Role of Wnt5a-Ror2 signaling in morphogenesis of the metanephric mesenchyme during ureteric budding

Molecular and Cellular Biology

Volumn 34, Issue 16, 2014, Pages 3096-3105

  Nishita, Michiru ^a   Qiao, Sen ^a   Miyamoto, Mari ^a   Okinaka, Yuka ^a   Yamada, Makiko ^b   Hashimoto, Ryuju ^b   Iijima, Kazumoto ^a   Otani, Hiroki ^b   Hartmann, Christine ^c   Nishinakamura, Ryuichi ^d   Minamia, Yasuhiro ^a  

^a KOBE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b SHIMANE UNIVERSITY   (Japan)

^c UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^d KUMAMOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; PROTEIN ROR2; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG; WNT5A PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRANCHING MORPHOGENESIS; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; EMBRYONIC STRUCTURES; GLOMERULUS; HYDRONEPHROSIS; HYDROURETER; KIDNEY DEVELOPMENT; MESENCHYME; MOUSE; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; URETER; URETERIC BUDDING; WILD TYPE; WNT SIGNALING PATHWAY;

ANIMALS; CELL PROLIFERATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR; KIDNEY; MICE; MICE, INBRED ICR; MICE, KNOCKOUT; MORPHOGENESIS; ORGAN CULTURE TECHNIQUES; ORGANOGENESIS; RECEPTOR TYROSINE KINASE-LIKE ORPHAN RECEPTORS; URETER; WNT PROTEINS; WNT SIGNALING PATHWAY; WOLFFIAN DUCTS;

EID: 84904497809     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00491-14     Document Type: Article

References (56)

