Vax1 is a novel homeobox-containing gene expressed in the developing anterior ventral forebrain

Development

Volumn 125, Issue 14, 1998, Pages 2599-2610

  Hallonet, Marc ^a   Hollemann, Thomas ^b   Wehr, Roland ^a   Jenkins, Nancy A ^c   Copeland, Neal G ^c   Pieler, Tomas ^b   Gruss, Peter ^a  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

^c NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Anterior neural ridge; Brain patterning; Dlx1; Emx; Forebrain; Ganglionic eminence; Homeobox; Neural differentiation; Not1; Olfactory placode; Pax6; Xenopus

Indexed keywords

ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CHROMOSOME 19; CONTROLLED STUDY; DEVELOPMENTAL GENETICS; EMBRYO; FOREBRAIN; GENE EXPRESSION; GENE MAPPING; GENETIC LINKAGE; HOMEOBOX; HUMAN; MOUSE; MUTANT; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; TISSUE DISTRIBUTION; XENOPUS;

AMINO ACID SEQUENCE; ANIMALS; BRAIN; CELL DIFFERENTIATION; CHROMOSOME MAPPING; CLONING, MOLECULAR; DNA-BINDING PROTEINS; EYE PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, HOMEOBOX; HOMEODOMAIN PROTEINS; IN SITU HYBRIDIZATION; MICE; MOLECULAR SEQUENCE DATA; NEUROPEPTIDES; PAIRED BOX TRANSCRIPTION FACTORS; REPRESSOR PROTEINS; RNA, MESSENGER; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, AMINO ACID; TRANSCRIPTION FACTORS; XENOPUS; XENOPUS PROTEINS;

ANIMALIA; MAMMALIA; VERTEBRATA;

EID: 0031827413     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (87)

