The zebrafish Iroquois gene iro7 positions the r4/r5 boundary and controls neurogenesis in the rostral hindbrain

Development

Volumn 131, Issue 13, 2004, Pages 3121-3131

  Lecaudey, Virginie ^a,b   Anselme, Isabelle ^a,b   Rosa, Frédéric ^a   Schneider Maunoury, Sylvie ^a,b  

^a ECOLE NORMALE SUPÉRIEURE   (France)

^b SORBONNE UNIVERSITÉ   (France)

Author keywords

Boundary; Hindbrain; Iro7; Iroquois; Neurogenesis; Rhombomere; vhnf1(tcf2)

Indexed keywords

HOMEODOMAIN PROTEIN; TRANSCRIPTION FACTOR; ZEBRAFISH PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CONTROLLED STUDY; EMBRYO; GASTRULATION; GENE ACTIVATION; GENE EXPRESSION REGULATION; MESENCEPHALON; MORPHOGENESIS; NERVOUS SYSTEM DEVELOPMENT; NEUROECTODERM; NEUROMERE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REGULATORY MECHANISM; RHOMBENCEPHALON; TISSUE DISTRIBUTION; ZEBRA FISH;

ANIMALS; DNA, COMPLEMENTARY; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE LIBRARY; HEPATOCYTE NUCLEAR FACTOR 1-BETA; HOMEODOMAIN PROTEINS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; NEURONS; PROTEIN BIOSYNTHESIS; RHOMBENCEPHALON; RNA; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; ZEBRAFISH; ZEBRAFISH PROTEINS;

ANIMALIA; DANIO RERIO;

EID: 4043080500     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.01190     Document Type: Article

References (78)

