Genomic characterization of Wilms' tumor suppressor 1 targets in nephron progenitor cells during kidney development

Development

Volumn 137, Issue 7, 2010, Pages 1189-1203

  Hartwig, Sunny ^a,b,c   Ho, Jacqueline ^a,b,c   Pandey, Priyanka ^a,b,c   MacIsaac, Kenzie ^d   Taglienti, Mary ^a,b,c   Xiang, Michael ^a   Alterovitz, Gil ^a   Ramoni, Marco ^a   Fraenkel, Ernest ^d,e   Kreidberg, Jordan A ^a,b,c  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c HARVARD STEM CELL INSTITUTE   (United States)

^d Massachusetts Institute of Technology Cambridge   (United States)

^e MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

ChIP chip; Kidney; Mouse; Progenitor; Transcription factor; WT1

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; EMBRYO; EX VIVO STUDY; EXPLANT; GENE EXPRESSION; GENE IDENTIFICATION; GENE TARGETING; GENETIC TRAIT; IN VIVO STUDY; KIDNEY DEVELOPMENT; MOUSE; NEPHRON; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STEM CELL; TUMOR SUPPRESSOR GENE; WILM TUMOR SUPPRESSOR 1 GENE; ANIMAL; ANIMAL EMBRYO; CHROMATIN IMMUNOPRECIPITATION; CYTOLOGY; FACTUAL DATABASE; FEMALE; GENE EXPRESSION REGULATION; GENETICS; HISTOLOGY; IN SITU HYBRIDIZATION; KIDNEY; METABOLISM; MICROARRAY ANALYSIS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PREGNANCY; PRENATAL DEVELOPMENT; TISSUE CULTURE TECHNIQUE;

ANTISENSE OLIGONUCLEOTIDE; WT1 PROTEIN;

ANIMALS; APOPTOSIS; BASE SEQUENCE; CHROMATIN IMMUNOPRECIPITATION; DATABASES, FACTUAL; EMBRYO, MAMMALIAN; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IN SITU HYBRIDIZATION; KIDNEY; MICE; MICROARRAY ANALYSIS; NEPHRONS; OLIGONUCLEOTIDES, ANTISENSE; PREGNANCY; STEM CELLS; TISSUE CULTURE TECHNIQUES; WT1 PROTEINS;

EID: 77950473796     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.045732     Document Type: Article

References (129)

1. Ai, X., Kitazawa, T., Do, A. T., Kusche-Gullberg, M., Labosky, P. A. and Emerson, C. P., Jr (2007). SULF1 and SULF2 regulate heparan sulfate-mediated GDNF signaling for esophageal innervation. Development 134, 3327-3338.
2. Alcedo, J., Ayzenzon, M., Von Ohlen, T., Noll, M. and Hooper, J. E. (1996). The Drosophila smoothened gene encodes a seven-pass membrane protein, a putative receptor for the hedgehog signal. Cell 86, 221-232. (Pubitemid 26286105)
3. Alvarez-Bolado, G. and Eichele, G. (2006). Analysing the developing brain transcriptome with the GenePaint platform. J. Physiol. 575, 347-352. (Pubitemid 44274736)
4. Andersson, T., Sodersten, E., Duckworth, J. K., Cascante, A., Fritz, N., Sacchetti, P., Cervenka, I., Bryja, V. and Hermanson, O. (2009). CXXC5 is a novel BMP4-regulated modulator of Wnt signaling in neural stem cells. J. Biol. Chem. 284, 3672-3681.
5. Arnaud, L., Ballif, B. A., Forster, E. and Cooper, J. A. (2003). Fyn tyrosine kinase is a critical regulator of disabled-1 during brain development. Curr. Biol. 13, 9-17. (Pubitemid 36080617)
6. Basile, J. R., Afkhami, T. and Gutkind, J. S. (2005). Semaphorin 4D/plexin-B1 induces endothelial cell migration through the activation of PYK2, Src, and the phosphatidylinositol 3-kinase-Akt pathway. Mol. Cell. Biol. 25, 6889-6898. (Pubitemid 41105890)
7. Bennington, J. and Beckwith, J. (1975). Tumors of the Kidney, Renal Pelvis and Ureter. Washington, DC: Armed Forces Institute of Pathology.
8. Bergsland, M. W. M., Malewicz, M., Perlmann, T. and Muhr, J. (2006). The establishment of neuronal properties is controlled by Sox4 and Sox11. Genes Dev. 20, 3475-3486. (Pubitemid 44969164)
9. Bohm, J., Buck, A., Borozdin, W., Mannan, A. U., Matysiak-Scholze, U., Adham, I., Schulz-Schaeffer, W., Floss, T., Wurst, W., Kohlhase, J. et al. (2008). Sall1, sall2, and sall4 are required for neural tube closure in mice. Am. J. Pathol. 173, 1455-1463.