1. Acampora, D., Mazan, S., Lallemand, V., Avantaggiato, V., Maury, M., Simeone, A. and Brûlet, P. (1995). Forebrain and midbrain regions are deleted in Otx2(-l-) mutants due to a defective anterior neuroectoderm specification during gastrulation. Development 121, 3279-3290.
2. Anderson, S. A., Eisenstat, D. D., Shi, L. and Rubenstein, J. L. R. (1997a). Interneuron migration from the basal forebrain to neocortex: dependence on Dlx genes. Science 278, 474-476.
3. Anderson, S. A., Mengshen, Q., Bulfone, A., Eisenstat, D. D., Meneses, J., Pedersen, R. and Rubenstein, J. L. R. (1997b). Mutations of the homeobox genes Dlx-1 and Dlx-2 disrupt the striatal subventricular zone and differentiation of late born striatal neurons. Neuron 19, 27-37.
4. Ang, S. L., Conlon, R. A., Jin, O. and Rossant, J. (1994). Positive and negative signals from mesoderm regulate the expression of mouse Otx2 in ectoderm explants. Development 120, 2979-2989.
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. Ariens Kappers, C. U., Huber, G. C. and Crosby, E. C. (1967). The comparative anatomy of the nervous system of vertebrates, including man. New York: Hafner Publishing Company, Inc.
8. Bayer, S. A. and Altman, J. (1987a). Development of the preoptic area: Time and site of origin, migratory routes, and settling patterns of its neurons. J. Comp. Neurol. 265, 65-95.
9. Bayer, S. A. and Altman, J. ( 1987b). Directions in neurogenic gradients and pattern of anatomical connections in the telencephalon. Prog. Neurobiol. 29, 57-106.
10. Bayer, S. A. and Altman, J. (1991). Development of the endopiriform nucleus and the claustrum in the rat brain. Neuroscience 45, 391-412.
11. Boek, R. and Kolakofsky, D. (1994). Position +5 and +6 can be major determinants of the efficiency of non-AUG initiation codons for protein synthesis. EMBO J. 13, 3608-3617.
12. Boulder Commitee (1970). Embryonic Vertebrate Central System: Revised Terminology. Anat. Rec. 166, 257-262.
13. Bouwmeester, T., Kim, S.-H., Sasai, Y., Lu, B. and De Robertis, E. (1996). Cerberus is a head-inducing secreted factor expressed in the anterior endoderm of Spemann's organizer. Nature 382, 595-601.
14. Brunelli, S., Faiella, A., Capra, V., Nigro, V., Simeone, A., Cama, A. and Boncinelli, E. (1996). Germline mutations in the homeobox gene EMX2 in patients with severe schizencephaly. Nat. Genet. 12, 94-6.
15. Bulfone, A., Puelles, L., Porteus, M. H., Frohman, M. A., Martin, G. R. and Rubenstein, J. L. R. (1993). Spatially restricted expression of Dlx-1, Dlx-2 (Tes-1), Gbx-2, and Wnt-3 in the embryonic day 12.5 mouse forebrain defines potential transverse and longitudinal segmental boundaries. J. Neurosci. 13, 3155-3172.
16. Caric, D., Gooday, D., Hill, R. E., McConnell, S. K. and Price, D. J. (1997) Determination of the migratory capacity of embryonic cortical cells lacking the transcription factor Pax-6. Development 124, 5087-5096.
17. Carpenter, M. B. (1991). Core text of neuroanatomy. Baltimore, MD, USA: Williams & Wilkins.
18. Cavener, D. R. and Ray, S. C. (1991). Eukaryotic start and stop translation sites. Nucl. Acids Res. 19, 3185-3192.
19. Copeland, N. G. and Jenkins, A. G. (1991). Development and applications of a molecular genetic linkage map of the mouse genome. Trends Genet. 7, 113-118.
20. Couly, G. F. and Le Douarin, N. M. (1987). Mapping of the early neural primordium in quail-chick chimeras. II. The prosencephalic neural plate and neural folds: implications for the genesis of cephalic human congenital abnormalities. Dev. Biol. 120, 198-214.
21. Dale, J. K., Vesque, C., Lints, T. J., Sampath, T. K., Furley, A., Dodd, J. and Placzek, M, (1997). Cooperation of BMP7 and SHH in the induction of forebrain ventral midline cells by prechordal mesoderm. Cell 90, 257-269.
22. Dalton, D., Chadwick, R. and McGinnis, W. (1989). Expression and embryonic function of empty spiracles: a Drosophila homeobox gene with two patterning functions on the anterior-posterior axis of the embryo. Genes Dev. 3, 1940-1956.
