The zebrafish iguana locus encodes Dzip1, a novel zinc-finger protein required for proper regulation of Hedgehog signaling

Development

Volumn 131, Issue 11, 2004, Pages 2521-2532

  Sekimizu, Kohshin ^a   Nishioka, Noriyuki ^b,c   Sasaki, Hiroshi ^b   Takeda, Hiroyuki ^a   Karlstrom, Rolf O ^d   Kawakami, Atsushi ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b RIKEN Center for Biosystems Dynamics Research   (Japan)

^c OSAKA UNIVERSITY   (Japan)

^d UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

Adaxial cells; cAMP dependent kinase A; Cyclopamine; dzip1; Forskolin; Hedgehog signaling; Midline mutant; Muscle cell specification; Neural tube patterning; Pest sequence; Zebrafish

Indexed keywords

CELL PROTEIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; PROTEIN DZIP1; PROTEIN GLI; REGULATOR PROTEIN; SONIC HEDGEHOG PROTEIN; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN;

ANIMAL CELL; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; ENZYME ACTIVITY; ENZYME INDUCTION; GENE ACTIVATION; GENE ACTIVITY; GENE CONTROL; GENE EXPRESSION; GENE LOCUS; GENE MUTATION; GENE REPRESSION; GENE TARGETING; GENETIC ANALYSIS; GENETIC CODE; HUMAN; HUMAN CELL; MOLECULAR CLONING; NEURAL TUBE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; SOMITE; ZEBRA FISH;

AMINO ACID SEQUENCE; ANIMALS; BODY PATTERNING; CARRIER PROTEINS; EMBRYO, NONMAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEDGEHOG PROTEINS; MOLECULAR SEQUENCE DATA; MUTATION; ONCOGENE PROTEINS; PEPTIDES; QUANTITATIVE TRAIT LOCI; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION; SOMITES; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; ZEBRAFISH; ZEBRAFISH PROTEINS; ZINC FINGERS;

ANIMALIA; DANIO RERIO; ERINACEIDAE; IGUANA; VERTEBRATA;

EID: 3042733150     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.01059     Document Type: Review

References (99)

