p120 catenin is required for normal renal tubulogenesis and glomerulogenesis

Development

Volumn 138, Issue 10, 2011, Pages 2099-2109

  Marciano, Denise K ^a,b,d   Brakeman, Paul R ^a   Lee, Chao Zong ^a   Spivak, Natalie ^a   Eastburn, Dennis J ^a   Bryant, David M ^a   Beaudoin III, Gerard M ^b   Hofmann, Ilse ^c   Mostov, Keith E ^a   Reichardt, Louis F ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Cadherins; Glomerulogenesis; Kidney development; Mouse; p120 catenin; Polycystic disease

Indexed keywords

CADHERIN; CATENIN; P120 CATENIN; PROTEIN P120; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG; UVOMORULIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; FEMALE; GENE DELETION; GENE SILENCING; GLOMERULUS; KIDNEY DEVELOPMENT; KIDNEY INTERSTITIUM; KIDNEY POLYCYSTIC DISEASE; KIDNEY TUBULE; MALE; MOUSE; NEPHRON; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; ARMADILLO DOMAIN PROTEINS; BASE SEQUENCE; CADHERINS; CATENINS; CELL ADHESION MOLECULES; CELL LINE; CELL POLARITY; CELL PROLIFERATION; CYTOSKELETON; DOGS; FEMALE; GENE KNOCKDOWN TECHNIQUES; KIDNEY DISEASES, CYSTIC; KIDNEY GLOMERULUS; KIDNEY TUBULES; MALE; MICE; MICE, KNOCKOUT; MODELS, BIOLOGICAL; MORPHOGENESIS; NEPHRONS; PHENOTYPE; PHOSPHOPROTEINS; PREGNANCY; RHO GTP-BINDING PROTEINS; RNA, SMALL INTERFERING;

MUS;

EID: 79955553393     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.056564     Document Type: Article

References (59)