23. De Carlos, J. A., Lopez-Mascaraque, L. and Valverde, F. (1995). The telencephalic vesicles are innervated by olfactory placode-derived cells: a possible mechanism to induce neocortical development. Neuroscience 68, 1167-1178.
24. De Carlos, J. A., Lopez-Mascaraque, L. and Valverde, F. (1996). Dynamics of cell migration from the lateral ganglionic eminence in the rat. J. Neurosci. 16, 6146-6156.
25. Doniach, T. (1993). Planar and vertical induction of anteroposterior pattern during the development of the amphibian central nervous system. J. Neurobiol. 24, 1256-1275.
26. Duboule, D. (1994). Guidebook to the Homeobox Genes. Oxford: Sambrook and Tooze publication at Oxford University Press.
27. Eagleson, G., Ferreiro, B. and Harris, W. A. (1995). Fate of the anterior neural ridge and the morphogenesis of the Xenopus forebrain. J. Neurobiol. 28, 146-158.
28. Eagleson, G. W. and Harris, W. A. (1990). Mapping of the presumptive brain regions in the neural plate of Xenopus laevis. J. Neurobiol. 21, 427-440.
29. Ericson, J., Morton, S., Kawakami, A., Roelink, H. and Jessell, T. M. (1996). Two critical periods of sonic hedgehog signaling required for the specification of motoneuron identity. Cell 87, 661-673.
30. Fentress, J. C., Stanfield, B. B. and Cowan, W. M. (1981). Observations on the development of the striatum in mice and rats. Anat. Embryol. 163, 275-298.
31. Kinkelstein, R. and Boncinelli, E. (1994). From fly head to mammalian forebrain: the story of otd and Otx. Trends Genet. 10, 310-315.
32. Fishell, G. (1997). Regionalization in the mammalian telensephalon. Curr. Opin. Neurobiol. 7, 62-69.
33. Gans, C. (1989). Stages in the origin of vertebrates: analysis by means of scenarios. Biol. Rev. Camb. Philos. Soc. 64, 221-268.
34. Glinka, A., Wei, W., Onichtchouk, D., Blumenstock, C. and Niehrs, C. (1997). Head induction by simultaneous repression of Bmp and Wnt signalling in Xenopus. Nature 389, 517-519.
35. Halliday, A. L. and Cepko, C. L. (1992). Generation and migration of cells in the developing striatum. Neuron 9, 15-26.
36. Hamburger, V. (1988). The Heritage of Experimental Embryology. Hans Spemann and the Organizer. Oxford: Oxford University Press.
37. Harland, R. M. (1991). In situ hybridization: an improved whole-mount method for Xenopus embryos. Methods Cell Biol. 36, 685-695.
38. Hirth, F., Therianos, S., Loop, T., Gehring, W. J., Reichert, H. and Furukubo-Tokunaga, K. (1995). Developmental defects in brain segmentation caused by mutations of the homeobox genes orthodenticle and empty spiracles in Drosophila. Neuron 15, 769-778.
39. Hogan, B. L. M., Horsburgh, G., Cohen, J., Hetherington, C. M., Fisher, G. and Lyon, M. F. (1986). Small eyes (Sey): a homozygous lethal mutation on chromosome 2 which affects the differentiation of both lens and nasal placodes in the mouse. J. Embryol. exp. Morph. 97, 95-110.
40. Hollemann, T., Bellefroid, E. and Pieler, T. (1998) The Xenopus homologue of the Drosophila gene tailless has a function in early eye development. Development 125, 2425-2432.
41. Houart, C., Westerfield, M. and Wilson, S. W. (1998). A small population of anterior cells patterns the forebrain during zebrafish gastrulation. Nature 391, 788-792.
42. Israel, D. I. (1993). A PCR-based method for high stringency screening of DNA libraries. Nucleic Acid Res. 21, 2627-2631.
43. Jenkins, N. A., Copeland, N. G., Taylor, B. A. and Lee, B. K. (1982). Organization, distribution, and stability of endogenous ecotopic murine leukemia virus DNA sequences in chromosomes of Mus musculus. J. Virol. 43, 26-36.
44. Juan, T. S.-C., McNiece, I. K., Argento, J. M., Jenkins, N. A., Gilbert, D. J. and Copland, N. G. (1997). Identification and mapping of Casp7, a cystein protease resembling CPP32beta, interleukin-1beta converting enzyme, and CED-3. Genomics 40, 86-93.
