A series of no isthmus (noi) alleles of the zebrafish pax2.1 gene reveals multiple signaling events in development of the midbrain-hindbrain boundary

Development

Volumn 125, Issue 16, 1998, Pages 3049-3062

  Lun, Klaus ^a   Brand, Michael ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Danio rerio; Midbrain hindbrain organizer; Neural patterning; Neurogenesis; no isthmus; Pax genes; Regionalization; Splicing; Zebrafish

Indexed keywords

ALLELE; ALTERNATIVE RNA SPLICING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CONTROLLED STUDY; DEVELOPMENTAL GENETICS; EMBRYO; EMBRYO PATTERN FORMATION; GENE EXPRESSION REGULATION; GENE STRUCTURE; HOMEOBOX; MESENCEPHALON; MUTANT; NEUROECTODERM; NONHUMAN; PRIORITY JOURNAL; RHOMBENCEPHALON; SIGNAL TRANSDUCTION; ZEBRA FISH;

ALLELES; ANIMALS; B-CELL-SPECIFIC ACTIVATOR PROTEIN; BRAIN; CONSERVED SEQUENCE; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENETIC MARKERS; IN SITU HYBRIDIZATION; MUTATION; NUCLEAR PROTEINS; PAIRED BOX TRANSCRIPTION FACTORS; PAX2 TRANSCRIPTION FACTOR; RNA SPLICING; SIGNAL TRANSDUCTION; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; ZEBRAFISH; ZEBRAFISH PROTEINS;

ANIMALIA; DANIO RERIO; VERTEBRATA;

EID: 0031667842     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (75)