10. Bor, Y., Swartz, J., Morrison, A., Rekosh, D., Ladomery, M. and Hammarskjold, M. L. (2006). The Wilms' tumor 1 (WT1) gene (+KTS isoform) functions with a CTE to enhance translation from an unspliced RNA with a retained intron. Genes Dev. 20, 1597-1608. (Pubitemid 43901099)
11. Boyer, L. A., Lee, T. I., Cole, M. F., Johnstone, S. E., Levine, S. S., Zucker, J. P., Guenther, M. G., Kumar, R. M., Murray, H. L., Jenner, R. G. et al. (2005). Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122, 947-956. (Pubitemid 41345211)
12. Brent, A. E. and Tabin, C. J. (2004). FGF acts directly on the somitic tendon progenitors through the Ets transcription factors Pea3 and Erm to regulate scleraxis expression. Development 131, 3885-3896.
13. Brunskill, E. W., Aronow, B. J., Georgas, K., Rumballe, B., Valerius, M. T., Aronow, J., Kaimal, V., Jegga, A. G., Yu, J., Grimmond, S. et al. (2008). Atlas of gene expression in the developing kidney at microanatomic resolution. Dev. Cell 15, 781-791.
14. Buglino, J. A. and Resh, M. D. (2008). Hhat is a palmitoylacyltransferase with specificity for N-palmitoylation of Sonic Hedgehog. J. Biol. Chem. 283, 22076-22088.
15. Call, K. M., Glaser, T., Ito, C. Y., Buckler, A. J., Pelletier, J., Haber, D. A., Rose, E. A., Kral, A., Yeger, H., Lewis, W. H. et al. (1990). Isolation and characterization of a zinc finger polypeptide gene at the human chromosome 11 Wilms' tumor locus. Cell 60, 509-520. (Pubitemid 20060879)
16. Capellini, T. D., Di Giacomo, G., Salsi, V., Brendolan, A., Ferretti, E., Srivastava, D., Zappavigna, V. and Selleri, L. (2006). Pbx1/Pbx2 requirement for distal limb patterning is mediated by the hierarchical control of Hox gene spatial distribution and Shh expression. Development 133, 2263-2273. (Pubitemid 43986136)
17. Capellini, T. D., Zewdu, R., Di Giacomo, G., Asciutti, S., Kugler, J. E., Di Gregorio, A. and Selleri, L. (2008). Pbx1/Pbx2 govern axial skeletal development by controlling Polycomb and Hox in mesoderm and Pax1/Pax9 in sclerotome. Dev. Biol. 321, 500-514.
18. Cho, E. A., Prindle, M. J. and Dressler, G. R. (2003). BRCT domain-containing protein PTIP is essential for progression through mitosis. Mol. Cell. Biol. 23, 1666-1673.
19. De Felici, M., Farini, D. and Dolci, S. (2009). In or out stemness: comparing growth factor signalling in mouse embryonic stem cells and primordial germ cells. Curr. Stem Cell Res. Ther. 4, 87-97.
20. Di-Poi, N., Zakany, J. and Duboule, D. (2007). Distinct roles and regulations for HoxD genes in metanephric kidney development. PLoS Genet. 3, e232.
21. Donovan, M. J., Natoli, T. A., Sainio, K., Amstutz, A., Jaenisch, R., Sariola, H. and Kreidberg, J. A. (1999). Initial differentiation of the metanephric mesenchyme is independent of WT1 and the ureteric bud. Dev. Genet. 24, 252-262. (Pubitemid 29211789)
22. Dressler, G. R., Deutsch, U., Chowdhury, K., Nornes, H. O. and Gruss, P. (1990). Pax2, a new murine paired-box-containing gene and its expression in the developing excretory system. Development 109, 787-795. (Pubitemid 20267191)
23. Drummond, I. A., Rupprecht, H. D., Rohwer-Nutter, P., Lopez-Guisa, J. M., Madden, S. L., Rauscher, F. J., 3rd and Sukhatme, V. P. (1994). DNA recognition by splicing variants of the Wilms' tumor suppressor, WT1. Mol. Cell. Biol. 14, 3800-3809. (Pubitemid 24160787)
24. Dudley, A. T., Lyons, K. M. and Robertson, E. J. (1995). A requirement for bone morphogenetic protein-7 during development of the mammalian kidney and eye. Genes Dev. 9, 2795-2807.
25. Edom-Vovard, F., Schuler, B., Bonnin, M. A., Teillet, M. A. and Duprez, D. (2002). Fgf4 positively regulates scleraxis and tenascin expression in chick limb tendons. Dev. Biol. 247, 351-366. (Pubitemid 34734870)
26. Englert, C., Hou, X., Maheswaran, S., Bennett, P., Ngwu, C., Re, G. G., Garvin, A. J., Rosner, M. R. and Haber, D. A. (1995). WT1 suppresses synthesis of the epidermal growth factor receptor and induces apoptosis. EMBO J. 14, 4662-4675.