45. Kastury, K., Druck, T., Huebner, K., Barletta, C., Acampora, D., Simeone, A., Faiella, A. and Boncinelli, E. (1994). Chromosome locations of human EMX and OTX genes. Genomics 22, 41-45.
46. Kozak, M. (1986). Point mutations define a sequence flanking the AUG initiator codon that modulates translation by eukaryotic ribosomes. Cell 44, 283-292.
47. Krumlauf, R., Marshall, H., Studer, M., Nonchev, S., Sham, M. H. and Lumsden, A. (1994). Hox homeobox genes and regionalisation of the nervous system. J. Neurobiol. 24, 1328-1340.
48. Lufkin, T. (1996). Transcriptional control of Hox genes in vertebrate nervous system. Curr. Opin. Genet. Dev. 6, 575-580.
49. Lumsden, A. and Krumlauf, R. (1996). Patterning the vertebrate neuraxis. Science 214, 1109-1115.
50. Mastick, G. S., Davis, N. M., Andrews, G. L. and Easter Jr, S. S. (1997). Pax-6 functions in boundary formation and axon guidance in the embryonic mouse fbrebrain. Development 124, 1985-1997.
51. Matsuo, I., Kuratani, S., Kimura, C., Takeda, N. and Aizawa, S. (1995). Mouse Otx2 functions in the formation and patterning of rostral head. Genes Der. 9, 2646-2658.
52. Matsuo, T., Osumi-Yamashita, N., Noji, S., Ohuchi, H., Koyama, E., Myokai, F., Matsuo, N., Taniguchi, S., Doi, H., Ninomiya, Y., Fujiwara, M., Watanabe, T. and Eto, K. (1993). A mutation in the Pax-6 gene in rat small eye is associated with impaired migration of midbrain crest cells. Nature Genet. 3, 299-304.
53. Oliver, G., Mailhos, A., Wehr, R., Copeland, N. G., Jenkins, N. A. and Gruss, P. (1995). Six3, a murine homologue of the sine oculis gene, demarcates the most anterior border of the developing neural plate and is expressed during eye development. Development 121, 4045-55.
54. Pannese, M., Polo, C., Andreazzoli, M., Vignali, R., Kablar, B., Barsacchi, G. and Boncinelli, E. (1995). The Xenopus homologue of Otx2 is a maternal homeobox gene that demarcates and specifies anterior body regions. Development 121, 707-720.
55. Pellegrini, M., Mansouri, A., Simeone, A., Boncinelli, E. and Gruss, P. (1996). Dentate gyrus formation requires Emx2. Development 122, 3893-3898.
56. Pellier, V. and Astic, L. (1994). Histochemical and immunocytochemical study of the migration of neurons from the rat olfactory placode. Cell Tissue Research 275, 587-598.
57. Price, M., Lemaistre, M., Pischetola, M., Di Lauro, R. and Duboule, D. (1991). A mouse gene related to Distal-less shows a restricted expression in the developing forebrain. Nature 351, 748-751.
58. Puelles, L. and Rubenstein, J. L. R. (1993). Expression patterns of homeobox and other putative regulatory genes in the embryonic mouse forebrain suggests a neuromeric organization. Trends Neurosci. 16, 472-479.
59. Qiu, M., Anderson, S., Chen, S., Meneses, J. J., Hevner, R., Kuwana, E., Pedersen, R. A. and Rubenstein, J. L. R. (1996). Mutation of the Emx-1 homeobox gene disruptd the corpus callosum. Dev. Biol. 178, 174-178.
60. Roberts, R. C. (1967). Small-eyes, a new dominant mutant in the mouse. Genet. Res. 9, 121-122.
61. Ruiz i Altaba, A. (1994). Pattern formation in the vertebrate neural plate. Trends Neurosci. 17, 233-243.
62. Saha, M. S. and Grainger, R. M. (1992). A labile period in the determination of the anterior-posterior axis during early neural development in Xenopus. Neuron 8, 1003-1014.
63. Schwanzel-Fukuda, M., Crossin, K. L., Pfaff, D. W., Bouloux, P. M. G., Hardelin, J. P. and Petit, C. (1996). Migration of luteinizing hormone-releasing hormone (LHRH) neurons in early human embryos. J. Comp. Neurol. 366, 547-557.
64. Shawlot, W. and Behringer, R. R. (1995). Requirement for Lim I in head-organizer function. Nature 374, 425-430.
65. Shimamura, K. and Rubinstein, J. L. R. (1997). Inductive interactions direct early regionalization of the mouse forebrain. Development 124, 2709-2718.