1. Aza-Blanc, P., Ramirez-Weber, F.-A., Laget, M.-P., Schwartz, C. and Kornberg, T. B. (1997). Proteolysis that is inhibited by hedgehog targets Cubitus interruptus protein to the nucleus and converts it to a repressor. Cell 89, 1043-1053.
2. Aza-Blanc, P., Lin, H. Y., Ruiz i Altaba, A. and Kornberg, T. B. (2000). Expression of the vertebrate Gli proteins in Drosophila reveals a distribution of activator and repressor activities. Development 127, 4293-4301.
3. Bai, C. B. and Joyner, A. L. (2001). Gli1 can rescue the in vivo function of Gli2. Development 128, 5161-5172.
4. Bai, C. B., Auerbach, W., Lee, J. S., Stephen, D. and Joyner, A. L. (2002). Gli2, but not Gli1, is required for initial Shh signaling and ectopic activation of the Shh pathway. Development 129, 4753-4761.
5. Barth, K. A. and Wilson, S. W. (1995). Expression of zebrafish nk2.2 is influenced by sonic hedgehog/vertebrate hedgehog-1 and demarcates a zone of neuronal differentiation in the embryonic forebrain. Development 121, 1755-1768.
6. Barresi, M. J., Stickney, H. L. and Devoto, S. H. (2000). The zebrafish slow-muscle-omitted gene product is required for Hedgehog signal transduction and the development of slow muscle identity. Development 127, 2189-2199.
7. Blagden, C. S., Currie, P. D., Ingham, P. W. and Hughes, S. M. (1997). Notochord induction of zebrafish slow muscle mediated by Sonic hedgehog. Genes Dev. 11, 2163-2175.
8. Brand, M., Heisenberg, C. P., Warga, R. M., Pelegri, F., Karlstrom, R. O., Beuchle, D., Picker, A., Jiang, Y. J., Furutani-Seiki, M., van Eeden, F. J. et al. (1996). Mutations affecting development of the midline and general body shape during zebrafish embryogenesis. Development 123, 129-142.
9. Bumcrot, D. A. and McMahon, A. P. (1995). Somite differentiation. Sonic signals somites. Curr. Biol. 5, 612-614.
10. Chen, J. N., Haffter, P., Odenthal, J., Vogelsang, E., Brand, M., van Eeden, F. J., Furutani-Seiki, M., Granato, M., Hammerschmidt, M., Heisenberg, C. P. et al. (1996). Mutations affecting the cardiovascular system and other internal organs in zebrafish. Development 123, 293-302.
11. Chen, Y., Gallaher, N., Goodman, R. and Smolik, S. (1998). Protein kinase A directly regulates the activity and proteolysis of Cubitus interruptus. Proc. Natl. Acad. Sci. USA 95, 2349-2354.
12. Chen, Y., Cardinaux, J., Goodman, R. and Smolik, S. (1999). Mutants of cubitus interruptus that are independent of PKA regulation are independent of hedgehog signaling. Development 126, 3607-3616.
13. Chen, W., Burgess, S. and Hopkins, N. (2001). Analysis of the zebrafish smoothened mutant reveals conserved and divergent functions of hedgehog activity. Development 128, 2385-2396.
14. Chiang, C., Litingtung, Y., Lee, E., Young, K. E., Corden, J. L., Westphal, H. and Beachy, P. A. (1996). Cyclopia and defective axial patterning in mice lacking sonic hedgehog gene function. Nature 383, 407-413.
15. Concordet, J. P., Lewis, K. E., Moore, J. W., Goodrich, L. V., Johnson, R. L., Scott, M. P. and Ingham, P. W. (1996). Spatial regulation of a zebrafish patched homologue reflects the roles of sonic hedgehog and protein kinase A in neural tube and somite patterning. Development 122, 2835-2846.
16. Currie, P. D. and Ingham, P. W. (1996). Induction of a specific muscle cell type by a hedgehog-like protein in zebrafish. Nature 382, 452-455.
17. Dai, P., Akimaru, H., Tanaka, Y., Maekawa, T., Nakafuku, M. and Ishii, S. (1999). Sonic hedgehog-induced activation of the Gli1 promoter is mediated by GLI3. J. Biol. Chem. 19, 8143-8152.
18. Ding, Q., Motoyama, J., Gasca, S., Rong, M., Sasaki, H., Rossant, J. and Hui, C.-C. (1998). Diminished Sonic hedgehog signaling and lack of floor plate differentiation in Gli2 mutant mice. Development 125, 2533-2543.
19. Ding, Q., Fukami, S., Meng, X., Nishizaki, Y., Zhang, X., Sasaki, H., Dlugosz, A., Nakafuku, M. and Hui, C. (1999). Mouse suppressor of fused is a negative regulator of sonic hedgehog signaling and alters the subcellular distribution of Gli1. Curr. Biol. 9, 1119-1122.