27. Fairall, L., Schwabe, J. W., Chapman, L., Finch, J. T. and Rhodes, D. (1993). The crystal structure of a two zinc-finger peptide reveals an extension to the rules for zinc-finger/DNA recognition. Nature 366, 483-487. (Pubitemid 24013885)
28. Farnham, P. J. (2009). Insights from genomic profiling of transcription factors. Nat. Rev. Genet. 10, 605-616.
29. Fischer, M., Pereira, P. M., Holtmann, B., Simon, C. M., Hanauer, A., Heisenberg, M. and Sendtner, M. (2009). P90 Ribosomal s6 kinase 2 negatively regulates axon growth in motoneurons. Mol. Cell. Neurosci. 42, 134-141.
30. Gao, X., Chen, X., Taglienti, M., Rumballe, B., Little, M. H. and Kreidberg, J. A. (2005). Angioblast-mesenchyme induction of early kidney development is mediated by Wt1 and Vegfa. Development 132, 5437-5449. (Pubitemid 43125871)
31. Gautrey, H., McConnell, J., Lako, M., Hall, J. and Hesketh, J. (2008). Staufen1 is expressed in preimplantation mouse embryos and is required for embryonic stem cell differentiation. Biochim. Biophys. Acta 1783, 1935-1942.
32. Gessler, M., Poustka, A., Cavenee, W., Neve, R. L., Orkin, S. H. and Bruns, G. A. (1990). Homozygous deletion in Wilms tumours of a zinc-finger gene identified by chromosome jumping. Nature 343, 774-778. (Pubitemid 20065258)
33. Gessler, M., Konig, A. and Bruns, G. A. (1992). The genomic organization and expression of the WT1 gene. Genomics 12, 807-813.
34. Giordano, S., Corso, S., Conrotto, P., Artigiani, S., Gilestro, G., Barberis, D., Tamagnone, L. and Comoglio, P. M. (2002). The semaphorin 4D receptor controls invasive growth by coupling with Met. Nat. Cell Biol. 4, 720-724. (Pubitemid 34993710)
35. Haber, D. A., Buckler, A. J., Glaser, T., Call, K. M., Pelletier, J., Sohn, R. L., Douglass, E. C. and Housman, D. E. (1990). An internal deletion within an 11p13 zinc finger gene contributes to the development of Wilms' tumor. Cell 61, 1257-1269. (Pubitemid 20208830)
36. Haber, D. A., Sohn, R. L., Buckler, A. J., Pelletier, J., Call, K. M. and Housman, D. E. (1991). Alternative splicing and genomic structure of the Wilms tumor gene WT1. Proc. Natl. Acad. Sci. USA 88, 9618-9622. (Pubitemid 21915682)
37. Hamatani, T., Carter, M. G., Sharov, A. A. and Ko, M. S. (2004). Dynamics of global gene expression changes during mouse preimplantation development. Dev. Cell 6, 117-131. (Pubitemid 38089210)
38. Hamatani, T., Ko, M., Yamada, M., Kuji, N., Mizusawa, Y., Shoji, M., Hada, T., Asada, H., Maruyama, T. and Yoshimura, Y. (2006). Global gene expression profiling of preimplantation embryos. Hum. Cell 19, 98-117.
39. Hamilton, T. B., Barilla, K. C. and Romaniuk, P. J. (1995). High affinity binding sites for the Wilms' tumour suppressor protein WT1. Nucleic Acids Res. 23, 277-284.
40. Harita, Y., Kurihara, H., Kosako, H., Tezuka, T., Sekine, T., Igarashi, T. and Hattori, S. (2008). Neph1, a component of the kidney slit diaphragm, is tyrosine-phosphorylated by the Src family tyrosine kinase and modulates intracellular signaling by binding to Grb2. J. Biol. Chem. 283, 9177-9186.
41. Hartwig, S., Hu, M. C., Cella, C., Piscione, T., Filmus, J. and Rosenblum, N. D. (2005). Glypican-3 modulates inhibitory Bmp2-Smad signaling to control renal development in vivo. Mech. Dev. 122, 928-938 (Pubitemid 40961553)
42. Hata, A., Lagna, G., Massague, J. and Hemmati-Brivanlou, A. (1998). Smad6 inhibits BMP/Smad1 signaling by specifically competing with the Smad4 tumor suppressor. Genes Dev. 12, 186-197. (Pubitemid 28060449)
43. Heinke, J., Wehofsits, L., Zhou, Q., Zoeller, C., Baar, K. M., Helbing, T., Laib, A., Augustin, H., Bode, C., Patterson, C. et al. (2008). BMPER is an endothelial cell regulator and controls bone morphogenetic protein-4-dependent angiogenesis. Circ. Res. 103, 804-812.