1. Aho, S., Levansuo, L., Montonen, O., Kari, C., Rodeck, U. and Uitto, J. (2002). Specific sequences in p120ctn determine subcellular distribution of its multiple isoforms involved in cellular adhesion of normal and malignant epithelial cells. J. Cell Sci. 115, 1391-1402.
2. Anastasiadis, P. Z., Moon, S. Y., Thoreson, M. A., Mariner, D. J., Crawford, H. C., Zheng, Y. and Reynolds, A. B. (2000). Inhibition of RhoA by p120 catenin. Nat. Cell Biol. 2, 637-644.
3. Boguslavsky, S., Grosheva, I., Landau, E., Shtutman, M., Cohen, M., Arnold, K., Feinstein, E., Geiger, B. and Bershadsky, A. (2007). p120 catenin regulates lamellipodial dynamics and cell adhesion in cooperation with cortactin. Proc. Natl. Acad. Sci. USA 104, 10882-10887.
4. Brakeman, P. R., Liu, K. D., Shimizu, K., Takai, Y. and Mostov, K. E. (2009). Nectin proteins are expressed at early stages of nephrogenesis and play a role in renal epithelial cell morphogenesis. Am. J. Physiol. Renal Physiol. 296, F564-F574.
5. Bryant, D. M., Datta, A., Rodriguez-Fraticelli, A. E., Peranen, J., Martin-Belmonte, F. and Mostov, K. E. (2010). A molecular network for de novo generation of the apical surface and lumen. Nat. Cell Biol. 12, 1035-1045.
6. Capaldo, C. T. and Macara, I. G. (2007). Depletion of E-cadherin disrupts establishment but not maintenance of cell junctions in Madin-Darby canine kidney epithelial cells. Mol. Biol. Cell 18, 189-200.
7. Cheng, H. T., Kim, M., Valerius, M. T., Surendran, K., Schuster-Gossler, K., Gossler, A., McMahon, A. P. and Kopan, R. (2007). Notch2, but not Notch1, is required for proximal fate acquisition in the mammalian nephron. Development 134, 801-811.
8. Chiasson, C. M., Wittich, K. B., Vincent, P. A., Faundez, V. and Kowalczyk, A. P. (2009). p120-catenin inhibits VE-cadherin internalization through a Rhoindependent mechanism. Mol. Biol. Cell 20, 1970-1980.
9. Cho, E. A. and Dressler, G. R. (2003). Formation and development of nephrons. In The Kidney: From Normal Development to Congenital Disease (ed. P. D. Vize, A. S. Woolf and J. Bard), pp. 195-208. Amsterdam and Boston: Academic Press.
10. Cho, E. A., Patterson, L. T., Brookhiser, W. T., Mah, S., Kintner, C. and Dressler, G. R. (1998). Differential expression and function of cadherin-6 during renal epithelium development. Development 125, 803-812.
11. Ciesiolka, M., Delvaeye, M., Van Imschoot, G., Verschuere, V., McCrea, P., van Roy, F. and Vleminckx, K. (2004). p120 catenin is required for morphogenetic movements involved in the formation of the eyes and the craniofacial skeleton in Xenopus. J. Cell Sci. 117, 4325-4339.
12. Dahl, U., Sjodin, A., Larue, L., Radice, G. L., Cajander, S., Takeichi, M., Kemler, R. and Semb, H. (2002). Genetic dissection of cadherin function during nephrogenesis. Mol. Cell. Biol. 22, 1474-1487.
13. Davis, M. A. and Reynolds, A. B. (2006). Blocked acinar development, Ecadherin reduction, and intraepithelial neoplasia upon ablation of p120-catenin in the mouse salivary gland. Dev. Cell 10, 21-31.
14. Davis, M. A., Ireton, R. C. and Reynolds, A. B. (2003). A core function for p120-catenin in cadherin turnover. J. Cell Biol. 163, 525-534.
15. Dressler, G. R. (2009). Advances in early kidney specification, development and patterning. Development 136, 3863-3874.
16. Duguay, D., Foty, R. A. and Steinberg, M. S. (2003). Cadherin-mediated cell adhesion and tissue segregation: qualitative and quantitative determinants. Dev. Biol. 253, 309-323.
17. Elia, L. P., Yamamoto, M., Zang, K. and Reichardt, L. F. (2006). p120 catenin regulates dendritic spine and synapse development through Rho-family GTPases and cadherins. Neuron 51, 43-56.
18. Fang, X., Ji, H., Kim, S. W., Park, J. I., Vaught, T. G., Anastasiadis, P. Z., Ciesiolka, M. and McCrea, P. D. (2004). Vertebrate development requires ARVCF and p120 catenins and their interplay with RhoA and Rac. J. Cell Biol. 165, 87-98.
19. Golenhofen, N. and Drenckhahn, D. (2000). The catenin, p120ctn, is a common membrane-associated protein in various epithelial and non-epithelial cells and tissues. Histochem. Cell Biol. 114, 147-155.
