Sall1-dependent signals affect Wnt signaling and ureter tip fate to initiate kidney development

Development

Volumn 137, Issue 18, 2010, Pages 3099-3106

  Kiefer, Susan M ^a,b,c   Robbins, Lynn ^a,b,c   Stumpff, Kelly M ^a,b,c   Lin, Congxing ^a,b,c   Ma, Liang ^a,b,c   Rauchman, Michael ^a,b,c  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Kidney development; Metanephric mesenchyme; Mouse; Sall1; Spalt; Tip fate; Ureter; Ureteric bud; Wnt; Wnt9b; catenin

Indexed keywords

BETA CATENIN; PROTEIN RET; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SALL1; UNCLASSIFIED DRUG; WNT PROTEIN; WNT11 PROTEIN; WNT9B PROTEIN; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; SALL1 PROTEIN, MOUSE; WNT9B PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; KIDNEY DEVELOPMENT; MALE; MESENCHYME; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION; URETER; ANIMAL; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETICS; KIDNEY; METABOLISM; MORPHOGENESIS; SIGNAL TRANSDUCTION;

ANIMALS; BETA CATENIN; BODY PATTERNING; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR; KIDNEY; MALE; MICE; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; URETER; WNT PROTEINS;

EID: 77956590347     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.037812     Document Type: Article

References (50)