44. Herzer, U., Crocoll, A., Barton, D., Howells, N. and Englert, C. (1999). The Wilms tumor suppressor gene wt1 is required for development of the spleen. Curr. Biol. 9, 837-840. (Pubitemid 29375188)
45. Hino, S., Kishida, S., Michiue, T., Fukui, A., Sakamoto, I., Takada, S., Asashima, M. and Kikuchi, A. (2001). Inhibition of the Wnt signaling pathway by Idax, a novel Dvl-binding protein. Mol. Cell. Biol. 21, 330-342. (Pubitemid 37410588)
46. Holst, C. R., Bou-Reslan, H., Gore, B. B., Wong, K., Grant, D., Chalasani, S., Carano, R. A., Frantz, G. D., Tessier-Lavigne, M., Bolon, B. et al. (2007). Secreted sulfatases Sulf1 and Sulf2 have overlapping yet essential roles in mouse neonatal survival. PLoS One 2, e575. (Pubitemid 351260206)
47. Huang da, W., Sherman, B. T., Tan, Q., Collins, J. R., Alvord, W. G., Roayaei, J., Stephens, R., Baseler, M. W., Lane, H. C. and Lempicki, R. A. (2007). The DAVID Gene Functional Classification Tool: a novel biological module-centric algorithm to functionally analyze large gene lists. Genome Biol. 8, R183. (Pubitemid 351895482)
48. Huber, O., Korn, R., McLaughlin, J., Ohsugi, M., Herrmann, B. G. and Kemler, R. (1996). Nuclear localization of beta-catenin by interaction with transcription factor LEF-1. Mech. Dev. 59, 3-10. (Pubitemid 26325455)
49. Ijpenberg, A., Perez-Pomares, J. M., Guadix, J. A., Carmona, R., Portillo- Sanchez, V., Macias, D., Hohenstein, P., Miles, C. M., Hastie, N. D. and Munoz-Chapuli, R. (2007). Wt1 and retinoic acid signaling are essential for stellate cell development and liver morphogenesis. Dev. Biol. 312, 157-170. (Pubitemid 350180752)
50. Iso, T., Kedes, L. and Hamamori, Y. (2003). HES and HERP families: multiple effectors of the Notch signaling pathway. J. Cell. Physiol. 194, 237-255. (Pubitemid 36176887)
51. Izaguirre, G., Aguirre, L., Hu, Y. P., Lee, H. Y., Schlaepfer, D. D., Aneskievich, B. J. and Haimovich, B. (2001). The cytoskeletal/non-muscle isoform of alphaactinin is phosphorylated on its actin-binding domain by the focal adhesion kinase. J. Biol. Chem. 276, 28676-28685. (Pubitemid 37451942)
52. Jena, N., Martin-Seisdedos, C., McCue, P. and Croce, C. M. (1997). BMP7 null mutation in mice: developmental defects in skeleton, kidney, and eye. Exp. Cell Res. 230, 28-37. (Pubitemid 27187536)
53. Jongstra-Bilen, J., Janmey, P. A., Hartwig, J. H., Galea, S. and Jongstra, J. (1992). The lymphocyte-specific protein LSP1 binds to F-actin and to the cytoskeleton through its COOH-terminal basic domain. J. Cell Biol. 118, 1443-1453.
54. Kang, S., Dong, S., Gu, T. L., Guo, A., Cohen, M. S., Lonial, S., Khoury, H. J., Fabbro, D., Gilliland, D. G., Bergsagel, P. L. et al. (2007). FGFR3 activates RSK2 to mediate hematopoietic transformation through tyrosine phosphorylation of RSK2 and activation of the MEK/ERK pathway. Cancer Cell 12, 201-214. (Pubitemid 47333416)
55. Kang, S., Elf, S., Dong, S., Hitosugi, T., Lythgoe, K., Guo, A., Ruan, H., Lonial, S., Khoury, H. J., Williams, I. R. et al. (2009). Fibroblast growth factor receptor 3 associates with and tyrosine phosphorylates p90 RSK2, leading to RSK2 activation that mediates hematopoietic transformation. Mol. Cell. Biol. 29, 2105-2117.
56. Kazama, I., Mahoney, Z., Miner, J. H., Graf, D., Economides, A. N. and Kreidberg, J. A. (2008). Podocyte-derived BMP7 is critical for nephron development. J. Am. Soc. Nephrol. 19, 2181-2191.
57. Keck, P. J., Hauser, S. D., Krivi, G., Sanzo, K., Warren, T., Feder, J. and Connolly, D. T. (1989). Vascular permeability factor, an endothelial cell mitogen related to PDGF. Science 246, 1309-1312. (Pubitemid 20066717)
58. Keith, B., Adelman, D. M. and Simon, M. C. (2001). Targeted mutation of the murine arylhydrocarbon receptor nuclear translocator 2 (Arnt2) gene reveals partial redundancy with Arnt. Proc. Natl. Acad. Sci. USA 98, 6692-6697. (Pubitemid 32538278)
59. Kim, M. K., McGarry, T. J., O Broin, P., Flatow, J. M., Golden, A. A. and Licht, J. D. (2009). An integrated genome screen identifies the Wnt signaling pathway as a major target of WT1. Proc. Natl. Acad. Sci. USA 106, 11154-11159.