20. Goto, S., Yaoita, E., Matsunami, H., Kondo, D., Yamamoto, T., Kawasaki, K., Arakawa, M. and Kihara, I. (1998). Involvement of R-cadherin in the early stage of glomerulogenesis. J. Am. Soc. Nephrol. 9, 1234-1241.
21. Grieshammer, U., Cebrian, C., Ilagan, R., Meyers, E., Herzlinger, D. and Martin, G. R. (2005). FGF8 is required for cell survival at distinct stages of nephrogenesis and for regulation of gene expression in nascent nephrons. Development 132, 3847-3857.
22. Gumbiner, B. M. (2005). Regulation of cadherin-mediated adhesion in morphogenesis. Nat. Rev. Mol. Cell Biol. 6, 622-634.
23. Halbleib, J. M. and Nelson, W. J. (2006). Cadherins in development: cell adhesion, sorting, and tissue morphogenesis. Genes Dev. 20, 3199-3214.
24. Happe, H., Leonhard, W. N., van der Wal, A., van de Water, B., Lantinga-van Leeuwen, I. S., Breuning, M. H., de Heer, E. and Peters, D. J. (2009). Toxic tubular injury in kidneys from Pkd1-deletion mice accelerates cystogenesis accompanied by dysregulated planar cell polarity and canonical Wnt signaling pathways. Hum. Mol. Genet. 18, 2532-2542.
25. Harris, P. C. (2009). 2008 Homer W. Smith award: insights into the pathogenesis of polycystic kidney disease from gene discovery. J. Am. Soc. Nephrol. 20, 1188-1198.
26. Inoue, T., Tanaka, T., Takeichi, M., Chisaka, O., Nakamura, S. and Osumi, N. (2001). Role of cadherins in maintaining the compartment boundary between the cortex and striatum during development. Development 128, 561-569.
27. Karner, C. M., Chirumamilla, R., Aoki, S., Igarashi, P., Wallingford, J. B. and Carroll, T. J. (2009). Wnt9b signaling regulates planar cell polarity and kidney tubule morphogenesis. Nat. Genet. 41, 793-799.
28. Keirsebilck, A., Bonne, S., Staes, K., van Hengel, J., Nollet, F., Reynolds, A. and van Roy, F. (1998). Molecular cloning of the human p120ctn catenin gene (CTNND1): expression of multiple alternatively spliced isoforms. Genomics 50, 129-146.
29. Li, J., Chen, F. and Epstein, J. A. (2000). Neural crest expression of Cre recombinase directed by the proximal Pax3 promoter in transgenic mice. Genesis 26, 162-164.
30. Liu, Y., Dong, Q. Z., Zhao, Y., Dong, X. J., Miao, Y., Dai, S. D., Yang, Z. Q., Zhang, D., Wang, Y., Li, Q. C. et al. (2009). P120-catenin isoforms 1A and 3A differently affect invasion and proliferation of lung cancer cells. Exp. Cell Res. 315, 890-898.
31. Mah, S. P., Saueressig, H., Goulding, M., Kintner, C. and Dressler, G. R. (2000). Kidney development in cadherin-6 mutants: delayed mesenchyme-toepithelial conversion and loss of nephrons. Dev. Biol. 223, 38-53.
32. McCrea, P. D. and Park, J. I. (2007). Developmental functions of the P120-catenin sub-family. Biochim. Biophys. Acta 1773, 17-33.
33. Meyer, T. N., Schwesinger, C., Sampogna, R. V., Vaughn, D. A., Stuart, R. O., Steer, D. L., Bush, K. T. and Nigam, S. K. (2006). Rho kinase acts at separate steps in ureteric bud and metanephric mesenchyme morphogenesis during kidney development. Differentiation 74, 638-647.
34. Michael, L., Sweeney, D. E. and Davies, J. A. (2005). A role for microfilamentbased contraction in branching morphogenesis of the ureteric bud. Kidney Int. 68, 2010-2018.
35. Mo, Y. Y. and Reynolds, A. B. (1996). Identification of murine p120 isoforms and heterogeneous expression of p120cas isoforms in human tumor cell lines. Cancer Res. 56, 2633-2640.
36. Montonen, O., Aho, M., Uitto, J. and Aho, S. (2001). Tissue distribution and cell type-specific expression of p120ctn isoforms. J. Histochem. Cytochem. 49, 1487-1496.
37. Noren, N. K., Liu, B. P., Burridge, K. and Kreft, B. (2000). p120 catenin regulates the actin cytoskeleton via Rho family GTPases. J. Cell Biol. 150, 567-580.
38. Oas, R. G., Xiao, K., Summers, S., Wittich, K. B., Chiasson, C. M., Martin, W. D., Grossniklaus, H. E., Vincent, P. A., Reynolds, A. B. and Kowalczyk, A. P. (2010). p120-catenin is required for mouse vascular development. Circ. Res. 106, 941-951.
39. Ohkubo, T. and Ozawa, M. (2004). The transcription factor Snail downregulates the tight junction components independently of E-cadherin downregulation. J. Cell Sci. 117, 1675-1685.