20. Echelard, Y., Epstein, D. J., St-Jacques, B., Shen, L., Mohler, J., McMahon, J. A. and McMahon, A. P. (1993). Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity. Cell 75, 1417-1430.
21. Ekker, S. C., Ungar, A. R., Greenstein, P., von Kessler, D. P., Porter, J. A., Moon, R. T. and Beachy, P. A. (1995). Patterning activities of vertebrate Hedgehog proteins in the developing eye and brain. Curr. Biol. 5, 944-955.
22. Epstein, D. J., Marti, E., Scott, M. P. and McMahon, A. P. (1996). Antagonizing cAMP-dependent protein kinase A in the dorsal CNS activates a conserved sonic hedgehog signaling pathway. Development 122, 2885-2894.
23. 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 motor neuron identity. Cell 87, 661-673.
24. Ericson, J., Rashbass, P., Schedl, A., Brenner-Morton, S., Kawakami, A., van Heyningen, V., Jessell, T. M. and Briscoe, J. (1997). Pax6 controls progenitor cell identity and neuronal fate in response to graded Shh signaling. Cell 90, 169-180.
25. Fan, C. M. and Tessier-Lavigne, M. (1994). Patterning of mammalian somites by surface ectoderm and notochord: evidence for sclerotome induction by a hedgehog homolog. Cell 79, 1175-1186.
26. Goodrich, L. V., Johnson, R. L., Milenkovic, L., McMahon, J. A. and Scott, M. P. (1996). Conservation of the hedgehog/patched signaling pathway from flies to mice: induction of a mouse patched gene by hedgehog. Genes Dev. 10, 301-312.
27. Goodrich, L. V. and Scott, M. P. (1998). Hedgehog and patched in neural development and disease. Neuron 21, 1243-1257.
28. Hammerschmidt, M., Bitgood, M. J. and McMahon, A. P. (1996). Protein kinase A is a common negative regulator of hedgehog signaling in the vertebrate embryo. Genes Dev. 10, 647-658.
29. Hughes, E. N. and August, J. T. (1981). Characterization of plasma membrane proteins identified by monoclonal antibodies. J. Biol. Chem. 256, 664-671.
30. Hui, C. C., Slusarski, D., Platt, K. A., Holmgren, R. and Joyner, A. L. (1994). Expression of three mouse homologs of the Drosophila segment polarity gene cubitus interruptus, Gli, Gli-2, and Gli-3, in ectoderm and mesoderm-derived tissues suggests multiple roles during postimplantation development. Dev. Biol. 62, 402-413.
31. Hynes, M., Stone, D. M., Dowd, M., Pitts-Meek, S., Goddard, A., Gurney, A. and Rosenthal, A. (1997). Control of cell pattern in the neural tube by the zinc finger transcription factor and oncogene gli-1. Neuron 19, 15-26.
32. Incardona, J. P., Gaffield, W., Kapur, R. P. and Roelink, H. (1998). The teratogenic Veratrum alkaloid cyclopamine inhibits sonic hedgehog signal transduction. Development 125, 3553-3562.
33. Ingham, P. W. and McMahon, A. P. (2001). Hedgehog signaling in animal development: paradigms and principles. Genes Dev. 15, 3059-3087.
34. Jiang, J. and Struhl, G. (1998). Regulation of the Hedgehog and Wingless signaling pathways by the F-box/WD40-repeat protein Slimb. Nature 391, 493-496.
35. Karlstrom, R. O., Trowe, T., Klostermann, S., Baier, H., Brand, M., Crawford, A. D., Grunewald, B., Haffter, P., Hoffmann, H., Meyer, S. U. et al. (1996). Zebrafish mutations affecting retinotectal axon pathfinding. Development 123, 427-438.
36. Karlstrom, R. O., Talbot, W. S. and Schier, A. F. (1999). Comparative synteny cloning of zebrafish you-too: mutations in the Hedgehog target gli2 affect ventral forebrain patterning. Genes Dev. 13, 388-393.
37. Karlstrom, R. O., Tyurina, O. V., Kawakami, A., Nishioka, N., Talbot, W. S., Sasaki, H., Schier, A. F. (2003). Genetic analysis of zebrafish gli1 and gli2 reveals divergent requirements for gli genes in vertebrate development. Development 130, 1549-1564.
38. Knapik, E. W., Goodman, A., Ekker, M., Chevrette, M., Delgado, J., Neuhauss, S., Shimoda, N., Driever, W., Fishman, M. C. and Jacob, H. J. (1998). A microsatellite genetic linkage map for zebrafish (Danio rerio). Nat. Genet. 18, 338-343.
