivo. Development 116, 357-368.
10. Dollé, P., Izpisùa-Belmonte, J. C., Falkenstein, H., Renucci, A. and Duboule, D. (1989). Co-ordinate expression of the murine Hox-5 complex homeobox-containing genes during limb pattern formation. Nature 342, 767-772.
11. Duboule, D. and Dolle, P. (1989). The structural and functional organization of the murine HOX gene family resembles that of Drosophila homeotic genes. EMBO J. 8, 1497-1505.
12. Dubrulle, J., McGrew, M. J. and Pourquie, O. (2001). FGF signaling controls somite boundary position and regulates segmentation clock control of spatiotemporal Hox gene activation. Cell 106, 219-232.
13. Dupé, V., Davenne, M., Brocard, J., Dollé, P., Mark, M., Dierich, A., Chambon, P. and Rijli, F. (1997). In vivo functional analysis of the Hoxa1 3′ retinoid response element (3′ RARE). Development 124, 399-410.
14. Dupé, V., Ghyselinck, N., Wendling, O., Chambon, P. and Mark, M. (1999). Key roles of retinoic acid receptors alpha and beta in the patterning of the caudal hindbrain, pharyngeal arches and otocyst in the mouse. Development 126, 5051-5059.
15. Ehrman, L. A. and Yutzey, K. E. (2001). Anterior expression of the caudal homologue cCdx-B activates a posterior genetic program in avian embryos. Dev. Dyn. 221, 412-421.
16. 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.
17. Favier, B. and Dolle, P. (1997). Developmental functions of mammalian Hox genes. Mol. Hum. Reprod. 3, 115-131.
18. Featherstone, M. (2002). Coactivators in transcription initiation: here are your orders. Curr. Opin. Genet. Dev. 12, 149-155.
19. Frumkin, A., Haffner, R., Shapira, E., Tarcic, N., Gruenbaum, Y. and Fainsod, A. (1993). The chicken CdxA homeobox gene and axial positioning during gastrulation. Development 118, 553-562.
20. Gale, E., Zile, M. and Maden, M. (1999). Hindbrain respecification in the retinoid-deficient quail. Mech. Dev. 89, 43-54.
21. Gaunt, S. J. (1988). Mouse homeobox gene transcripts occupy different but overlapping domains in embryonic germ layers and organs: a comparison of Hox-3.1 and Hox-1.5. Development 103, 135-144.
22. Gaunt, S. J. (2000). Evolutionary shifts of vertebrate structures and Hox expression up and down the axial series of segments: a consideration of possible mechanisms. Int. J. Dev. Biol. 44, 109-117.
23. Gavalas, A. (2002). ArRAnging the hindbrain. Trends Neurosci. 25, 61-64.
24. Gavalas, A. and Krumlauf, R. (2000). Retinoid signaling and hindbrain patterning. Curr. Opin. Genet. Dev. 10, 380-386.
25. Gavalas, A., Trainor, P., Ariza-McNaughton, L. and Krumlauf, R. (2001). Synergy between Hoxa1 and Hoxb1: The relationship between arch patterning and the generation of cranial neural crest. Development 128, 3017-3027.
26. 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.
27. 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.
28. Graham, A., Papalopulu, N. and Krumlauf, R. (1989). The murine and Drosophila homeobox clusters have common features of organization and expression. Cell 57, 367-378.
29. Grieder, N. C., Marty, T., Ryoo, H. D., Mann, R. S. and Affolter, M. (1997). Synergistic activation of a Drosophila enhancer by HOM/EXD and DPP signaling. EMBO J. 16, 7402-7410.
30. Henrique, D., Adam, J., Myat, A., Chitnis, A., Lewis, J. and Ish-Horowicz, D. (1995). Expression of a Delta homologue in prospective neurons in the chick. Nature 375, 787-790.
31. Houle, M., Prinos, P., Iulianella, A., Bouchard, N. and Lohnes, D. (2000). Retinoic acid regulation of Cdx1: an indirect mechanism for retinoids and vertebral specification. Mol. Cell Biol. 20, 6579-6586.
32. Huang, D., Chen, S., Langston, A. and Gudas, L. (1998). A conserved retinoic acid responsive element in the murine Hoxb-1 gene is required for expression in the developing gut. Development 125, 3235-3246.
33. Irving, C. and Mason, I. (2000). Signaling by fgf8 from the isthmus patterns the anterior hindbrain and establishes the anterior limit of Hox gene expression. Development 127, 177-186.