1. Araki, I. and Nakamura, H. (1999). Engrailed defines the position of dorsal di-mesencephalic boundary by repressing diencephalic fate. Development 126, 5127-5135.
2. Bell, E., Wingate, R. J. and Lumsden, A. (1999). Homeotic transformation of rhombomere identity after localized Hoxb1 misexpression. Science 284, 2168-2171.
3. Bellefroid, E. J., Kobbe, A., Gruss, P., Pieler, T., Gurdon, J. B. and Papalopulu, N. (1998). Xiro3 encodes a Xenopus homolog of the Drosophila Iroquois genes and functions in neural specification. EMBO J. 17, 191-203.
4. Bosse, A., Zulch, A., Becker, M. B., Torres, M., Gomez-Skarmeta, J. L., Modolell, J. and Gruss, P. (1997). Identification of the vertebrate Iroquois homeobox gene family with overlapping expression during early development of the nervous system. Mech. Dev. 69, 169-181.
5. Burglin, T. R. (1997). Analysis of TALE superclass homeobox genes (MEIS, PBC, KNOX, Iroquois, TGIF) reveals a novel domain conserved between plants and animals. Nucleic Acids Res. 25, 4173-4180.
6. Calleja, M., Renaud, O., Usui, K., Pistillo, D., Morata, G. and Simpson, P. (2002). How to pattern an epithelium: lessons from achaete-scute regulation on the notum of Drosophila. Gene 292, 1-12.
7. Cavodeassi, F., Diez del Corral, R., Campuzano, S. and Dominguez, M. (1999). Compartments and organising boundaries in the Drosophila eye: the role of the homeodomain Iroquois proteins. Development 126, 4933-4942.
8. Cavodeassi, F., Modolell, J. and Campuzano, S. (2000). The Iroquois homeobox genes function as dorsal selectors in the Drosophila head. Development 127, 1921-1929.
9. Cavodeassi, F., Modolell, J. and Gomez-Skarmeta, J. L. (2001). The Iroquois family of genes: from body building to neural patterning. Development 128, 2847-2855.
10. Chandrasekhar, A., Moens, C. B., Warren, J. T., Jr, Kimmel, C. B. and Kuwada, J. Y. (1997). Development of branchiomotor neurons in zebrafish. Development 124, 2633-2644.
11. Choe, S. K., Vlachakis, N. and Sagerstrom, C. G. (2002). Meis family proteins are required for hindbrain development in the zebrafish. Development 129, 585-595.
12. 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.
13. Diez del Corral, R., Aroca, P., Gomez-Skarmeta, J. L., Cavodeassi, F. and Modolell, J. (1999). The Iroquois homeodomain proteins are required to specify body wall identity in Drosophila. Genes Dev. 13, 1754-1761.
14. 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.
15. Ferretti, E., Marshall, H., Popperl, H., Maconochie, M., Krumlauf, R. and Blasi, F. (2000). Segmental expression of Hoxb2 in r4 requires two separate sites that integrate cooperative interactions between Prep1, Pbx and Hox proteins. Development 127, 155-166.
16. Furley, A. J., Morton, S. B., Manalo, D., Karagogeos, D., Dodd, J. and Jessell, T. M. (1990). The axonal glycoprotein TAG-1 is an immunoglobulin superfamily member with neurite outgrowth-promoting activity. Cell 61, 157-170.
17. Furthauer, M., Thisse, C. and Thisse, B. (1997). A role for FGF-8 in the dorsoventral patterning of the zebrafish gastrula. Development 124, 4253-4264.
18. Giudicelli, F., Taillebourg, E., Charnay, P. and Gilardi-Hebenstreit, P. (2001). Krox-20 patterns the hindbrain through both cell-autonomous and non cell-autonomous mechanisms. Genes Dev. 15, 567-580.
19. Giudicelli, F., Gilardi-Hebenstreit, P., Mechta-Grigoriou, F., Poquet, C. and Charnay, P. (2003). Novel activities of Mafb underlie its dual role in hindbrain segmentation and regional specification. Dev. Biol. 253, 150-162.
20. Gomez-Skarmeta, J. L., del Corral, R. D., de la Calle-Mustienes, E., Ferre-Marco, D. and Modolell, J. (1996). Araucan and caupolican, two members of the novel iroquois complex, encode homeoproteins that control proneural and vein-forming genes. Cell 85, 95-105.
21. Gomez-Skarmeta, J. L., Glavic, A., de la Calle-Mustienes, E., Modolell, J. and Mayor, R. (1998). Xiro, a Xenopus homolog of the Drosophila Iroquois complex genes, controls development at the neural plate. EMBO J. 17, 181-190.
22. Gomez-Skarmeta, J. L. and Modolell, J. (2002). Iroquois genes: genomic organization and function in vertebrate neural development. Curr. Opin. Genet. Dev. 12, 403-408.
23. Graham, A. and Lumsden, A. (1996). Interactions between rhombomeres modulate Krox-20 and follistatin expression in the chick embryo hindbrain. Development 122, 473-480.