39. Koebernick, K. and Pieler, T. (2002). Gli-type zinc finger proteins as bipotential transducers of Hedgehog signaling. Differentiation 70, 69-76.
40. Kogerman, P., Grimm, T., Kogerman, L., Krause, D., Unden, A. B., Sandstedt, B., Toftgard, R., and Zaphiropoulos, P. G. (1999). Mammalian suppressor-of-fused modulates nuclear cytoplasmic shuttling of Gli-1. Nat. Cell Biol. 1, 312-319.
41. Krauss, S., Concordet, J. P. and Ingham, P. W. (1993). A functionally conserved homolog of the Drosophila segment polarity gene hh is expressed in tissues with polarizing activity in zebrafish embryos. Cell 75, 1431-1444.
42. Lee, J., Platt, K. A., Censullo, P. and Ruiz i Altaba, A. (1997). Gli1 is a target of sonic hedgehog that induces ventral neural tube development. Development 124, 2537-2552.
43. Lepage, T., Cohen, S. M., Diaz-Benjumea, F. J. and Parkhurst, S. M. (1995). Signal transduction by cAMP-dependent protein kinase A in Drosophila limb patterning. Nature 373, 711-715.
44. Lewis, K. E., Currie, P. D., Roy, S., Schauerte, H., Haffter, P. and Ingham, P. W. (1999). Control of muscle cell-type specification in the zebrafish embryo by Hedgehog signaling. Dev. Biol. 216, 469-480.
45. Li, W., Ohlmeyer, J. T., Lane, M. E. and Kalderon, D. (1995). Function of protein kinase A in hedgehog signal transduction and Drosophila imaginal disc development. Cell 80, 553-562.
46. Litingtung, Y. and Chiang, C. (2000). Specification of ventral neuron types is mediated by an antagonistic interaction between Shh and Gli3. Nat. Neurosci. 3, 979-985.
47. Macdonald, R., Barth, K. A., Xu, Q., Holder, N., Mikkola, I. and Wilson, S. W. (1995). Midline signaling is required for Pax gene regulation and patterning of the eyes. Development 121, 3267-3278.
48. Marigo, V., Johnson, R. L., Vortkamp, A. and Tabin, C. J. (1996). Sonic hedgehog differentially regulates expression of gli and gli3 during limb development. Dev. Biol. 180, 273-283.
49. Masuya, H., Sagai, T., Wakana, S., Moriwaki, K. and Shiroishi, T. (1995). A duplicated zone of polarizing activity in polydactylous mouse mutants. Genes Dev. 9, 1645-1653.
50. Matise, M., Epstein, D., Park, H., Platt, K. and Joyner, A. (1998). Gli2 is required for the induction of floor plate and adjacent cells, but not most ventral neurons in the mouse central nervous system. Development 125, 2759-2770.
51. McMahon, A. P. (2000). More surprises in the hedgehog signaling pathway. Cell 100, 185-188.
52. McMahon, A., Ingham, P. and Tabin, C. (2003). The developmental roles and clinical significance of Hedeghog signaling. Curr. Top. Dev. Biol. 53, 1-114.
53. Methot, N. and Basler, K. (2000). Suppressor of fused opposes hedgehog transduction by impeding nuclear accumulation of the activator form of Cubitus interruptus. Development 127, 4001-4010.
54. Methot, N. and Basler, K. (2001). An absolute requirement for Cubitus interruptus in Hedgehog signaling. Development 128, 733-742.
55. Morin-Kensicki, E. M. and Eisen, J. S. (1997). Sclerotome development and peripheral nervous system segmentation in embryonic zebrafish. Development 124, 159-167.
56. Monnier, V., Dussillol, E., Alves, G., Lamour-Isnard, C. and Plessis, A. (1998). Molecular interactions between three members of the Drosophila Hedgehog signaling pathway: Suppressor of fused links the ser-thr kinase Fused and the transcription factor Cubitus interruptus. Curr. Biol. 8, 583-586.
57. Moore, F. L., Jaruzelska, J., Fox, M. S., Urano, J., Firpo, M. T., Turek, P. J., Dorfman, D. M. and Pera, R. A. (2003). Human Pumilio-2 is expressed in embryonic stem cells and germ cells and interacts with DAZ (Deleted in AZoospermia) and DAZ-like proteins. Proc. Natl. Acad. Sci. USA 100, 538-543.
58. Murone, M., Luoh, S. M., Stone, D., Li, W., Gurney, A., Armanini, M., Grey, C., Rosenthal, A. and de Sauvage, F. J. (2000). Gli regulation by the opposing activities of fused and suppressor of fused. Nat. Cell Biol. 2, 310-312.