1. Basson, M. A., Akbulut, S., Watson-Johnson, J., Simon, R., Carroll, T. J., Shakya, R., Gross, I., Martin, G. R., Lufkin, T., McMahon, A. P. et al. (2005). Sprouty1 is a critical regulator of GDNF/RET-mediated kidney induction. Dev. Cell 8, 229-239.
2. Basson, M. A., Watson-Johnson, J., Shakya, R., Akbulut, S., Hyink, D., Costantini, F. D., Wilson, P. D., Mason, I. J. and Licht, J. D. (2006). Branching morphogenesis of the ureteric epithelium during kidney development is coordinated by the opposing functions of GDNF and Sprouty1. Dev. Biol. 299, 466-477.
3. Bohm, J., Sustmann, C., Wilhelm, C. and Kohlhase, J. (2006). SALL4 is directly activated by TCF/LEF in the canonical Wnt signaling pathway. Biochem. Biophys. Res. Commun. 348, 898-907.
4. Bridgewater, D., Cox, B., Cain, J., Lau, A., Athaide, V., Gill, P. S., Kuure, S., Sainio, K. and Rosenblum, N. D. (2008). Canonical WNT/beta-catenin signaling is required for ureteric branching. Dev. Biol. 317, 83-94.
5. Bush, K. T., Vaughn, D. A., Li, X., Rosenfeld, M. G., Rose, D. W., Mendoza, S. A. and Nigam, S. K. (2006). Development and differentiation of the ureteric bud into the ureter in the absence of a kidney collecting system. Dev. Biol. 298, 571-584.
6. Carroll, T. J., Park, J. S., Hayashi, S., Majumdar, A. and McMahon, A. P. (2005). Wnt9b plays a central role in the regulation of mesenchymal to epithelial transitions underlying organogenesis of the mammalian urogenital system. Dev. Cell 9, 283-292.
7. Caruana, G., Cullen-McEwen, L., Nelson, A. L., Kostoulias, X., Woods, K., Gardiner, B., Davis, M. J., Taylor, D. F., Teasdale, R. D., Grimmond, S. M. et al. (2006). Spatial gene expression in the T-stage mouse metanephros. Gene Expr. Patterns 6, 807-825. (Pubitemid 44309434)
8. Chai, L., Yang, J., Di, C., Cui, W., Kawakami, K., Lai, R. and Ma, Y. (2006). Transcriptional activation of the SALL1 by the human SIX1 homeodomain during kidney development. J. Biol. Chem. 281, 18918-18926.
9. Chen, Y. X., Krull, C. E. and Reneker, L. W. (2004). Targeted gene expression in the chicken eye by in ovo electroporation. Mol. Vis. 10, 874-883.
10. Chihara, T. and Hayashi, S. (2000). Control of tracheal tubulogenesis by Wingless signaling. Development 127, 4433-4442.
11. Costantini, F. (2006). Renal branching morphogenesis: concepts, questions, and recent advances. Differentiation 74, 402-421.
12. 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.
13. Harada, N., Tamai, Y., Ishikawa, T., Sauer, B., Takaku, K., Oshima, M. and Taketo, M. M. (1999). Intestinal polyposis in mice with a dominant stable mutation of the beta-catenin gene. EMBO J. 18, 5931-5942.
14. Iglesias, D. M., Hueber, P. A., Chu, L., Campbell, R., Patenaude, A. M., Dziarmaga, A. J., Quinlan, J., Mohamed, O., Dufort, D. and Goodyer, P. R. (2007). Canonical WNT signaling during kidney development. Am. J. Physiol. Renal Physiol. 293, F494-F500.
15. Jain, S., Encinas, M., Johnson, E. M., Jr and Milbrandt, J. (2006). Critical and distinct roles for key RET tyrosine docking sites in renal development. Genes Dev. 20, 321-333.
16. Jho, E. H., Zhang, T., Domon, C., Joo, C. K., Freund, J. N. and Costantini, F. (2002). Wnt/beta-catenin/Tcf signaling induces the transcription of Axin2, a negative regulator of the signaling pathway. Mol. Cell. Biol. 22, 1172-1183.
17. Karner, C. M., Dietrich, M. F., Johnson, E. B., Kappesser, N., Tennert, C., Percin, F., Wollnik, B., Carroll, T. J. and Herz, J. (2010). Lrp4 regulates initiation of ureteric budding and is crucial for kidney formation-a mouse model for Cenani-Lenz syndrome. PLoS ONE 5, e10418.
18. Kiefer, S. M., McDill, B. W., Yang, J. and Rauchman, M. (2002). Murine Sall1 represses transcription by recruiting a histone deacetylase complex. J. Biol. Chem. 277, 14869-14876.
19. Kiefer, S. M., Ohlemiller, K. K., Yang, J., McDill, B. W., Kohlhase, J. and Rauchman, M. (2003). Expression of a truncated Sall1 transcriptional repressor is responsible for Townes-Brocks syndrome birth defects. Hum. Mol. Genet. 12, 2221-2227.
20. Kiefer, S. M., Robbins, L., Barina, A., Zhang, Z. and Rauchman, M. (2008). SALL1 truncated protein expression in Townes-Brocks syndrome leads to ectopic expression of downstream genes. Hum. Mutat. 29, 1133-1140.
21. Kuure, S., Popsueva, A., Jakobson, M., Sainio, K. and Sariola, H. (2007). Glycogen synthase kinase-3 inactivation and stabilization of beta-catenin induce nephron differentiation in isolated mouse and rat kidney mesenchymes. J. Am. Soc. Nephrol. 18, 1130-1139.
22. Lauberth, S. M. and Rauchman, M. (2006). A conserved 12-amino acid motif in Sall1 recruits the nucleosome remodeling and deacetylase corepressor complex. J. Biol. Chem. 281, 23922-23931.
23. Linton, J. M., Martin, G. R. and Reichardt, L. F. (2007). The ECM protein nephronectin promotes kidney development via integrin α8β1-mediated stimulation of Gdnf expression. Development 134, 2501-2509.
24. Little, M. H., Brennan, J., Georgas, K., Davies, J. A., Davidson, D. R., Baldock, R. A., Beverdam, A., Bertram, J. F., Capel, B., Chiu, H. S. et al. (2007). A high-resolution anatomical ontology of the developing murine genitourinary tract. Gene Expr. Patterns 7, 680-699.