1. Acampora, D., Avantaggito, V., Tuorto, F. and Simeone, A. (1997). Genetic control of brain morphogenesis through Otx gene dosage requirement. Development 124, 3639-3650.
2. Adams, B., Dörfler, P., Aguzzi, A., Kozmik, Z., Urbanek, P., Maurer-Fogy, I. and Busslinger, M. (1992). Pax-5 encodes the transcription factor BSAP and is expressed in B lymphocytes, the developing CNS, and adult testis. Genes Dev. 6, 1589-1607.
3. Anderson, K. V., Jürgens, G. and Nüsslein-Volhard, C. (1985) Establishment of dorsal-ventral polarity in the Drosophila embryo: genetic studies on the role of the Toll gene product. Cell 42, 779-789.
4. Ang, S. L. (1996). The brain organization. Nature 380, 25-26.
5. Ang, S. L., Jin, O., Rhinn, M., Daigle, N., Stevenson, L. and Rossant, J. (1996). A targeted mouse Otx2 mutation leads to severe defects in gastrulation and formation of axial mesoderm and to deletion of rostral brain. Development 122, 243-252.
6. Ang, S. L. and Rossant, J. (1993). Anterior mesendoderm induces mouse Engrailed genes in explant cultures. Development 118, 139-149.
7. Asano, M. and Gruss, P. (1992). Pax-5 is expressed at the midbrain-hindbrain boundary during mouse development. Mech. Dev. 39, 29-39.
8. Bally-Cuif, L. and Wassef, M. (1995). Determination events in the nervous system of the vertebrate embryo. Curr. Opin. Genet. Dev. 5, 450-458.
9. Brand, M., Heisenberg, C.-P., Jiang, Y.-J., Beuchle, D., Lun, K., van Eeden, F. J. M., Furutani-Seiki, M., Granato, M., Haffter, P., Hammerschmidt, M., Kane, D. A., Kelsh, R. N., Mullins, M. C., Odenthal, J. and Nüsslein-Volhard, C. (1996). Mutations in zebrafish genes affecting the formation of the boundary between midbrain and hindbrain. Development 123, 179-190.
10. Brown, N. H. and Kafatos, F. C. (1988). Functional cDNA libraries from Drosophila embryos. J. Mol. Biol. 203, 425-437.
11. Butler, A. B. and Hodos, W. (1996). Comparative Vertebrate Neuroanatomy. New York: Wiley-Liss.
12. Crossley, P. H., Martinez, S. and Martin, G. R. (1996). Midbrain development induced by FGF8 in the chick embryo. Nature 380, 66-68.
13. Dahl, E., Koseki, H. and Balling, R. (1997). Pax genes and organogenesis. BioEssays 19, 755-765.
14. Danielian, P. S. and McMahon, A. P. (1996). Engrailed-1 as a target of the Wnt-1 signalling pathway in vertebrate midbrain development. Nature 383, 332-334.
15. DeRobertis, E. M. and Sasai, Y. (1996). A common plan for dorsoventral patterning in Bilateria. Nature 380, 37-40.
16. Dörfler, P. and Busslinger, M. (1996). C-terminal activating and inhibitory domains determine the transactivation potential of BSAP (Pax-5), Pax-2 and Pax-8. EMBO J. 15, 1971-1982.
17. Ekker, M., Wegner, J., Akimenko, M. A. and Westerfield, M. (1992). Coordinate embryonic expression of three zebrafish engrailed genes. Development 116, 1001-1010.
18. Epstein, D. J., Vogan, K. J., Trasler, D. G. and Gruss, P. (1993). A mutation within intron 3 of the Pax-3 gene produces aberrantly spliced mRNA transcripts in the splotch (Sp) mouse mutant. Proc. Nat. Acad. Sci. USA 90, 532-536.
19. 1Neu mutation is identical to a human PAX2 mutation in a family with renal-coloboma syndrome and results in developmental defects of the brain, ear, eye and kidney. Proc. Nat. Acad. Sci. USA 93, 13870-13875.
20. Fürthauer, M., Thisse, C. and Thisse, B. (1997). A role for Fgf-8 in the dorsoventral patterning of the zebrafish gastrula. Development 124, 4253-4264.
21. Hanson, I. M., Fletcher, J. M., Jordan, T., Brown, A., Taylor, D., Adams, R. J., Punnet, H. H. and van Heyningen, V. (1994). Mutations at the PAX6 Locus are found in heterogenous anterior segment malformations including Peters' anomaly. Nat. Genet. 6, 168-173.
22. Hatta, K., Bremiller, R., Westerfield, M. and Kimmel, C. B. (1991) Diversity of expression of engrailed-like antigens in zebrafish. Development 112, 821-832.
23. Heller, N. and Brändli, A. (1997). Xenopus Pax-2 displays multiple splice forms during embryogenesis and pronephric kidney development. Mech. Dev. 69, 83-104.
24. Joyner, A. L. (1996). Engrailed, Wnt and Pax genes regulate midbrain-hindbrain development. Trends Genet. 12, 15-20.
25. Kelly, G. M. and Moon, R. T. (1995). Involvement of wnt1 and pax2 in the formation of the midbrain-hindbrain boundary in the zebrafish gastrula. Dev. Genet. 17, 129-140.
26. 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.
27. Köster, R., Stick, R., Loosli, F. and Wittbrodt, J. (1997). Medaka spalt acts as a target gene of hedgehog signaling. Development 124, 3147-3156.