34. Isaacs, H., Pownall, M. and Slack, J. (1998). Regulation of Hox gene expression and posterior development but the Xenopus caudal homolog Xcad3. EMBO J. 17, 3413-3427.
35. 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.
36. Itasaki, N., Bel-Vialar, S. and Krumlauf, R. (1999). "Shocking" developments in chick embryology: electroporation and in ovo gene expression. Nat. Cell Biol. 1, E203-207.
37. Izpisua-Belmonte, J., Falkenstein, H., Dolle, P., Renucci, A. and Duboule, D. (1991a). Murine genes related to the Drosophila AbdB homeotic gene are sequentially expressed during development of the posterior part of the body. EMBO J. 10, 2279-2289.
38. Izpisua-Belmonte, J.-C., Tickle, C., Dolle, P., Wolpert, L. and Duboule, D. (1991b). Expression of homeobox Hox-4 genes and the specification of position in chick wing development. Nature 350, 585-589.
39. Kessel, M. (1992). Respecification of vertebral identities by retinoic acid. Development 115, 487-501.
40. Kessel, M. and Gruss, P. (1991). Homeotic transformations of murine prevertebrae and concomitant alteration of Hox codes induced by retinoic acid. Cell 67, 89-104.
41. Kmita, M., van Der Hoeven, F., Zakany, J., Krumlauf, R. and Duboule, D. (2000). Mechanisms of Hox gene colinearity: transposition of the anterior Hoxb1 gene into the posterior HoxD complex. Genes Dev. 14, 198-211.
42. Kolm, P., Apekin, V. and Sive, H. (1997). Xenopus hindbrain patterning requires retinoid signaling. Dev. Biol. 192, 1-16.
43. Krumlauf, R. (1993). Mouse Hox genetic functions. Curr. Opin. Genet. Dev. 3, 621-625.
44. Krumlauf, R. (1994). Hox genes in vertebrate development. Cell 78, 191-201.
45. Lamb, T. M. and Harland, R. M. (1995). Fibroblast growth factor is a direct neural inducer, which combined with noggin generates anterior-posterior neural pattern. Development 121, 3627-3636.
46. Langston, A., Thompson, J. and Gudas, L. (1997). Retinoic acid-responsive enhancers located 3′ of the HoxA and the HoxB gene clusters. J. Biol. Chem. 272, 2167-2175.
47. Langston, A. W. and Gudas, L. J. (1992). Identification of a retinoic acid responsive enhancer 3′ of the murine homeobox gene Hox-1.6. Mech. Dev. 38, 217-228.
48. Liu, J. P., Laufer, E. and Jessell, T. M. (2001). Assigning the positional identity of spinal motor neurons. rostrocaudal patterning of Hox-c expression by FGFs, Gdf11 and retinoids. Neuron 32, 997-1012.
49. Maconochie, M. K., Nonchev, S., Morrison, A. and Krumlauf, R. (1996). Paralogous Hox genes: Function and regulation. Annu. Rev. Genet. 30, 529-556.
50. Maden, M., Hunt, P., Eriksson, U., Kuroiwa, A., Krumlauf, R. and Summerbell, D. (1991). Retinoic acid-binding protein and homeobox expression in rhombomeres of the chick embryo. Development 111, 35-44.
51. Manzanares, M., Bel-Vialar, S., Ariza-McNaughton, L., Ferreti, E., Marshall, H., Maconochie, M., Blasi, F. and Krumlauf, R. (2001). Independent regulation of initiation and maintenance phases of Hoxa3 expression in the vertebrate hindbrain. Development 128, 3595-3607.
52. Manzanares, M., Wada, H., Itasaki, N., Trainor, P. A., Krumlauf, R. and Holland, P. W. (2000). Conservation and elaboration of Hox gene regulation during evolution of the vertebrate head. Nature 408, 854-857.
53. Marin, F. and Charnay, P. (2000). Hindbrain patterning: FGFs regulate Krox20 and mafB/kr expression in the otic/preotic region. Development 127, 4925-4935.
54. Marom, K., Shapira, E. and Fainsod, A. (1997). The chicken caudal genes establish an anterior-posterior gradient by partially overlapping temporal and spatial patterns of expression. Mech. Dev. 64, 41-52.
55. Marshall, H., Morrison, A., Studer, M., Pöpperl, H. and Krumlauf, R. (1996). Retinoids and Hox genes. FASEB J. 10, 969-978.