24. Grillenzoni, N., van Helden, J., Dambly-Chaudiere, C. and Ghysen, A. (1998). The iroquois complex controls the somatotopy of Drosophila notum mechanosensory projections. Development 125, 3563-3569.
25. Guthrie, S. and Lumsden, A. (1991). Formation and regeneration of rhombomere boundaries in the developing chick hindbrain. Development 112, 221-229.
26. Guthrie, S., Prince, V. and Lumsden, A. (1993). Selective dispersal of avian rhombomere cells in orthotopic and heterotopic grafts. Development 118, 527-538.
27. Hanneman, E., Trevarrow, B., Metcalfe, W. K., Kimmel, C. B. and Westerfield, M. (1988). Segmental pattern of development of the hindbrain and spinal cord of the zebrafish embryo. Development 103, 49-58.
28. Hatta, K. (1992). Role of the floor plate in axonal patterning in the zebrafish CNS. Neuron 9, 629-642.
29. Hauptmann, G. and Gerster, T. (1994). Two-color whole-mount in situ hybridization to vertebrate and Drosophila embryos. Trends Genet. 10, 266.
30. Helmbacher, F., Pujades, C., Desmarquet, C., Frain, M., Rijli, E. M., Chambon, P. and Charnay, P. (1998). Hoxal and Krox-20 synergize to control the development of rhombomere 3. Development 125, 4739-4748.
31. Higashijima, S., Hotta, Y. and Okamoto, H. (2000). Visualization of cranial motor neurons in live transgenic zebrafish expressing green fluorescent protein under the control of the islet-1 promoter/enhancer. J. Neurosci. 20, 206-218.
32. Irving, C., Nieto, M. A., DasGupta, 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.
33. Itoh, M., Kudoh, T., Dedekian, M., Kim, C. H. and Chitnis, A. B. (2002). A role for iro1 and iro7 in the establishment of an anteroposterior compartment of the ectoderm adjacent to the midbrain-hindbrain boundary. Development 129, 2317-2327.
34. 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.
35. Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B. and Schilling, T. F. (1995). Stages of embryonic development of the zebrafish. Dev. Dyn. 203, 253-310.
36. Kobayashi, D., Kobayashi, M., Matsumoto, K., Ogura, T., Nakafuku, M. and Shimamura, K. (2002). Early subdivisions in the neural plate define distinct competence for inductive signals. Development 129, 83-93.
37. Krauss, S., Johansen, T., Korzh, V. and Fjose, A. (1991). Expression of the zebrafish paired hox gene pax[zf-b] during early neurogenesis. Development 113, 1193-1206.
38. Krauss, S., Maden, M., Holder, N. and Wilson, S. W. (1992). Zebrafish pax[b] is involved in the formation of the midbrain-hindbrain boundary. Nature 360, 87-89.
39. Kudoh, T., Tsang, M., Hukriede, N. A., Chen, X., Dedekian, M., Clarke, C. J., Kiang, A., Schultz, S., Epstein, J. A., Toyama, R. et al. (2001). A gene expression screen in zebrafish embryogenesis. Genome Res. 11, 1979-1987.
40. Kwak, S. J., Phillips, B. T., Heck, R. and Riley, B. B. (2002). An expanded domain of fgf3 expression in the hindbrain of zebrafish valentino mutants results in mis-patterning of the otic vesicle. Development 129, 5279-5287.
41. Larsen, C. W., Zeltser, L. M. and Lumsden, A. (2001). Boundary formation and compartition in the avian diencephalon. J. Neurosci. 21, 4699-4711.
42. Lecaudey, V., Thisse, C., Thisse, B. and Schneider-Maunoury, S. (2001). Sequence and expression pattern of ziro7, a novel, divergent zebrafish iroquois homeobox gene. Mech. Dev. 109, 383-388.
43. Leger, S. and Brand, M. (2002). Fgf8 and Fgf3 are required for zebrafish ear placode induction, maintenance and inner ear patterning. Mech. Dev. 119, 91-108.
44. Leyns, L., Gomez-Skarmeta, J. L. and Dambly-Chaudiere, C. (1996). iroquois: a prepattern gene that controls the formation of bristles on the thorax of Drosophila. Mech. Dev. 59, 63-72.
45. Lumsden, A. and Krumlauf, R. (1996). Patterning the vertebrate neuraxis. Science 274, 1109-1115.
46. Marin, F. and Charnay, P. (2000). Hindbrain patterning: FGFs regulate Krox20 and mafB/kr expression in the otic/preotic region. Development 127, 4925-4935.
47. Maroon, H., Walshe, J., Mahmood, R., Kiefer, P., Dickson, C. and Mason I. (2002). Fgf3 and Fgf8 are required together for formation of the otic placode and vesicle. Development 129, 2099-2108.
48. Matsunaga, E., Araki, I. and Nakamura, H. (2000). Pax6 defines the dimesencephalic boundary by repressing En1 and Pax2. Development 127, 2357-2365.
49. 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.