1. Oishi I, Suzuki H, Onishi N, Takada R, Kani S, Ohkawara B, Koshida I, Suzuki K, Yamada G, Schwabe GC, Mundlos S, Shibuya H, Takada S, Minami Y. 2003. The receptor tyrosine kinase Ror2 is involved in noncanonical Wnt5a/JNK signalling pathway. Genes Cells 8:645-654. http://dx.doi.org/10.1046/j.1365-2443.2003.00662.x.
2. Mikels AJ, Nusse R. 2006. Purified Wnt5a protein activates or inhibits beta-catenin-TCF signaling depending on receptor context. PLoS Biol. 4:e115. http://dx.doi.org/10.1371/journal.pbio.0040115.
3. Nishita M, Enomoto M, Yamagata K, Minami Y. 2010. Cell/tissuetropic functions of Wnt5a signaling in normal and cancer cells. Trends Cell Biol. 20:346-354. http://dx.doi.org/10.1016/j.tcb.2010.03.001.
4. Nishita M, Itsukushima S, Nomachi A, Endo M, Wang Z, Inaba D, Qiao S, Takada S, Kikuchi A, Minami Y. 2010. Ror2/Frizzled complex mediates Wnt5a-induced AP-1 activation by regulating Dishevelled polymerization. Mol. Cell. Biol. 30:3610-3619. http://dx.doi.org/10.1128/MCB.00177-10.
5. Nishita M, Yoo SK, Nomachi A, Kani S, Sougawa N, Ohta Y, Takada S, Kikuchi A, Minami Y. 2006. Filopodia formation mediated by receptor tyrosine kinase Ror2 is required for Wnt5a-induced cell migration. J. Cell Biol. 175:555-562. http://dx.doi.org/10.1083/jcb.200607127.
6. Schambony A, Wedlich D. 2007. Wnt-5A/Ror2 regulate expression of XPAPC through an alternative noncanonical signaling pathway. Dev. Cell 12:779-792. http://dx.doi.org/10.1016/j.devcel.2007.02.016.
7. Nomachi A, Nishita M, Inaba D, Enomoto M, Hamasaki M, Minami Y. 2008. Receptor tyrosine kinase Ror2 mediates Wnt5a-induced polarized cell migration by activating c-Jun N-terminal kinase via actin-binding protein Filamin A. J. Biol. Chem. 283:27973-27981. http://dx.doi.org/10.1074/jbc. M802325200.
8. He F, Xiong W, Yu X, Espinoza-Lewis R, Liu C, Gu S, Nishita M, Suzuki K, Yamada G, Minami Y, Chen Y. 2008. Wnt5a regulates directional cell migration and cell proliferation via Ror2-mediated noncanonical pathway in mammalian palate development. Development 135:3871-3879. http://dx.doi.org/10.1242/dev.025767.
9. Laird DJ, Altshuler-Keylin S, Kissner MD, Zhou X, Anderson KV. 2011. Ror2 enhances polarity and directional migration of primordial germ cells. PLoS Genet. 7:e1002428. http://dx.doi.org/10.1371/journal.pgen.1002428.
10. Gao B, Song H, Bishop K, Elliot G, Garrett L, English MA, Andre P, Robinson J, Sood R, Minami Y, Economides AN, Yang Y. 2011. Wnt signaling gradients establish planar cell polarity by inducing Vangl2 phosphorylation through Ror2. Dev. Cell 20:163-176. http://dx.doi.org/10.1016/j.devcel.2011.01.001.
11. O'Connell MP, Fiori JL, Xu M, Carter AD, Frank BP, Camilli TC, French AD, Dissanayake SK, Indig FE, Bernier M, Taub DD, Hewitt SM, Weeraratna AT. 2010. The orphan tyrosine kinase receptor, ROR2, mediates Wnt5A signaling in metastatic melanoma. Oncogene 29:34-44. http://dx.doi.org/10.1038/onc.2009.305.
12. Endo M, Doi R, Nishita M, Minami Y. 2012. Ror family receptor tyrosine kinases regulate the maintenance of neural progenitor cells in the developing neocortex. J. Cell Sci. 125:2017-2029. http://dx.doi.org/10.1242/jcs.097782.
13. Al-Shawi R, Ashton SV, Underwood C, Simons JP. 2001. Expression of the Ror1 and Ror2 receptor tyrosine kinase genes during mouse development. Dev. Genes Evol. 211:161-171. http://dx.doi.org/10.1007/s004270100140.
14. Matsuda T, Nomi M, Ikeya M, Kani S, Oishi I, Terashima T, Takada S, Minami Y. 2001. Expression of the receptor tyrosine kinase genes, Ror1 and Ror2, during mouse development. Mech. Dev. 105:153-156. http://dx.doi.org/10.1016/S0925-4773(01)00383-5.
15. Yamaguchi TP, Bradley A, McMahon AP, Jones S. 1999. A Wnt5a pathway underlies outgrowth of multiple structures in the vertebrate embryo. Development 126:1211-1223.
16. DeChiara TM, Kimble RB, Poueymirou WT, Rojas J, Masiakowski P, Valenzuela DM, Yancopoulos GD. 2000. Ror2, encoding a receptor-like tyrosine kinase, is required for cartilage and growth plate development. Nat. Genet. 24:271-274. http://dx.doi.org/10.1038/73488.
17. Minami Y, Oishi I, Endo M, Nishita M. 2010. Ror-family receptor tyrosine kinases in noncanonical Wnt signaling: Their implications in developmental morphogenesis and human diseases. Dev. Dyn. 239:1-15. http://dx.doi.org/10.1002/dvdy.21991.