56. 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.
57. 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.
58. Mathis, L., Kulesa, P. M. and Fraser, S. E. (2001). FGF receptor signaling is required to maintain neural progenitors during Hensen's node progression. Nat. Cell Biol. 3, 559-566.
59. McGinnis, W. and Krumlauf, R. (1992). Homeobox genes and axial patterning. Cell 68, 283-302.
60. Moens, C. B. and Prince, V. E. (2002). Constructing the hindbrain: Insights from the zebrafish. Dev. Dyn. 224, 1-17.
61. Morales, A. V., de la Rosa, E. J. and de Pablo, E. (1996). Expression of the cCdx-B homeobox gene in chick embryo suggests its participation in rostrocaudal axial patterning. Dev. Dyn. 206, 343-353.
62. Morrison, A., Ariza-McNaughton, L., Gould, A., Featherstone, M. and Krumlauf, R. (1997). HOXD4 and regulation of the group 4 paralog genes. Development 124, 3135-3146.
63. Morrison, A., Chaudhuri, C., Ariza-McNaughton, L., Muchamore, I., Kuroiwa, A. and Krumlauf, R. (1995). Comparative analysis of chicken Hoxb-4 regulation in transgenic mice. Mech. Dev. 53, 47-59.
64. Niederreither, K., Subbarayan, V., Dollé, P. and Chambon, P. (1999). Embryonic retinoic acid synthesis is essential for early mouse post- implantation development. Nature Genet. 21, 444-448.
65. Niederreither, K. V. J., Schuhbaur, B., Chambon, P. and Dolle, P. (2000). Retinoic acid synthesis and hindbrain patterning in the mouse embryo. Development 127, 75-85.
66. Packer, A. I., Crotty, D. A., Elwell, V. A. and Wolgemuth, D. J. (1998). Expression of the murine Hoxa4 gene requires both autoregulation and a conserved retinoic acid response element. Development 125, 1991-1998.
67. Partanen, J., Schwartz, L. and Rossant, J. (1998). Opposite phenotypes of hypomorphic and Y766 phosphorylation site mutations reveal a function for Fgfr1 in anteroposterior patterning of mouse embryos. Genes Dev. 12, 2332-2344.
68. 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.
69. Pownall, M., Tucker, A., Slack, J. and Isaacs, H. (1996). eFGF, Xcad3 and Hox genes form a molecular pathway that establishes the anteroposterior axis in Xenopus. Development 122, 3881-3892.
70. Prinos, P., Joseph, S., Oh, K., Meyer, B. I., Gruss, P. and Lohnes, D. (2001). Multiple pathways governing Cdx1 expression during murine development. Dev. Biol. 239, 257-269.
71. Ryoo, H., Marty, T., Casares, F., Affolter, M. and Mann, R. (1999). Regulation of Hox target genes by a DNA bound Homothorax/Hox/Extradenticle complex. Development 126, 5137-5148.
72. Saleh, M., Rambaldi, I., Yang, X. J. and Featherstone, M. S. (2000). Cell signaling switches HOX-PBX complexes from repressors to activators of transcription mediated by histone deacetylases and histone acetyltransferases. Mol. Cell Biol. 20, 8623-8633.
73. Sharpe, J., Nonchev, S., Gould, A., Whiting, J. and Krumlauf, R. (1998). Selectivity, sharing and competitive interactions in the regulation of Hoxb genes. EMBO J. 17, 1788-1798.
74. Simeone, A., Avantaggiato, V., Moroni, M. C., Mavilio, F., Arra, C., Cotelli, F., Nigro, V. and Acampora, D. (1995). Retinoic acid induces stage-specific antero-posterior transformation of rostral central nervous system. Mech. Dev. 51, 83-98.
75. Slack, J. M. W. and Tannahill, D. (1992). Mechanism of anteroposterior axis specification in vertebrates. Lessons from the amphibians. Development 114, 285-302.
76. Sockanathan, S. and Jessell, T. M. (1998). Motor neuron-derived retinoid signaling specifies the subtype identity of spinal motor neurons. Cell 94, 503-514.
77. Storey, K. G., Goriely, A., Sargent, C. M., Brown, J. M., Burns, H. D., Abud, H. M. and Heath, J. K. (1998). Early posterior neural tissue is induced by FGF in the chick embryo. Development 125, 473-484.