28. Kozmik, Z., Wang, S., Dörfler, P., Adams, B. and Busslinger, M. (1992) The promoter of the CD19 gene is a target for the B-cell-specific transcription factor BSAP. Mol. Cell Biol. 12, 2662-2672.
29. Krauss, S., Johansen, T., Korzh, V. and Fjose, A. (1991). Expression of the zebrafish paired box gene pax[zf-b] during early neurogenesis. Development 113, 1193-1206.
30. Lee, S. M., Danielian, P. S., Fritzsch, B. and McMahon, A. P. (1997) Evidence that FGF8 signalling from the midbrain-hindbrain junction regulates growth and polarity in the developing midbrain. Development 124, 959-969.
31. Lumsden, A. and Krumlauf, R. (1996). Patterning the vertebrate neuraxis. Science 274, 1109-1115.
32. Macdonald, R., Barth, K. A., Xu, Q., Holder, N., Mikkola, I. and Wilson, S. W. (1995). Midline signalling is required for Pax gene regulation and patterning of the eyes. Development 121, 3267-3278.
33. Macdonald, R., Scholes, J., Strähle, U., Brennan, C., Holder, N., Brand, M. and Wilson, S. W. (1997). The Pax protein Noi is required for commissural axon pathway formation in the rostral forebrain. Development 124, 2397-2408.
34. Marin, F. and Puelles, L. (1994). Patterning of the embryonic avian midbrain after experimental inversions: a polarizing activity from the isthmus. Dev. Biol. 163, 19-37.
35. Martinez, S., Wassef, M. and Alvarado-Mallart, R. M. (1991). Induction of a mesencephalic phenotype in the 2-day-old chick prosencephalon is preceded by the early expression of the homeobox gene en. Neuron 6, 971-981.
36. Martinez-Arias, A. (1993). Development and patterning of the larval epidermis of Drosophila. In The Development of Drosophila melanogaster (ed. M. Bate and A. Martinez-Arias), pp. 517-608. Cold Spring Harbour: Cold Spring Harbour Press.
37. - mice results from stepwise deletion of engrailed-expressing cells by 9. 5 days postcoitum. Cell 69, 581-595.
38. Meyers, E. N., Lewandoski, M. and Martin, G. R. (1998). An Fgf8 mutant allelic series generated by Cre- and Flp-mediated recombination. Nat. Genet. 18, 136-142.
39. Millen, K. J., Wurst, W., Herrup, K. and Joyner, A. (1994). Abnormal embryonic cerebellar development and patterning of postnatal foliation in two mouse Engrailed-2 mutants. Development 120, 695-706.
40. Millet, S. and Alvarado Mallart, R. M. (1995). Expression of the homeobox-containing gene En-2 during the development of the chick central nervous system. Eur. J. Neurosci. 7, 777-791.
41. Miyagawa, T., Amanuma, H., Kuroiwa, A. and Takeda, H. (1996). Specification of posterior midbrain region in zebrafish neuroepithelium. Genes to Cells 1, 369-377.
42. Molven, A., Njolstad, P. R. and Fjose, A. (1991). Genomic structure and restricted neural expression of the zebrafish wnt-1 (int-1) gene. EMBO J. 10, 799-807.
43. Müller, M., v. Weizsäcker, E. and Campos-Ortega, J. A. (1996). Transcription of a zebrafish gene of the hairy-Enhancer of split family delineates the midbrain anlage in the neural plate. Dev. Genes Evol. 206, 153-160.
44. Nornes, H. O., Dressler, G. R., Knapik, E. W., Deutsch, U. and Gruss, P. (1990). Spatially and temporally restricted expression of Pax2 during murine neurogenesis. Development 109, 797-809.
45. Nutt, S. L., Morrison, A. M., Dörfler, P., Rolink, A. and Busslinger, M. (1998). Identification of BSAP (Pax-5) target genes in early B-cell development by loss- and gain-of-function experiments. EMBO J. 17, 2319-2333.
46. Padgett, R. A., Grabowski, P. J., Konarska, M. M., Seiler, S. and Sharp, P. A. (1986). Splicing of messenger RNA precursors. Ann. Rev. Biochem. 55, 1119-1150.
47. Pfeffer, P. L., Gerster, T., Lun, K., Brand, M. and Busslinger, M. (1998). Characterization of three novel members of the zebrafish Pax2/5/8 family: dependency of Pax5 and Pax8 expression on the Pax2. 1 (noi) function. Development 125, 3063-3074.
48. Plachov, D., Chowdhury, K., Walther, C., Simon, D., Guenet, J. L. and Gruss, P. (1990). Pax8, a murine paired box gene expressed in the developing excretory system and thyroid gland. Development 110, 643-651.
49. Puelles, L., Marín, F., Martinez-de-la-Torre, M. and Martínez, S. (1996). The midbrain-hindbrain junction: a model system for brain regionalization through morphogenetic neuroepithelial interactions. In Mammalian Development (ed. P. Lonai), pp. 173-197. Harwood.
50. Reifers, F., Böhli, H., Walsh, E. C., Crossley, P. H., Stainier, D. Y. R. and Brand, M. (1998). Fgf8 is mutated in zebrafish acerebellar mutants and is required for maintenance of midbrain-hindbrain boundary development and somitogenesis. Development 125, 2381-2395.