60. Kobayashi, H., Kawakami, K., Asashima, M. and Nishinakamura, R. (2007). Six1 and Six4 are essential for Gdnf expression in the metanephric mesenchyme and ureteric bud formation, while Six1 deficiency alone causes mesonephrictubule defects. Mech. Dev. 124, 290-303. (Pubitemid 46400394)
61. Kobayashi, A., Valerius, M. T., Mugford, J. W., Carroll, T. J., Self, M., Oliver, G. and McMahon, A. P. (2008). Six2 defines and regulates a multipotent self-renewing nephron progenitor population throughout mammalian kidney development. Cell Stem Cell 3, 169-181.
62. Konishi, Y., Ikeda, K., Iwakura, Y. and Kawakami, K. (2006). Six1 and Six4 promote survival of sensory neurons during early trigeminal gangliogenesis. Brain Res. 1116, 93-102. (Pubitemid 44485014)
63. Kozak, K. R., Abbott, B. and Hankinson, O. (1997). ARNT-deficient mice and placental differentiation. Dev. Biol. 191, 297-305.
64. Kreidberg, J. A., Sariola, H., Loring, J. M., Maeda, M., Pelletier, J., Housman, D. and Jaenisch, R. (1993). WT-1 is required for early kidney development. Cell 74, 679-691. (Pubitemid 23259748)
65. Lagna, G., Hata, A., Hemmati-Brivanlou, A. and Massague, J. (1996). Partnership between DPC4 and SMAD proteins in TGF-beta signalling pathways. Nature 383, 832-836. (Pubitemid 26372668)
66. Le, N., Nagarajan, R., Wang, J. Y., Svaren, J., LaPash, C., Araki, T., Schmidt, R. E. and Milbrandt, J. (2005). Nab proteins are essential for peripheral nervous system myelination. Nat. Neurosci. 8, 932-940.
67. Lee, K. F., Simon, H., Chen, H., Bates, B., Hung, M. C. and Hauser, C. (1995). Requirement for neuregulin receptor erbB2 in neural and cardiac development. Nature 378, 394-398.
68. Lee, T. I., Johnstone, S. E. and Young, R. A. (2006). Chromatin immunoprecipitation and microarray-based analysis of protein location. Nat. Protoc. 1, 729-748.
69. Leimeister, C., Schumacher, N. and Gessler, M. (2003). Expression of Notch pathway genes in the embryonic mouse metanephros suggests a role in proximal tubule development. Gene Expr. Patterns 3, 595-598. (Pubitemid 37074912)
70. Leung, D. W., Cachianes, G., Kuang, W. J., Goeddel, D. V. and Ferrara, N. (1989). Vascular endothelial growth factor is a secreted angiogenic mitogen. Science 246, 1306-1309. (Pubitemid 20066716)
71. Levay, A. K., Peacock, J. D., Lu, Y., Koch, M., Hinton, R. B., Jr, Kadler, K. E. and Lincoln, J. (2008). Scleraxis is required for cell lineage differentiation and extracellular matrix remodeling during murine heart valve formation in vivo. Circ. Res. 103, 948-956.
72. Liu, J., Zhang, L., Wang, D., Shen, H., Jiang, M., Mei, P., Hayden, P. S., Sedor, J. R. and Hu, H. (2003). Congenital diaphragmatic hernia, kidney agenesis and cardiac defects associated with Slit3-deficiency in mice. Mech. Dev. 120, 1059-1070. (Pubitemid 37205048)
73. Liu, L., Cara, D. C., Kaur, J., Raharjo, E., Mullaly, S. C., Jongstra-Bilen, J., Jongstra, J. and Kubes, P. (2005). LSP1 is an endothelial gatekeeper of leukocyte transendothelial migration. J. Exp. Med. 201, 409-418. (Pubitemid 40229415)
74. London, T. B., Lee, H. J., Shao, Y. and Zheng, J. (2004). Interaction between the internal motif KTXXXI of Idax and mDvl PDZ domain. Biochem. Biophys. Res. Commun. 322, 326-332. (Pubitemid 39093873)
75. Luo, G., Hofmann, C., Bronckers, A. L., Sohocki, M., Bradley, A. and Karsenty, G. (1995). BMP-7 is an inducer of nephrogenesis, and is also required for eye development and skeletal patterning. Genes Dev. 9, 2808-2820.
76. Lyons, K. M., Hogan, B. L. and Robertson, E. J. (1995). Colocalization of BMP 7 and BMP 2 RNAs suggests that these factors cooperatively mediate tissue interactions during murine development. Mech. Dev. 50, 71-83.