25. Ma, Y., Cui, W., Yang, J., Qu, J., Di, C., Amin, H. M., Lai, R., Ritz, J., Krause, D. S. and Chai, L. (2006). SALL4, a novel oncogene, is constitutively expressed in human acute myeloid leukemia (AML) and induces AML in transgenic mice. Blood 108, 2726-2735.
26. Mahoney, Z. X., Sammut, B., Xavier, R. J., Cunningham, J., Go, G., Brim, K. L., Stappenbeck, T. S., Miner, J. H. and Swat, W. (2006). Discs-large homolog 1 regulates smooth muscle orientation in the mouse ureter. Proc. Natl. Acad. Sci. USA 103, 19872-19877.
27. Majumdar, A., Vainio, S., Kispert, A., McMahon, J. and McMahon, A. P. (2003). Wnt11 and Ret/Gdnf pathways cooperate in regulating ureteric branching during metanephric kidney development. Development 130, 3175-3185.
28. Marose, T. D., Merkel, C. E., McMahon, A. P. and Carroll, T. J. (2008). Beta-catenin is necessary to keep cells of ureteric bud/Wolffian duct epithelium in a precursor state. Dev. Biol. 314, 112-126.
29. Michael, L. and Davies, J. A. (2004). Pattern and regulation of cell proliferation during murine ureteric bud development. J. Anat. 204, 241-255.
30. Michos, O., Goncalves, A., Lopez-Rios, J., Tiecke, E., Naillat, F., Beier, K., Galli, A., Vainio, S. and Zeller, R. (2007). Reduction of BMP4 activity by gremlin 1 enables ureteric bud outgrowth and GDNF/WNT11 feedback signalling during kidney branching morphogenesis. Development 134, 2397-2405.
31. Mugford, J. W., Yu, J., Kobayashi, A. and McMahon, A. P. (2009). High-resolution gene expression analysis of the developing mouse kidney defines novel cellular compartments within the nephron progenitor population. Dev. Biol. 333, 312-323.
32. Nie, X., Sun, J., Gordon, R. E., Cai, C. L. and Xu, P. X. (2010). SIX1 acts synergistically with TBX18 in mediating ureteral smooth muscle formation. Development 137, 755-765.
33. 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.
34. Novak, A., Guo, C., Yang, W., Nagy, A. and Lobe, C. G. (2000). Z/EG, a double reporter mouse line that expresses enhanced green fluorescent protein upon Cre-mediated excision. Genesis 28, 147-155.
35. Onai, T., Sasai, N., Matsui, M. and Sasai, Y. (2004). Xenopus XsalF: anterior neuroectodermal specification by attenuating cellular responsiveness to Wnt signaling. Dev. Cell 7, 95-106.
36. Osafune, K., Takasato, M., Kispert, A., Asashima, M. and Nishinakamura, R. (2006). Identification of multipotent progenitors in the embryonic mouse kidney by a novel colony-forming assay. Development 133, 151-161.
37. Park, J. S., Valerius, M. T. and McMahon, A. P. (2007). Wnt/β-catenin signaling regulates nephron induction during mouse kidney development. Development 134, 2533-2539.
38. Ribeiro, C., Neumann, M. and Affolter, M. (2004). Genetic control of cell intercalation during tracheal morphogenesis in Drosophila. Curr. Biol. 14, 2197-2207.
39. Sato, A., Kishida, S., Tanaka, T., Kikuchi, A., Kodama, T., Asashima, M. and Nishinakamura, R. (2004). Sall1, a causative gene for Townes-Brocks syndrome, enhances the canonical Wnt signaling by localizing to heterochromatin. Biochem. Biophys. Res. Commun. 319, 103-113.
40. Schedl, A. (2007). Renal abnormalities and their developmental origin. Nat. Rev. Genet. 8, 791-802.
41. Schmidt-Ott, K. M., Yang, J., Chen, X., Wang, H., Paragas, N., Mori, K., Li, J. Y., Lu, B., Costantini, F., Schiffer, M. et al. (2005). Novel regulators of kidney development from the tips of the ureteric bud. J. Am. Soc. Nephrol. 16, 1993-2002.
42. Schmidt-Ott, K. M., Masckauchan, T. N., Chen, X., Hirsh, B. J., Sarkar, A., Yang, J., Paragas, N., Wallace, V. A., Dufort, D., Pavlidis, P. et al. (2007). β-catenin/TCF/Lef controls a differentiation-associated transcriptional program in renal epithelial progenitors. Development 134, 3177-3190.
43. Schuchardt, A., D'Agati, V., Larsson-Blomberg, L., Costantini, F. and Pachnis, V. (1995). RET-deficient mice: an animal model for Hirschsprung's disease and renal agenesis. J. Intern. Med. 238, 327-332.
44. Schuchardt, A., D'Agati, V., Pachnis, V. and Costantini, F. (1996). Renal agenesis and hypodysplasia in ret-k- mutant mice result from defects in ureteric bud development. Development 122, 1919-1929.
45. Shakya, R., Watanabe, T. and Costantini, F. (2005). The role of GDNF/Ret signaling in ureteric bud cell fate and branching morphogenesis. Dev. Cell 8, 65-74.
46. Srinivas, S., Wu, Z., Chen, C. M., D'Agati, V. and Costantini, F. (1999). Dominant effects of RET receptor misexpression and ligand-independent RET signaling on ureteric bud development. Development 126, 1375-1386.
47. Sweeney, D., Lindstrom, N. and Davies, J. A. (2008). Developmental plasticity and regenerative capacity in the renal ureteric bud/collecting duct system. Development 135, 2505-2510.
48. Uchiyama, Y., Sakaguchi, M., Terabayashi, T., Inenaga, T., Inoue, S., Kobayashi, C., Oshima, N., Kiyonari, H., Nakagata, N., Sato, Y. et al. (2010). Kif26b, a kinesin family gene, regulates adhesion of the embryonic kidney mesenchyme. Proc. Natl. Acad. Sci. USA 107, 9240-9245.
49. Uez, N., Lickert, H., Kohlhase, J., de Angelis, M. H., Kuhn, R., Wurst, W. and Floss, T. (2008). Sall4 isoforms act during proximal-distal and anterior-posterior axis formation in the mouse embryo. Genesis 46, 463-477.
50. 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.