51. Rétaux, S. and Harris, W. A. (1996). Engrailed and retinotectal topography. Trends Genet. 19, 542-546.
52. Rowitch, D. H. and McMahon, A. P. (1995). Pax-2 expression in the murine neural plate precedes and encompasses the expression domains of Wnt-1 and En-1. Mech. Dev. 52, 3-8.
53. Sanyanusin, P., Norrish, J. H., Ward, T. A., Nebel, A., McNoe, L. A. and Eccles, M. R. (1996). Genomic Structure of the Human PAX2 Gene. Genomics 35, 258-261.
54. Sanyanusin, P., Schimmenti, L. A., Noe, L. A., Ward, T. A., Pierpont, M. E. M., Sullivan, M. J., Dobyns, W. B. and Eccles, M. R. (1995). Mutation of the Pax2 gene in a family with optic nerve colobomas, renal abnormalities and vesicouretal reflux. Nat. Genet. 9, 358-363.
55. Schier, A. F., Neuhauss, S. C. F., Harvey, M., Malicki, J., Solnica-Krezel, L., Stainier, D. Y. R., Zwartkruis, F., Abdelilah, S., Stemple, D. L., Rangini, Z., Yang, H. and Driever, W. (1996). Mutations affecting development of the embryonic zebrafish brain. Development 123, 165-178.
56. Schwarz, M., Alvarez-Bolado, G., Urbanek, P., Busslinger, M. and Gruss, P. (1997). Conserved biological function between Pax-2 and Pax-5 in midbrain and cerebellum development: Evidence from targeted mutations. Proc. Nat. Acad. Sci. USA 94, 14518-14523.
57. Shimamura, K. and Rubenstein, J. L. (1997). Inductive interactions direct early regionalization of the mouse forebrain. Development 124, 2709-2718.
58. 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.
59. Song, D. L., Chalepakis, G., Gruss, P. and Joyner, A. L. (1996). Two Pax-binding sites are required for early embryonic brain expression of an Engrailed-2 transgene. Development 122, 627-635.
60. Takada, S., Stark, K. L., Shea, M. J., Vassileva, G., McMahon, J. A. and McMahon, A. P. (1994). Wnt-3a regulates somite and tailbud formation in the mouse embryo. Genes Dev. 8, 174-189.
61. Tanabe, Y. and Jessel, T. M. (1996). Diversity and pattern in the developing spinal cord. Science 274, 1115-1123.
62. Tassabehji, M., Read, A. P., Newton, V. E., Harris, R., Balling, R., Gruss, P. and Strachan, T. (1992). Waardenburg's syndrome patients have mutations in the human homologue of the Pax-3 paired box gene. Nature 355, 635-636.
63. Tassabehji, M., Read, A. P., Newton, V. E., Patton, M., Gruss, P., Harris, R. and Strachan, T. (1993). Mutations in the PAX3 gene causing Waardenburg syndrome type 1 and type 2. Nat. Genet. 3, 26-30.
64. Tavassoli, K., Rüger, W. and Horst, J. (1997). Alternative splicing in PAX2 generates a new reading frame and an extended conserved coding region at the carboxy terminus. Hum. Genet. 101, 371-375.
65. Torres, M., Gómez-Pardo, E., Dressler, G. R. and Gruss, P. (1995). Pax2 controls multiple steps of urogenital development. Development 121, 4057-4065.
66. Treisman, R., Orkin, S. H. and Maniatis, T. (1983). Structural and functional defects in beta thalassemia. Prog. Clin. Biol. Res. 134, 99-121.
67. Urbanek, P., Fetka, I., Meisler, M. H. and Busslinger, M. (1997). Cooperation of Pax2 and Pax5 in midbrain and cerebellum development. Proc. Nat. Acad. Sci. USA 94, 5703-5703.
68. Urbanek, P., Wang, Z. Q., Fetka, I., Wagner, E. F. and Busslinger, M. (1994). Complete block of early B cell differentiation and altered patterning of the posterior midbrain in mice lacking Pax5/BSAP. Cell 79, 901-912.
69. Wada, H., Saiga, H., Satoh, N. and Holland, P. W. H. (1998). Tripartite organization of the ancestral chordate brain and the antiquity of placodes: insights from ascidian Pax-2/5/8, Hox and Otx genes. Development 125, 1113-1122.
70. Wassarman, K. M., Lewandoski, M., Campbell, K., Joyner, A. L., Rubenstein, J. L., Martinez, S. and Martin, G. R. (1997). Specification of the anterior hindbrain and establishment of a normal mid/hindbrain organizer is dependent on Gbx2 gene function. Development 124, 2923-2934.
71. Wehr, R. and Gruss, P. (1996). Pax and vertebrate development. Int. J. Dev. Biol. 40, 369-377.
72. Westerfield, M. (1994). The Zebrafish Book. Edition 2.1, Oregon: University of Oregon Press.
73. Woo, K. and Fraser, S. E. (1997). Specification of the zebrafish nervous system by nonaxial signals. Science 277, 254-257.
74. Wurst, W., Auerbach, A. B. and Joyner, A. L. (1994). Multiple developmental defects in Engrailed-1 mutant mice: an early mid-hindbrain deletion and patterning defects in forelimbs and sternum. Development 120, 2065-2075.
75. Xu, W., Rould, M. A., Jun, S., Desplan, C. and Pabo, C. O. (1995). Crystal structure of a paired domain-DNA complex at 2. 5 A resolution reveals structural basis for Pax developmental mutations. Cell 80, 639-650.