77. Macisaac, K. D., Gordon, D. B., Nekludova, L., Odom, D. T., Schreiber, J., Gifford, D. K., Young, R. A. and Fraenkel, E. (2006). A hypothesis-based approach for identifying the binding specificity of regulatory proteins from chromatin immunoprecipitation data. Bioinformatics 22, 423-429. (Pubitemid 43231416)
78. Marion, R. M., Fortes, P., Beloso, A., Dotti, C. and Ortin, J. (1999). A human sequence homologue of Staufen is an RNA-binding protein that is associated with polysomes and localizes to the rough endoplasmic reticulum. Mol. Cell. Biol. 19, 2212-2219. (Pubitemid 29098279)
79. Matsunaga, E. (1981). Genetics of Wilms' tumor. Hum. Genet. 57, 231-246.
80. Meagher, M. J. and Braun, R. E. (2001). Requirement for the murine zinc finger protein ZFR in perigastrulation growth and survival. Mol. Cell. Biol. 21, 2880-2890.
81. Miller, S. F., Summerhurst, K., Runker, A. E., Kerjan, G., Friedel, R. H., Chedotal, A., Murphy, P. and Mitchell, K. J. (2007). Expression of Plxdc2/TEM7R in the developing nervous system of the mouse. Gene Expr. Patterns 7, 635-644. (Pubitemid 46464648)
82. Mitiku, N. and Baker, J. C. (2007). Genomic analysis of gastrulation and organogenesis in the mouse. Dev. Cell 13, 897-907. (Pubitemid 350163037)
83. Miyazaki, Y., Oshima, K., Fogo, A., Hogan, B. L. and Ichikawa, I. (2000). Bone morphogenetic protein 4 regulates the budding site and elongation of the mouse ureter. J. Clin. Invest. 105, 863-873. (Pubitemid 30203059)
84. Mo, R., Freer, A. M., Zinyk, D. L., Crackower, M. A., Michaud, J., Heng, H. H., Chik, K. W., Shi, X. M., Tsui, L. C., Cheng, S. H. et al. (1997). Specific and redundant functions of Gli2 and Gli3 zinc finger genes in skeletal patterning and development. Development 124, 113-123. (Pubitemid 27053011)
85. Moore, A. W., Schedl, A., McInnes, L., Doyle, M., Hecksher-Sorensen, J. and Hastie, N. D. (1998). YAC transgenic analysis reveals Wilms' tumour 1 gene activity in the proliferating coelomic epithelium, developing diaphragm and limb. Mech. Dev. 79, 169-184. (Pubitemid 29038033)
86. Moore, A. W., McInnes, L., Kreidberg, J., Hastie, N. D. and Schedl, A. (1999). YAC complementation shows a requirement for Wt1 in the development of epicardium, adrenal gland and throughout nephrogenesis. Development 126, 1845-1857. (Pubitemid 29240319)
87. Muir, T., Sadler-Riggleman, I. and Skinner, M. K. (2005). Role of the basic helixloop-helix transcription factor, scleraxis, in the regulation of Sertoli cell function and differentiation. Mol. Endocrinol. 19, 2164-2174. (Pubitemid 41124210)
88. Mundlos, S., Pelletier, J., Darveau, A., Bachmann, M., Winterpacht, A. and Zabel, B. (1993). Nuclear localization of the protein encoded by the Wilms' tumor gene WT1 in embryonic and adult tissues. Development 119, 1329-1341. (Pubitemid 23358597)
89. Murone, M., Rosenthal, A. and de Sauvage, F. J. (1999). Sonic hedgehog signaling by the patched-smoothened receptor complex. Curr. Biol. 9, 76-84. (Pubitemid 29083531)
90. Nakagama, H., Heinrich, G., Pelletier, J. and Housman, D. E. (1995). Sequence and structural requirements for high-affinity DNA binding by the WT1 gene product. Mol. Cell. Biol. 15, 1489-1498.
91. Nakao, A., Afrakhte, M., Moren, A., Nakayama, T., Christian, J. L., Heuchel, R., Itoh, S., Kawabata, M., Heldin, N. E., Heldin, C. H. et al. (1997). Identification of Smad7, a TGFbeta-inducible antagonist of TGF-beta signalling. Nature 389, 631-635. (Pubitemid 27446184)
92. Nishinakamura, R., Matsumoto, Y., Nakao, K., Nakamura, K., Sato, A., Copeland, N. G., Gilbert, D. J., Jenkins, N. A., Scully, S., Lacey, D. L. et al. (2001). Murine homolog of SALL1 is essential for ureteric bud invasion in kidney development. Development 128, 3105-3115. (Pubitemid 32825755)
93. Pal, C. and Hurst, L. D. (2000). The evolution of gene number: are heritable and non-heritable errors equally important? Heredity 84, 393-400. (Pubitemid 30400025)
94. Pavletich, N. P. and Pabo, C. O. (1993). Crystal structure of a five-finger GLI-DNA complex: new perspectives on zinc fingers. Science 261, 1701-1707.
