Non-canonical Wnt5a/Ror2 signaling regulates kidney morphogenesis by controlling intermediate

Human Molecular Genetics

Volumn 23, Issue 25, 2014, Pages 6807-6814

  Yun, Kangsun ^a   Ajima, Rieko ^a,b   Sharma, Nirmala ^a   Costantini, Frank ^c   Mackem, Susan ^a   Lewandoski, Mark ^a   Yamaguchi, Terry P ^a   Perantoni, Alan O ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b NewYork Presbyterian Hospital   (United States)

^c OSAKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CRE RECOMBINASE; MEMBRANE PROTEIN; PROTEIN ROR2; TRANSCRIPTION FACTOR PAX2; UNCLASSIFIED DRUG; WNT5A PROTEIN; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; INTEGRASE; PAX2 PROTEIN, MOUSE; RECEPTOR TYROSINE KINASE LIKE ORPHAN RECEPTOR; ROR2 PROTEIN, MOUSE; WNT PROTEIN; WNT5A PROTEIN, MOUSE;

ANIMAL TISSUE; ARTICLE; CONGENITAL ANOMALIES OF THE KIDNEY AND URINARY TRACT; DOWN REGULATION; EMBRYO; EMBRYO DEVELOPMENT; GDNF GENE; GENE; GENE DELETION; GENE EXPRESSION; GENE MUTATION; KIDNEY DEVELOPMENT; KIDNEY DUPLICATION; KIDNEY MALFORMATION; MESENCHYME; MESENCHYME CELL; MESODERM; MOUSE; NONHUMAN; PRIORITY JOURNAL; ROR2 GENE; SIGNAL TRANSDUCTION; URETER; URINARY TRACT MALFORMATION; WNT5A GENE; ANIMAL; DEFICIENCY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOMOZYGOTE; KIDNEY; MAMMALIAN EMBRYO; MESENCHYMAL STROMA CELL; METABOLISM; MORPHOGENESIS; PATHOLOGY; TIME FACTOR; TRANSGENIC MOUSE; WOLFFIAN DUCT;

MUS;

ANIMALS; EMBRYO, MAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR; HOMOZYGOTE; INTEGRASES; KIDNEY; MESENCHYMAL STROMAL CELLS; MESODERM; MICE; MICE, TRANSGENIC; MORPHOGENESIS; PAX2 TRANSCRIPTION FACTOR; RECEPTOR TYROSINE KINASE-LIKE ORPHAN RECEPTORS; SIGNAL TRANSDUCTION; TIME FACTORS; URETER; WNT PROTEINS; WOLFFIAN DUCTS;

EID: 84939158275     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddu397     Document Type: Article

References (36)