66. Simeone, A., Acampora, D., Gulisano, M., Stornaiuolo, A. and Boncinelli, E. (1992a). Nested expression domains of four homeobox genes in developing rostral brain. Nature 358, 687-690.
67. Simeone, A., Acampora, D., Mallamaci, A., Stornaiuolo, A., D'Apice, M. R., Nigro, V. and Boncinelli, E. (1993). A vertebrate gene related to orthodenticle contains a homeodomain of the bicoid class and demarcates anterior neuroectoderm in the gastrulating mouse embryo. EMBO J. 12, 2735-2747.
68. Simeone, A., Gulisano, M., Acampora, D., Stornaiuolo, A., Rambaldi, M. and Boncinelli, E. (1992b). Two vertebrate homeobox genes related to the Drosophila empty spiracles gene are expressed in the embryonic cerebral cortex. EMBO J. 11, 2541-2550.
69. Spemann, H. and Mangold, H. (1924). Über die Induktion von Embryoanlagen durch Implantation artfremder Organisatoren. Roux Arch. EntwMech. Org. 100, 599-638.
70. St-Onge, L., Sosa-Pineda, B., Chowdhury, K., Mansouri, A. and Gruss, P. (1997). Pax6 is required for differentiation of glucagon-producing alpha-cells in mouse pancreas. Nature 387, 406-409.
71. Stein, S. and Kessel, M. (1995). A homeobox gene involved in node, notochord and neural plate formation of chick embryos. Mech. Dev. 49, 37-48.
72. Stein, S., Niss, K. and Kessel, M. (1996). Differential activation of the clustered homeobox genes CNOT2 and CNOT1 during notogenesis in the chick. Dev. Biol. 180, 519-533.
73. Stoykova, A., Fritsch, R., Walther, C. and Gruss, P. (1996). Forebrain patterning defects in Small eve mutant mice. Development 122, 3453-3465.
74. Stoykova, A., Götz, M., Gruss, P. and Price, J. (1997). Pax6-dependent regulation of adhesive patterning. R-cadherin expression and boundary formation in developing forebrain. Development 124, 3765-3777.
75. Stoykova, A. and Gruss, P. (1994). Roles of Pax-genes in developing and adult brain as suggested by expression patterns. J. Neurosci. 14, 1395-1412.
76. Szele, F. G. and Cepko, C. L. (1996). A subset of clones in the chick telencephalon arranged in rostrocaudal arrays. Current Biol. 6, 1685-1690.
77. Talbot, W. S., Trevarrow, B., Halpern, M. E., Melby, A. E., Farr, G., Postlethwait, J. H., Jowett, T., Kimmel, C. B. and Kimelman, D. (1995). A homeobox gene essential for zebrarish notochord development. Nature 378, 150-157
78. Thomas, P. and Beddington, R. (1996). Anterior primitive endoderm may be responsible for patterning the anterior neural plate of the mouse embryo. Current Biol. 6, 1487-1496.
79. Thor, T. (1995). The genetics of brain development: Conserved programs in flies and mice. Neuron 15, 975-977.
80. von Dassow, G., Schmidt, J. E. and Kimelman, D. (1993). Induction of the Xenopus organizer: expression and regulation of Xnol, a novel FGF and activin-regulated homeo box gene. Genes Dev. 7, 355-366.
81. Walldorf, U. and Gehring, W. J. (1992). Empty spiracles, a gap gene containing a homeobox involved in Drosophila head development. EMBO J. 11, 2247-2259.
82. Walther, C. and Gruss, P. (1991). Pax-6, a murine paired box gene, is expressed in the developing CNS. Development 113, 1435-1449.
83. Warren, N. and Price, D. J. (1997). Roles of Pax-6 in murine diencephalic development. Development 124, 1573-1582.
84. Wijnholds, J., Chowdhury, K., Wehr, R. and Gruss, P. (1995). Segment specific expression of the neuronatin gene during early hindbrain development. Dev. Biol. 171, 73-84.
85. Wilkinson, D. G. (1992). In Situ Hybridization: A Practical Approach Oxford: IRL Press.
86. Yoshida, M., Suda, Y., Matsuo, I., Miyamoto, N., Takeda, N., Kuratani, S. and Aizawa, S. (1997). Emx1 and Emx2 functions in development of dorsal telencephalon. Development 124, 101-111.
87. Zheng, L. M., Pfaff, D. W. and Schwanzel-Fukuda, M. (1992). Electron microscopic identification of luteinizing hormone-releasing hormone-immunoreactive neurons in the medial olfactory placode and basal forebrain of embryonic mice. Neuroscience 46, 407-418.