95. Pelletier, J., Schalling, M., Buckler, A. J., Rogers, A., Haber, D. A. and Housman, D. (1991). Expression of the Wilms' tumor gene WT1 in the murine urogenital system. Genes Dev. 5, 1345-1356. (Pubitemid 21906043)
96. Pendino, F., Nguyen, E., Jonassen, I., Dysvik, B., Azouz, A., Lanotte, M., Segal-Bendirdjian, E. and Lillehaug, J. R. (2009). Functional involvement of RINF, retinoid-inducible nuclear factor (CXXC5), in normal and tumoral human myelopoiesis. Blood 113, 3172-3181.
97. Piscione, T. D., Phan, T. and Rosenblum, N. D. (2001). BMP7 controls collecting tubule cell proliferation and apoptosis via Smad1-dependent and -independent pathways. Am. J. Physiol. Renal Physiol. 280, F19-F33. (Pubitemid 32473293)
98. Poladia, D. P., Kish, K., Kutay, B., Hains, D., Kegg, H., Zhao, H. and Bates, C. M. (2006). Role of fibroblast growth factor receptors 1 and 2 in the metanephric mesenchyme. Dev. Biol. 291, 325-339.
99. Pritchard-Jones, K., Fleming, S., Davidson, D., Bickmore, W., Porteous, D., Gosden, C., Bard, J., Buckler, A., Pelletier, J., Housman, D. et al. (1990). The candidate Wilms' tumour gene is involved in genitourinary development. Nature 346, 194-197. (Pubitemid 20221639)
100. Rauscher, F. J., 3rd, Morris, J. F., Tournay, O. E., Cook, D. M. and Curran, T. (1990). Binding of the Wilms' tumor locus zinc finger protein to the EGR-1 consensus sequence. Science 250, 1259-1262.
101. Reddy, J. C., Hosono, S. and Licht, J. D. (1995). The transcriptional effect of WT1 is modulated by choice of expression vector. J. Biol. Chem. 270, 29976-29982. (Pubitemid 26001673)
102. Rothenpieler, U. W. and Dressler, G. R. (1993). Pax-2 is required for mesenchyme-to-epithelium conversion during kidney development. Development 119, 711-720.
103. Ryan, G., Steele-Perkins, V., Morris, J. F., Rauscher, F. J., 3rd and Dressler, G. R. (1995). Repression of Pax-2 by WT1 during normal kidney development. Development 121, 867-875.
104. Scharnhorst, V., van der Eb, A. J. and Jochemsen, A. G. (2001). WT1 proteins: functions in growth and differentiation. Gene 273, 141-161. (Pubitemid 32786908)
105. Schnabel, C. A., Godin, R. E. and Cleary, M. L. (2003). Pbx1 regulates nephrogenesis and ureteric branching in the developing kidney. Dev. Biol. 254, 262-276.
106. Scholz, H., Wagner, K. D. and Wagner, N. (2009). Role of the Wilms' tumour transcription factor, Wt1, in blood vessel formation. Pflugers Arch. 458, 315-323.
107. Schwabe, J. W., Fairall, L., Chapman, L., Finch, J. T., Dutnall, R. N. and Rhodes, D. (1993). The cocrystal structures of two zinc-stabilized DNA-binding domains illustrate different ways of achieving sequence-specific DNA recognition. Cold Spring Harb. Symp. Quant. Biol. 58, 141-147. (Pubitemid 24219473)
108. Self, M., Lagutin, O. V., Bowling, B., Hendrix, J., Cai, Y., Dressler, G. R. and Oliver, G. (2006). Six2 is required for suppression of nephrogenesis and progenitor renewal in the developing kidney. EMBO J. 25, 5214-5228. (Pubitemid 44658538)
109. Sock, E., Rettig, S. D., Enderich, J., Bosl, M. R., Tamm, E. R. and Wegner, M. (2004). Gene targeting reveals a widespread role for the high-mobility-group transcription factor Sox11 in tissue remodeling. Mol. Cell. Biol. 24, 6635-6644. (Pubitemid 38944343)
110. Steidl, C., Leimeister, C., Klamt, B., Maier, M., Nanda, I., Dixon, M., Clarke, R., Schmid, M. and Gessler, M. (2000). Characterization of the human and mouse HEY1, HEY2, and HEYL genes: cloning, mapping, and mutation screening of a new bHLH gene family. Genomics 66, 195-203. (Pubitemid 30429754)
111. Stone, D. M., Hynes, M., Armanini, M., Swanson, T. A., Gu, Q., Johnson, R. L., Scott, M. P., Pennica, D., Goddard, A., Phillips, H. et al. (1996). The tumour-suppressor gene patched encodes a candidate receptor for Sonic hedgehog. Nature 384, 129-134. (Pubitemid 26386461)
112. Taketomi, T., Yoshiga, D., Taniguchi, K., Kobayashi, T., Nonami, A., Kato, R., Sasaki, M., Sasaki, A., Ishibashi, H., Moriyama, M. et al. (2005). Loss of mammalian Sprouty2 leads to enteric neuronal hyperplasia and esophageal achalasia. Nat. Neurosci. 8, 855-857.