1. Kume, T., Deng, K. and Hogan, B.L. (2000) Murine forkhead/winged helix genes Foxc1 (Mf1) and Foxc2 (Mfh1) are required for the early organogenesis of the kidney and urinary tract. Development, 127, 1387-1395.
2. Whitten, S.M. and Wilcox, D.T. (2001) Duplex systems. Prenat. Diagn., 21, 952-957.
3. Obara-Ishihara, T., Kuhlman, J., Niswander, L. and Herzlinger, D. (1999) The surface ectoderm is essential for nephric duct formation in intermediate mesoderm. Development, 126, 1103-1108.
4. Dressler, G.R. (2009) Advances in early kidney specification, development and patterning. Development, 136, 3863-3874.
5. Costantini, F. (2012) Genetic controls and cellular behaviors in branching morphogenesis of the renal collecting system. Wiley Interdiscip. Rev. Dev. Biol., 1, 693-713.
6. Costantini, F. and Kopan, R. (2010) Patterning a complex organ: branching morphogenesis and nephron segmentation in kidney development. Dev. Cell, 18, 698-712.
7. Saburi, S., Hester, I., Fischer, E., Pontoglio, M., Eremina, V., Gessler, M., Quaggin, S.E., Harrison, R., Mount, R. and McNeill, H. (2008) Loss of Fat4 disrupts PCP signaling and oriented cell division and leads to cystic kidney disease. Nat. Genet., 40, 1010-1015.
8. Takeuchi, S., Takeda, K., Oishi, I., Nomi, M., Ikeya, M., Itoh, K., Tamura, S., Ueda, T., Hatta, T., Otani, H. et al. (2000) Mouse Ror2 receptor tyrosine kinase is required for the heart development and limb formation. Genes Cells, 5, 71-78.
9. Lyashenko, N., Weissenbock, M., Sharir, A., Erben, R.G., Minami, Y. and Hartmann, C. (2010) Mice lacking the orphan receptor ror1 have distinct skeletal abnormalities and are growth retarded. Dev. Dyn., 239, 2266-2277.
10. Kikuchi, A., Yamamoto, H., Sato, A. and Matsumoto, S. (2012) Wnt5a: its signalling, functions and implication in diseases. Acta Physiol. (Oxf.), 204, 17-33.
11. Yamaguchi, T.P., Bradley, A., McMahon, A.P. and Jones, S. (1999)AWnt5a pathway underlies outgrowth of multiple structures in the vertebrate embryo. Development, 126, 1211-1223.
12. Cha, K.B., Douglas, K.R., Potok, M.A., Liang, H., Jones, S.N. and Camper, S.A. (2004) WNT5A signaling affects pituitary gland shape. Mech. Dev., 121, 183-194.
13. Cervantes, S., Yamaguchi, T.P. and Hebrok, M.(2009)Wnt5ais essential for intestinal elongation in mice. Dev. Biol., 326, 285-294.
14. Qian, D., Jones, C., Rzadzinska, A., Mark, S., Zhang, X., Steel, K.P., Dai, X. and Chen, P. (2007) Wnt5a functions in planar cell polarity regulation in mice. Dev. Biol., 306, 121-133.
15. Sinha, T., Wang, B., Evans, S., Wynshaw-Boris, A. and Wang, J. (2012) Disheveled mediated planar cell polarity signaling is required in the second heart field lineage for outflow tract morphogenesis. Dev. Biol., 370, 135-144.
16. Oishi, I., Suzuki, H., Onishi, N., Takada, R., Kani, S., Ohkawara, B., Koshida, I., Suzuki, K., Yamada, G., Schwabe, G.C. et al. (2003) The receptor tyrosine kinase Ror2 is involved in non-canonical Wnt5a/JNK signalling pathway. Genes Cells, 8, 645-654.
17. Perantoni, A.O., Timofeeva, O., Naillat, F., Richman, C., Pajni-Underwood, S., Wilson, C., Vainio, S., Dove, L.F. and Lewandoski, M. (2005) Inactivation of FGF8 in early mesoderm reveals an essential role in kidney development. Development, 132, 3859-3871.
18. Grieshammer, U., Le, M., Plump, A.S., Wang, F., Tessier-Lavigne, M. and Martin, G.R. (2004) SLIT2-mediated ROBO2 signaling restricts kidney induction to a single site. Dev. Cell, 6, 709-717.
19. 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.
20. 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.