50. McClintock, J. M., Carlson, R., Mann, D. M. and Prince, V. E. (2001). Consequences of Hox gene duplication in the vertebrates: an investigation of the zebrafish Hox paralogue group 1 genes. Development 128, 2471-2484.
51. McClintock, J. M., Kheirbek, M. A. and Prince, V. E. (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.
52. McNeill, H., Yang, C. H., Brodsky, M., Ungos, J. and Simon, M. A. (1997). mirror encodes a novel PBX-class homeoprotein that functions in the definition of the dorsal-ventral border in the Drosophila eye. Genes Dev. 11, 1073-1082.
53. Metcalfe, W. K., Mendelson, B. and Kimmel, C. B. (1986). Segmental homologies among reticulospinal neurons in the hindbrain of the zebrafish larva. J. Comp. Neurol. 251, 147-159.
54. Moens, C. B., Cordes, S. P., Giorgianni, M. W., Barsh, G. S. and Kimmel, C. B. (1998). Equivalence in the genetic control of hindbrain segmentation in fish and mouse. Development 125, 381-391.
55. Moens, C. B. and Prince, V. E. (2002). Constructing the hindbrain: Insights from the zebrafish. Dev. Dyn. 224, 1-17.
56. Morrison, A. D. (1998). 1 + 1=r4 and much much more. BioEssays 20, 794-797.
57. 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.
58. Nasevicius, A. and Ekker, S. C. (2000). Effective targeted gene 'knockdown' in zebrafish. Nat. Genet. 26, 216-220.
59. Oxtoby, E. and Jowett, T. (1993). Cloning of the zebrafish krox-20 gene (kfx-20) and its expression during hindbrain development. Nucleic Acids Res. 21, 1087-1095.
60. Popperl, H., Rikhof, H., Chang, H., Haffter, P., Kimmel, C. B. and Moens, C. B. (2000). Iazarus is a novel pbx gene that globally mediates hox gene function in zebrafish. Mol. Cell 6, 255-267.
61. Prince, V. E., Moens, C. B., Kimmel, C. B. and Ho, R. K. (1998). Zebrafish hox genes: expression in the hindbrain region of wild-type and mutants of the segmentation gene, valentino. Development 125, 393-406.
62. Rhinn, M. and Brand, M. (2001). The midbrain-hindbrain boundary organizer. Curr. Opin. Neurobiol. 11, 34-42.
63. 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.
64. Rupp, R. A., Snider, L. and Weintraub, H. (1994). Xenopus embryos regulate the nuclear localization of XMyoD. Genes Dev. 8, 1311-1323.
65. Schneider-Maunoury, S., Gilardi-Hebenstreit, P. and Charnay, P. (1998). How to build a vertebrate hindbrain. Lessons from genetics. C. R. Acad. Sci. Iii 321, 819-834.
66. Sun, Z. and Hopkins, N. (2001). vhnf1, the MODY5 and familial GCKD-associated gene, regulates regional specification of the zebrafish gut, pronephros, and hindbrain. Genes Dev. 15, 3217-3229.
67. Torres, M. and Giraldez, F. (1998). The development of the vertebrate inner ear. Mech. Dev. 71, 5-21.
68. Trainor, P. A. and Krumlauf, R. (2000). Patterning the cranial neural crest: hindbrain segmentation and Hox gene plasticity. Nat. Rev. Neurosci. 1, 116-124.
69. Voiculescu, O., Taillebourg, E., Pujades, C., Kress, C., Buart, S., Charnay, P. and Schneider-Maunoury, S. (2001). Hindbrain patterning: Krox20 couples segmentation and specification of regional identity. Development 128, 4967-4978.
70. 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.
71. Westerfield, M. (1994). The Zebrafish Book, 2.1 edn. Eugene, OR: University of Oregon Press.
72. Wiellette, E. L. and Sive, H. (2003). vhnf1 and Fgf signals synergize to specify rhombomere identity in the zebrafish hindbrain. Development 130, 3821-3829.
73. Wilkinson, D. G., Bhatt, S., Chavrier, P., Bravo, R. and Charnay, P. (1989). Segment-specific expression of a zinc-finger gene in the developing nervous system of the mouse. Nature 337, 461-464.
74. Wizenmann, A. and Lumsden, A. (1997). Segregation of rhombomeres by differential chemoaffinity. Mol. Cell Neurosci. 9, 448-459.
75. Wurst, W. and Bally-Cuif, L. (2001). Neural plate patterning: upstream and downstream of the isthmic organizer. Nat. Rev. Neurosci. 2, 99-108.
76. 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.
77. Xu, Q., Mellitzer, G., Robinson, V. and Wilkinson, D. G. (1999). In vivo cell sorting in complementary segmental domains mediated by Eph receptors and ephrins. Nature 399, 267-271.
78. Yang, C. H., Simon, M. A. and McNeill, H. (1999). mirror controls planar polarity and equator formation through repression of fringe expression and through control of cell affinities. Development 126, 5857-5866.