59. Nakano, Y., Kim, H. R., Kawakami, A., Roy, S., Schier, A. and Ingham, P. W. (2004). Inactivation of dispatched 1 by the chameleon mutation disrupts Hedgehog signaling in the zebrafish embryo. Dev. Biol. (in press).
60. Nybakken, K. and Perrimon, N. (2002). Hedgehog signal transduction: recent findings Curr. Opin. Genet. Dev. 12, 503-511.
61. Odenthal, J., van Eeden, F. J., Haffter, P., Ingham, P. W. and Nusslein-Volhard, C. (2000). Two distinct cell populations in the floor plate of the zebrafish are induced by different pathways. Dev. Biol. 219, 350-363.
62. Ohlmeyer, J. and Kalderon, D. (1998). Hedgehog stimulates maturation of Cubitus interruptus into a labile transcriptional activator. Nature 396, 749-753.
63. Pan, D. and Rubin, G. M. (1995). cAMP-dependent protein kinase and hedgehog act antagonistically in regulating decapentaplegic transcription in Drosophila imaginal discs. Cell 80, 543-552.
64. Park, H. L., Bai, C., Platt, K. A., Matise, M. P., Beeghly, A., Hui, C. C., Nakashima, M. and Joyner, A. L. (2000). Mouse Gli1 mutants are viable but have defects in SHH signaling in combination with a Gli2 mutation. Development 127, 1593-1605.
65. Pearse, R. V., II, Collier, L. S., Scott, M. P. and Tabin, C. J. (1999). Vertebrate homologs of Drosophila Suppressor of fused interact with the Gli family of transcriptional regulators. Dev. Biol. 212, 323-336.
66. Persson, M., Stamataki, D., te Welscher, P., Andersson, E., Bose, J., Ruther, U., Ericson, J. and Briscoe, J. (2002). Dorsal-ventral patterning of the spinal cord requires Gli3 transcriptional repressor activity. Genes Dev. 16, 2865-2878.
67. Pham, A., Therond, P., Alves, G., Tournier, E. B., Busson, D., Lamour-Isnard, C., Bouchon, B. L., Preat, T. and Tricoire, H. (1995). The Suppressor of fused gene encodes a novel PEST protein involved in Drosophila segment polarity establishment. Genetics 140, 587-598.
68. Postlethwait, J. H. and Talbot, W. S. (1997). Zebrafish genomics: from mutants to genes. Trends Genet. 13, 183-190.
69. Price, M. and Kalderon, D. (1999). Proteolysis of cubitus interruptus in Drosophila requires phosphorylation by protein kinase A. Development 126, 4331-4339.
70. Radhakrishna, U., Wild, A., Grzeschik, K.-H. and Antonarakis, S. E. (1997). Mutation in Gli3 in postaxial polydactyly type A. Nat. Genet. 17, 269-271.
71. Rechsteiner, M. and Rogers, S. W. (1996). PEST sequences and regulation by proteolysis. Trends Biochem. Sci. 21, 267-271.
72. Robbins, D., Nybakken, K., Kobayashi, R., Sisson, J., Bishop, J. and Therond, P. (1997). Hedgehog elicits signal transduction by means of a large complex containing the kinesin-related protein Costal2. Cell 90, 225-234.
73. Roelink, H., Augsburger, A., Heemskerk, J., Korzh, V., Norlin, S., Ruiz i Altaba, A., Tanabe, Y., Placzek, M., Edlund, T., Jessell, T. M. et al. (1994). Floor plate and motor neuron induction by vhh-1, a vertebrate homolog of hedgehog expressed by the notochord. Cell 76, 761-775.
74. Roy, S., Wolff, C. and Ingham, P. W. (2001). The u-boot mutation identifies a Hedgehog-regulated myogenic switch for fiber-type diversification in the zebrafish embryo. Genes Dev. 15, 1563-1576.
75. Ruiz i Altaba, A. (1998). Combinatorial Gli function in floor plate and neuronal inductions by Sonic hedgehog. Development 125, 2203-2212.
76. Ruiz i Altaba, A. (1999a). Gli proteins encode context-dependent positive and negative functions: implications for development and disease. Development 126, 3205-3216.
77. Ruiz i Altaba, A. (1999b). Gli proteins and hedgehog signaling - development and cancer. Trends Genet. 15, 418-425.
78. Ruiz i Altaba, A., Sanchez, P. and Dahmane, N. (2002). Gli and hedgehog in cancer: tumours, embryos and stem cells. Nat. Rev. Cancer 2, 361-372.
79. Sasaki, H., Nishizaki, Y., Hui, C., Nakafuku, M. and Kondoh, H. (1999). Regulation of Gli2 and Gli3 activities by an amino-terminal repression domain: implication of Gli2 and Gli3 as primary mediators of Shh signaling. Development 126, 3915-3924.