78. Streit, A., Berliner, A. J., Papanayotou, C., Sirulnik, A. and Stern, C. D. (2000). Initiation of neural induction by FGF signaling before gastrulation. Nature 406, 74-78.
79. 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.
80. 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.
81. Studer, M., Pöpperl, H., Marshall, H., Kuroiwa, A. and Krumlauf, R. (1994). Role of a conserved retinoic acid response element in rhombomere restriction of Hoxb-1. Science 265, 1728-1732.
82. Subramanian, V., Meyer, B. I. and Gruss, P. (1995). Disruption of the murine homeobox gene Cdx1 affects axial skeletal identities by altering the mesodermal expression domains of Hox genes. Cell 83, 641-653.
83. Szebenyi, G. and Fallon, J. F. (1999). Fibroblast growth factors as multifunctional signaling factors. Int. Rev. Cytol. 185, 45-106.
84. Taylor, J. K., Levy, T., Suh, E. R. and Traber, P. G. (1997). Activation of enhancer elements by the homeobox gene Cdx2 is cell line specific. Nucl. Acids Res. 25, 2293-2300.
85. Trainor, P., Manzanares, M. and Krumlauf, R. (2000). Genetic interactions during hindbrain segmentation in the mouse embryo. In Results and Problems in Cell Differentiation, vol. 30 (ed. Gogginet and Rackic), pp. 51-89. Berlin-Heidelberg: Springer-Verlag.
86. Trainor, P. A., Ariza-McNaughton, L. and Krumlauf, R. (2002). Role of the isthmus and FGFs in resolving the paradox of neural crest plasticity and prepatterning. Science 295, 1288-1291.
87. van der Hoeven, F, Zákány, J. and Duboule, D. (1996). Gene transpositions in the HoxD complex reveal a hierarchy of regulatory controls. Cell 85, 1025-1035.
88. Vasiliauskas, D. and Stern, C. D. (2001). Patterning the embryonic axis: FGF signaling and how vertebrate embryos measure time. Cell 106, 133-136.
89. 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.
90. Walshe, J. and Mason, I. (2000). Expression of FGFR1, FGFR2 and FGFR3 during early neural development in the chick embryo. Mech. Dev. 90, 103-110.
91. Wedden, S. E., Pang, K. and Eichele, G. (1989). Expression pattern of homeobox-containing genes during chick embryogenesis. Development 105, 639-650.
92. White, J. C., Highland, M., Kaiser, M. and Clagett-Dame, M. (2000). Vitamin A-deficiency in the rat embryo results in anteriorization of the posterior hindbrain, which is prevented by maternal consumption of retinoic acid or retinol. Dev. Biol. 220, 263-284.
93. White, J. C., Shankar, V. N., Highland, M., Epstein, M. L., DeLuca, H. F. and Clagett-Dame, M. (1998). Defects in embryonic hindbrain development and fetal resorption resulting from vitamin A deficiency in the rat are prevented by feeding pharmacological levels of all-trans-retinoic acid. Proc. Natl. Acad. Sci. USA 95, 13459-13464.
94. Whiting, J., Marshall, H., Cook, M., Krumlauf, R., Rigby, P. W. J., Stott, D. and Allemann, R. K. (1991). Multiple spatially specific enhancers are required to reconstruct the pattern of Hox-2.6 gene expression. Genes Dev. 5, 2048-2059.
95. 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.
96. Wilson, S., Rydstrom, A., Trimborn, T., Willert, K., Nusse, R., Jessell, T. M. and Edlund, T. (2001). The status of Wnt signaling regulates neural and epidermal fates in the chick embryo. Nature 411, 325-330.
97. Wilson, S. I, Graziano, E., Harland, R., Jessell, T. M. and Edlund, T. (2000). An early requirement for FGF signaling in the acquisition of neural cell fate in the chick embryo. Curr. Biol. 10, 421-429.
98. Yokouchi, Y., Sasaki, H. and Kuroiwa, A. (1991). Homeobox gene expression correlated with the bifurcation process of limb cartilage development. Nature 353, 443-445.
99. Zakany, J., Kmita, M., Alarcon, P., de la Pompa, J. L. and Duboule, D. (2001). Localized and transient transcription of Hox genes suggests a link between patterning and the segmentation clock. Cell 106, 207-217.
100. Zhang, F., Nagy Kovacs, E. and Featherstone, M. S. (2000). Murine hoxd4 expression in the CNS requires multiple elements including a retinoic acid response element. Mech. Dev. 96, 79-89.