21. Anderson, M.J., Naiche, L.A., Wilson, C.P., Elder, C., Swing, D.A. and Lewandoski, M. (2013) TCreERT2, a transgenic mouse line for temporal control of Cre-mediated recombination in lineages emerging from the primitive streak or tail bud. PLoS ONE, 8, e62479.
22. van Amerongen, R., Fuerer, C., Mizutani, M. and Nusse, R. (2012) Wnt5a can both activate and repress Wnt/beta-catenin signaling during mouse embryonic development. Dev. Biol., 369, 101-114.
23. Najdi, R., Proffitt, K., Sprowl, S., Kaur, S., Yu, J., Covey, T.M., Virshup, D.M. and Waterman, M.L. (2012)Auniform human Wnt expression library reveals a shared secretory pathway and unique signaling activities. Differentiation, 84, 203-213.
24. Nakaya, M.A., Biris, K., Tsukiyama, T., Jaime, S., Rawls, J.A. and Yamaguchi, T.P. (2005) Wnt3a links left-right determination with segmentation and anteroposterior axis elongation. Development, 132, 5425-5436.
25. Afzal, A.R., Rajab, A., Fenske, C.D., Oldridge, M., Elanko, N., Ternes-Pereira, E., Tuysuz, B., Murday, V.A., Patton, M.A., Wilkie, A.O. et al. (2000) Recessive Robinow syndrome, allelic to dominant brachydactyly type B, is caused by mutation of ROR2. Nat. Genet., 25, 419-422.
26. Person, A.D., Beiraghi, S., Sieben, C.M., Hermanson, S., Neumann, A.N., Robu, M.E., Schleiffarth, J.R., Billington, C.J. Jr, van Bokhoven, H., Hoogeboom, J.M. et al. (2010) WNT5A mutations in patients with autosomal dominant Robinow syndrome. Dev. Dyn., 239, 327-337.
27. Patton, M.A. and Afzal, A.R. (2002) Robinow syndrome. J. Med. Genet., 39, 305-310.
28. Gao, B., Song, H., Bishop, K., Elliot, G., Garrett, L., English, M.A., Andre, P., Robinson, J., Sood, R., Minami, Y. et al. (2011) Wnt signaling gradients establish planar cell polarity by inducing Vangl2 phosphorylation through Ror2. Dev. Cell, 20, 163-176.
29. Gray, R.S., Roszko, I. and Solnica-Krezel, L. (2011) Planar cell polarity: coordinating morphogenetic cell behaviors with embryonic polarity. Dev. Cell, 21, 120-133.
30. Nishita, M., Qiao, S., Miyamoto, M., Okinaka, Y., Yamada, M., Hashimoto, R., Iijima, K., Otani, H., Hartmann, C., Nishinakamura, R. et al. (2014) Role of Wnt5a-Ror2 signaling in morphogenesis of the metanephric mesenchyme during ureteric budding. Mol. Cell. Biol, 34, 3096-3105.
31. Miyoshi, H., Ajima, R., Luo, C.T., Yamaguchi, T.P. and Stappenbeck, T.S. (2012) Wnt5a potentiates TGF-beta signaling to promote colonic crypt regeneration after tissue injury. Science, 338, 108-113.
32. Chi, X., Hadjantonakis, A.K., Wu, Z., Hyink, D. and Costantini, F. (2009)A transgenic mousethat reveals cell shape and arrangement during ureteric bud branching. Genesis, 47, 61-66.
33. Kitagaki, J., Ueda, Y., Chi, X., Sharma, N., Elder, C.M., Truffer, E., Costantini, F., Lewandoski, M. and Perantoni, A.O. (2011) FGF8is essential for formation of the ductal system in the male reproductive tract. Development, 138, 5369-5378.
34. Nguyen, M.T., Zhu, J., Nakamura, E., Bao, X. and Mackem, S. (2009) Tamoxifen-dependent, inducible Hoxb6CreERT recombinase function in lateral plate and limb mesoderm, CNS isthmic organizer, posterior trunk neural crest, hindgut, and tailbud. Dev. Dyn., 238, 467-474.
35. Wang, H., Yang, Y., Sharma, N., Tarasova, N.I., Timofeeva, O.A., Winkler-Pickett, R.T., Tanigawa, S. and Perantoni, A.O. (2010) STAT1 activation regulates proliferation and differentiation of renal progenitors. Cell. Signal., 22, 1717-1726.
36. Yun, K., Choi, Y.D., Nam, J.H., Park, Z. and Im, S.H. (2007) NF-kappaB regulates Lef1 gene expression in chondrocytes. Biochem. Biophys. Res. Commun., 357, 589-595.