113. Tang, X., Feng, Y. and Ye, K. (2007). Src-family tyrosine kinase fyn phosphorylates phosphatidylinositol 3-kinase enhancer-activating Akt, preventing its apoptotic cleavage and promoting cell survival. Cell Death Differ. 14, 368-377. (Pubitemid 46092239)
114. Taniguchi, K., Ayada, T., Ichiyama, K., Kohno, R., Yonemitsu, Y., Minami, Y., Kikuchi, A., Maehara, Y. and Yoshimura, A. (2007). Sprouty2 and Sprouty4 are essential for embryonic morphogenesis and regulation of FGF signaling. Biochem. Biophys. Res. Commun. 352, 896-902. (Pubitemid 44895609)
115. Thate, C., Englert, C. and Gessler, M. (1998). Analysis of WT1 target gene expression in stably transfected cell lines. Oncogene 17, 1287-1294. (Pubitemid 28446169)
116. Torres, M., Gomez-Pardo, E. and Gruss, P. (1996). Pax2 contributes to inner ear patterning and optic nerve trajectory. Development 122, 3381-3391. (Pubitemid 26395981)
117. Toyofuku, T., Zhang, H., Kumanogoh, A., Takegahara, N., Suto, F., Kamei, J., Aoki, K., Yabuki, M., Hori, M., Fujisawa, H. et al. (2004a). Dual roles of Sema6D in cardiac morphogenesis through region-specific association of its receptor, Plexin-A1, with off-track and vascular endothelial growth factor receptor type 2. Genes Dev. 18, 435-447. (Pubitemid 38316350)
118. Toyofuku, T., Zhang, H., Kumanogoh, A., Takegahara, N., Yabuki, M., Harada, K., Hori, M. and Kikutani, H. (2004b). Guidance of myocardial patterning in cardiac development by Sema6D reverse signalling. Nat. Cell Biol. 6, 1204-1211. (Pubitemid 39625119)
119. Vokes, S. A., Ji, H., McCuine, S., Tenzen, T., Giles, S., Zhong, S., Longabaugh, W. J., Davidson, E. H., Wong, W. H. and McMahon, A. P. (2007). Genomic characterization of Gli-activator targets in sonic hedgehog-mediated neural patterning. Development 134, 1977-1989. (Pubitemid 46939242)
120. Wagner, K. D., Wagner, N., Vidal, V. P., Schley, G., Wilhelm, D., Schedl, A., Englert, C. and Scholz, H. (2002). The Wilms' tumor gene Wt1 is required for normal development of the retina. EMBO J. 21, 1398-1405. (Pubitemid 34246518)
121. Wagner, N., Wagner, K. D., Hammes, A., Kirschner, K. M., Vidal, V. P., Schedl, A. and Scholz, H. (2005). A splice variant of the Wilms' tumour suppressor Wt1 is required for normal development of the olfactory system. Development 132, 1327-1336. (Pubitemid 40528792)
122. Watson, A. J. and Barcroft, L. C. (2001). Regulation of blastocyst formation. Front. Biosci. 6, D708-D730.
123. Wellik, D. M. (2009). Hox genes and vertebrate axial pattern. Curr. Top. Dev. Biol. 88, 257-278.
124. Wu, R. Y., Zhang, Y., Feng, X. H. and Derynck, R. (1997). Heteromeric and homomeric interactions correlate with signaling activity and functional cooperativity of Smad3 and Smad4/DPC4. Mol. Cell. Biol. 17, 2521-2528. (Pubitemid 27175133)
125. Wurm, A., Sock, E., Fuchshofer, R., Wegner, M. and Tamm, E. R. (2008). Anterior segment dysgenesis in the eyes of mice deficient for the high-mobility-group transcription factor Sox11. Exp. Eye Res. 86, 895-907.
126. Xu, X., Weinstein, M., Li, C., Naski, M., Cohen, R. I., Ornitz, D. M., Leder, P. and Deng, C. (1998). Fibroblast growth factor receptor 2 (FGFR2)-mediated reciprocal regulation loop between FGF8 and FGF10 is essential for limb induction. Development 125, 753-765. (Pubitemid 28108099)
127. Zhang, X., Xing, G. and Saunders, G. F. (1999). Proto-oncogene N-myc promoter is down regulated by the Wilms' tumor suppressor gene WT1. Anticancer Res. 19, 1641-1648. (Pubitemid 29392717)
128. Zhang, Y., Feng, X., We, R. and Derynck, R. (1996). Receptor-associated Mad homologues synergize as effectors of the TGF-beta response. Nature 383, 168-172. (Pubitemid 26303979)
129. Zhao, H., Kegg, H., Grady, S., Truong, H. T., Robinson, M. L., Baum, M. and Bates, C. M. (2004). Role of fibroblast growth factor receptors 1 and 2 in the ureteric bud. Dev. Biol. 276, 403-415. (Pubitemid 39592403)