80. Sbrogna, J. L., Barresi, M. J. F. and Karlstrom, R. O. (2003). Multiple roles for Hedgehog signaling in zebrafish pituitary development. Dev. Biol. 254, 19-35.
81. Schauerte, H. E., van Eeden, F. J., Fricke, C., Odenthal, J., Strahle, U. and Haffter, P. (1998). Sonic hedgehog is not required for the induction of medial floor plate cells in the zebrafish. Development 125, 2983-2993.
82. Schier, A. F., Neuhauss, S. C. F., Helde, K. A., Talbot, W. S. and Driever, W. (1997). The one-eyed pinhead gene functions in mesoderm and endoderm formation in zebrafish and interacts with no tail. Development 124, 327-342.
83. Seamon, K. B. and Daly, J. W. (1981). Forskolin: a unique diterpene activator of cyclic AMP-generating systems. J. Cyclic Nucl. Res. 7, 201-224.
84. Shin, S. H., Kogerman, P., Lindstrom, E., Toftgard, R. and Biesecker, L. G. (1999). GLI3 mutations in human disorders mimic Drosophila cubitus interruptus protein functions and localization. Proc. Natl. Acad. Sci. USA 96, 2880-2884.
85. Sisson, J. C., Ho, K., S., Suyama, K. and Scott, M. P. (1997). Costal2, a novel kinesin-related protein in the hedgehog signaling pathway. Cell 90, 235-245.
86. Stegman, M., Vallance, J., Elangovan, G., Sosinski, J., Cheng, Y. and Robbins, D. (2000). Identification of a tetrameric hedgehog signaling complex. J. Biol. Chem. 275, 21809-21812.
87. Taipale, J., Chen, J. K., Cooper, M. K., Wang, B., Mann, R. K., Milenkovic, L., Scott, M. P. and Beachy, P. A. (2000). Effects of oncogenic mutations in Smoothened and Patched can be reversed by cyclopamine. Nature 406, 1005-1009.
88. Tole, S., Ragsdale, C. W. and Grove, E. A. (2000). Dorsoventral patterning of the telencephalon is disrupted in the mouse mutant extra-toes(J). Dev. Biol. 217, 254-265.
89. van Eeden, F. J., Granato, M., Schach, U., Brand, M., Furutani-Seiki, M., Haffter, P., Hammerschmidt, M., Heisenberg, C. P., Jiang, Y. J., Kane, D. A. et al. (1996a). Genetic analysis of fin formation in the zebrafish, Danio rerio. Development 123, 255-262.
90. van Eeden, F. J., Granato, M., Schach, U., Brand, M., Furutani-Seiki, M., Haffter, P., Hammerschmidt, M., Heisenberg, C. P., Jiang, Y. J., Kane, D. A. et al. (1996b). Mutations affecting somite formation and patterning in the zebrafish, Danio rerio. Development 123, 153-164.
91. Varga, Z. M., Amores, A., Lewis, K. E., Yan, Y. L., Postlethwait, J. H., Eisen, J. S. and Westerfield, M. (2001). Zebrafish smoothened functions in ventral neural tube specification and axon tract formation. Development 128, 3497-3509.
92. Villavicencio, E. H, Walterhouse, D. O. and Iannaccone, P. M. (2000). The sonic hedgehog-patched-gli pathway in human development and disease. Am. J. Hum. Genet. 67, 1047-1054.
93. von Mering, C. and Basler, K. (1999). Distinct and regulated activities of human Gli proteins in Drosophila. Curr. Biol. 9, 1319-1322.
94. Wallis, D. and Muenke, M. (2000). Mutations in holoprosencephaly. Hum. Mutat. 16, 99-108.
95. Wang, B., Fallon, J. F. and Beachy, P. A. (2000). Hedgehog-regulated processing of Gli3 produces an anterior/posterior repressor gradient in the developing vertebrate limb. Cell 100, 423-434.
96. Wang, Q. T. and Holmgren, R. A. (1999). The subcellular localization and activity of Drosophila cubitus interruptus are regulated at multiple levels. Development 126, 5097-5106.
97. Weinberg, E. S., Allende, M. L., Kelly, C. S., Abdelhamid, A., Murakami, T., Andermann, P., Doerre, O. G., Grunwald, D. J. and Riggleman, B. (1996). Developmental regulation of zebrafish MyoD in wild-type, no tail and spadetail embryos. Development 122, 271-280.
98. Westerfield, M. (1993). The Zebrafish Book. Eugene: University of Oregon Press.
99. Wolff, C., Roy, S. and Ingham, P. W. (2003). Multiple muscle cell identities induced by distinct levels and timing of hedgehog activity in the zebrafish embryo. Curr. Biol. 13, 1169-1181.