18. Takeuchi S, Takeda K, Oishi I, Nomi M, Ikeya M, Itoh K, Tamura S, Ueda T, Hatta T, Otani H, Terashima T, Takada S, Yamamura H, Akira S, Minami Y. 2000. Mouse Ror2 receptor tyrosine kinase is required for the heart development and limb formation. Genes Cells 5:71-78. http://dx.doi.org/10.1046/j.1365-2443.2000.00300.x.
19. Afzal AR, Rajab A, Fenske CD, Oldridge M, Elanko N, Ternes-Pereira E, Tuysuz B, Murday VA, Patton MA, Wilkie AO, Jeffery S. 2000. Recessive Robinow syndrome, allelic to dominant brachydactyly type B, is caused by mutation of ROR2. Nat. Genet. 25:419-422. http://dx.doi.org/10.1038/78107.
20. van Bokhoven H, Celli J, Kayserili H, van Beusekom E, Balci S, Brussel W, Skovby F, Kerr B, Percin EF, Akarsu N, Brunner HG. 2000. Mutation of the gene encoding the ROR2 tyrosine kinase causes autosomal recessive Robinow syndrome. Nat. Genet. 25:423-426. http://dx.doi.org/10.1038/78113.
21. Soliman AT, Rajab A, Alsalmi I, Bedair SM. 1998. Recessive Robinow syndrome: with emphasis on endocrine functions. Metabolism 47:1337-1343. http://dx.doi.org/10.1016/S0026-0495(98)90301-8.
22. Tufan F, Cefle K, Turkmen S, Turkmen A, Zorba U, Dursun M, Ozturk S, Palanduz S, Ecder T, Mundlos S, Horn D. 2005. Clinical and molecular characterization of two adults with autosomal recessive Robinow syndrome. Am. J. Med. Genet. A 136:185-189. http://dx.doi.org/10.1002/ajmg.a.30785.
23. Saxen L. 1987. Organogenesis of the kidney. Cambridge University Press, Cambridge, United Kingdom.
24. Pope JC, IV, Brock JW, III, Adams MC, Stephens FD, Ichikawa I. 1999. How they begin and how they end: classic and new theories for the development and deterioration of congenital anomalies of the kidney and urinary tract, CAKUT. J. Am. Soc. Nephrol. 10:2018-2028.
25. Song R, Yosypiv IV. 2012. Development of the kidney medulla. Organogenesis 8:10-17. http://dx.doi.org/10.4161/org.19308.
26. Cacalano G, Farinas I, Wang LC, Hagler K, Forgie A, Moore M, Armanini M, Phillips H, Ryan AM, Reichardt LF, Hynes M, Davies A, Rosenthal A. 1998. GFRalpha1 is an essential receptor component for GDNF in the developing nervous system and kidney. Neuron 21:53-62. http://dx.doi.org/10.1016/S0896-6273(00)80514-0.
27. Enomoto H, Araki T, Jackman A, Heuckeroth RO, Snider WD, Johnson EM, Jr, Milbrandt J. 1998. GFR alpha1-deficient mice have deficits in the enteric nervous system and kidneys. Neuron 21:317-324. http://dx.doi.org/10.1016/S0896-6273(00)80541-3.
28. Moore MW, Klein RD, Farinas I, Sauer H, Armanini M, Phillips H, Reichardt LF, Ryan AM, Carver-Moore K, Rosenthal A. 1996. Renal and neuronal abnormalities in mice lacking GDNF. Nature 382:76-79. http://dx.doi.org/10.1038/382076a0.
29. Pichel JG, Shen L, Sheng HZ, Granholm AC, Drago J, Grinberg A, Lee EJ, Huang SP, Saarma M, Hoffer BJ, Sariola H, Westphal H. 1996. Defects in enteric innervation and kidney development in mice lacking GDNF. Nature 382:73-76. http://dx.doi.org/10.1038/382073a0.
30. Sanchez MP, Silos-Santiago I, Frisen J, He B, Lira SA, Barbacid M. 1996. Renal agenesis and the absence of enteric neurons in mice lacking GDNF. Nature 382:70-73. http://dx.doi.org/10.1038/382070a0.
31. Schuchardt A, D'Agati V, Larsson-Blomberg L, Costantini F, Pachnis V. 1994. Defects in the kidney and enteric nervous system of mice lacking the tyrosine kinase receptor Ret. Nature 367:380-383. http://dx.doi.org/10.1038/367380a0.
32. Grieshammer U, Le M, Plump AS, Wang F, Tessier-Lavigne M, Martin GR. 2004. SLIT2-mediated ROBO2 signaling restricts kidney induction to a single site. Dev. Cell 6:709-717. http://dx.doi.org/10.1016/S1534-5807(04)00108-X.
33. Kume T, Deng K, Hogan BL. 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.
34. Basson MA, Akbulut S, Watson-Johnson J, Simon R, Carroll TJ, Shakya R, Gross I, Martin GR, Lufkin T, McMahon AP, Wilson PD, Costantini FD, Mason IJ, Licht JD. 2005. Sprouty1 is a critical regulator of GDNF/RET-mediated kidney induction. Dev. Cell 8:229-239. http://dx.doi.org/10.1016/j.devcel.2004.12.004.
35. Srinivas S, Goldberg MR, Watanabe T, D'Agati V, al-Awqati Q, 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.