40. Park, J. S., Valerius, M. T. and McMahon, A. P. (2007). Wnt/beta-catenin signaling regulates nephron induction during mouse kidney development. Development 134, 2533-2539.
41. Patel, V., Li, L., Cobo-Stark, P., Shao, X., Somlo, S., Lin, F. and Igarashi, P. (2008). Acute kidney injury and aberrant planar cell polarity induce cyst formation in mice lacking renal cilia. Hum. Mol. Genet. 17, 1578-1590.
42. Perez-Moreno, M., Davis, M. A., Wong, E., Pasolli, H. A., Reynolds, A. B. and Fuchs, E. (2006). p120-catenin mediates inflammatory responses in the skin. Cell 124, 631-644.
43. Perrais, M., Chen, X., Perez-Moreno, M. and Gumbiner, B. M. (2007). Ecadherin homophilic ligation inhibits cell growth and epidermal growth factor receptor signaling independently of other cell interactions. Mol. Biol. Cell 18, 2013-2025.
44. Price, S. R., De Marco Garcia, N. V., Ranscht, B. and Jessell, T. M. (2002). Regulation of motor neuron pool sorting by differential expression of type II cadherins. Cell 109, 205-216.
45. Reynolds, A. B. (2007). p120-catenin: past and present. Biochim. Biophys. Acta 1773, 2-7.
46. Saxen, L. and Sariola, H. (1987). Early organogenesis of the kidney. Pediatr. Nephrol. 1, 385-392.
47. Schmidt-Ott, K. M. and Barasch, J. (2008). WNT/beta-catenin signaling in nephron progenitors and their epithelial progeny. Kidney Int. 74, 1004-1008.
48. Smalley-Freed, W. G., Efimov, A., Burnett, P. E., Short, S. P., Davis, M. A., Gumucio, D. L., Washington, M. K., Coffey, R. J. and Reynolds, A. B. (2010). p120-catenin is essential for maintenance of barrier function and intestinal homeostasis in mice. J. Clin. Invest. 120, 1824-1835.
49. Soto, E., Yanagisawa, M., Marlow, L. A., Copland, J. A., Perez, E. A. and Anastasiadis, P. Z. (2008). p120 catenin induces opposing effects on tumor cell growth depending on E-cadherin expression. J. Cell Biol. 183, 737-749.
50. Srinivas, S., Goldberg, M. R., Watanabe, T., D'Agati, V., al-Awqati, Q. and Costantini, F. (1999). Expression of green fluorescent protein in the ureteric bud of transgenic mice: a new tool for the analysis of ureteric bud morphogenesis. Dev. Genet. 24, 241-251.
51. Usui, J., Kurihara, H., Shu, Y., Tomari, S., Kanemoto, K., Koyama, A., Sakai, T., Takahashi, T. and Nagata, M. (2003). Localization of intercellular adherens junction protein p120 catenin during podocyte differentiation. Anat. Embryol. (Berl.) 206, 175-184.
52. van Noort, M., Meeldijk, J., van der Zee, R., Destree, O. and Clevers, H. (2002). Wnt signaling controls the phosphorylation status of beta-catenin. J. Biol. Chem. 277, 17901-17905.
53. Walter, B., Schlechter, T., Hergt, M., Berger, I. and Hofmann, I. (2008). Differential expression pattern of protein ARVCF in nephron segments of human and mouse kidney. Histochem. Cell Biol. 130, 943-956.
54. Wildenberg, G. A., Dohn, M. R., Carnahan, R. H., Davis, M. A., Lobdell, N. A., Settleman, J. and Reynolds, A. B. (2006). p120-catenin and p190RhoGAP regulate cell-cell adhesion by coordinating antagonism between Rac and Rho. Cell 127, 1027-1039.
55. Xiao, K., Allison, D. F., Buckley, K. M., Kottke, M. D., Vincent, P. A., Faundez, V. and Kowalczyk, A. P. (2003). Cellular levels of p120 catenin function as a set point for cadherin expression levels in microvascular endothelial cells. J. Cell Biol. 163, 535-545.
56. Xiao, K., Garner, J., Buckley, K. M., Vincent, P. A., Chiasson, C. M., Dejana, E., Faundez, V. and Kowalczyk, A. P. (2005). p120-Catenin regulates clathrindependent endocytosis of VE-cadherin. Mol. Biol. Cell 16, 5141-5151.
57. Yanagisawa, M. and Anastasiadis, P. Z. (2006). p120 catenin is essential for mesenchymal cadherin-mediated regulation of cell motility and invasiveness. J. Cell Biol. 174, 1087-1096.
58. Yanagisawa, M., Huveldt, D., Kreinest, P., Lohse, C. M., Cheville, J. C., Parker, A. S., Copland, J. A. and Anastasiadis, P. Z. (2008). A p120 catenin isoform switch affects Rho activity, induces tumor cell invasion, and predicts metastatic disease. J. Biol. Chem. 283, 18344-18354.
59. Yu, J., Carroll, T. J. and McMahon, A. P. (2002). Sonic hedgehog regulates proliferation and differentiation of mesenchymal cells in the mouse metanephric kidney. Development 129, 5301-5312.