36. Kani S, Oishi I, Yamamoto H, Yoda A, Suzuki H, Nomachi A, Iozumi K, Nishita M, Kikuchi A, Takumi T, Minami Y. 2004. The receptor tyrosine kinase Ror2 associates with and is activated by casein kinase Iepsilon. J. Biol. Chem. 279:50102-50109. http://dx.doi.org/10.1074/jbc. M409039200.
37. Hoshi M, Batourina E, Mendelsohn C, Jain S. 2012. Novel mechanisms of early upper and lower urinary tract patterning regulated by RetY1015 docking tyrosine in mice. Development 139:2405-2415. http://dx.doi.org/10.1242/dev.078667.
38. Yamada M, Udagawa J, Matsumoto A, Hashimoto R, Hatta T, Nishita M, Minami Y, Otani H. 2010. Ror2 is required for midgut elongation during mouse development. Dev. Dyn. 239:941-953. http://dx.doi.org/10.1002/dvdy.22212.
39. Nishinakamura R, Matsumoto Y, Nakao K, Nakamura K, Sato A, Copeland NG, Gilbert DJ, Jenkins NA, Scully S, Lacey DL, Katsuki M, Asashima M, Yokota T. 2001. Murine homolog of SALL1 is essential for ureteric bud invasion in kidney development. Development 128:3105-3115.
40. Ren D, Minami Y, Nishita M. 2011. Critical role of Wnt5a-Ror2 signaling in motility and invasiveness of carcinoma cells following Snail-mediated epithelial-mesenchymal transition. Genes Cells 16:304-315. http://dx.doi.org/10.1111/j.1365-2443.2011.01487.x.
41. Jahan E, Matsumoto A, Udagawa J, Rafiq AM, Hashimoto R, Rahman OI, Habib H, Sekine J, Otani H. 2010. Effects of restriction of fetal jaw movement on prenatal development of the temporalis muscle. Arch. Oral Biol. 55:919-927. http://dx.doi.org/10.1016/j.archoralbio.2010.07.010.
42. Georgas KM, Chiu HS, Lesieur E, Rumballe BA, Little MH. 2011. Expression of metanephric nephron-patterning genes in differentiating mesonephric tubules. Dev. Dyn. 240:1600-1612. http://dx.doi.org/10.1002/dvdy.22640.
43. Mackie GG, Stephens FD. 1975. Duplex kidneys: a correlation of renal dysplasia with position of the ureteral orifice. J. Urol. 114:274-280.
44. Batourina E, Choi C, Paragas N, Bello N, Hensle T, Costantini FD, Schuchardt A, Bacallao RL, Mendelsohn CL. 2002. Distal ureter morphogenesis depends on epithelial cell remodeling mediated by vitamin A and Ret. Nat. Genet. 32:109-115. http://dx.doi.org/10.1038/ng952.
45. Kaku Y, Ohmori T, Kudo K, Fujimura S, Suzuki K, Evans SM, Kawakami Y, Nishinakamura R. 2013. Islet1 deletion causes kidney agenesis and hydroureter resembling CAKUT. J. Am. Soc. Nephrol. 24:1242-1249. http://dx.doi.org/10.1681/ASN.2012050528.
46. Gotoh H, Masuzaki H, Taguri H, Yoshimura S, Ishimaru T. 1998. Effect of experimentally induced urethral obstruction and surgical decompression in utero on renal development and function in rabbits. Early Hum. Dev. 52:111-123. http://dx.doi.org/10.1016/S0378-3782(98)00020-6.
47. McVary KT, Maizels M. 1989. Urinary obstruction reduces glomerulogenesis in the developing kidney: a model in the rabbit. J. Urol. 142:646-651, 667-668.
48. Temelcos C, Hutson JM. 2004. Ontogeny of the VATER kidney in a rat model. Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 278:520-527. http://dx.doi.org/10.1002/ar.a.20030.
49. Whitten SM, Wilcox DT. 2001. Duplex systems. Prenat. Diagn. 21:952-957. http://dx.doi.org/10.1002/pd.206.
50. Fisher CE, Michael L, Barnett MW, Davies JA. 2001. Erk MAP kinase regulates branching morphogenesis in the developing mouse kidney. Development 128:4329-4338.
51. Watanabe T, Costantini F. 2004. Real-time analysis of ureteric bud branching morphogenesis in vitro. Dev. Biol. 271:98-108. http://dx.doi.org/10.1016/j.ydbio.2004.03.025.
52. Majumdar A, Vainio S, Kispert A, McMahon J, McMahon AP. 2003. Wnt11 and Ret/Gdnf pathways cooperate in regulating ureteric branching during metanephric kidney development. Development 130:3175-3185. http://dx.doi.org/10.1242/dev.00520.
53. Mugford JW, Sipila P, Kobayashi A, Behringer RR, McMahon AP. 2008. Hoxd11 specifies a program of metanephric kidney development within the intermediate mesoderm of the mouse embryo. Dev. Biol. 319: 396-405. http://dx.doi.org/10.1016/j.ydbio.2008.03.044.
54. Carroll TJ, Park JS, Hayashi S, Majumdar A, McMahon AP. 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. http://dx.doi.org/10.1016/j.devcel.2005.05.016.
55. Taguchi A, Kaku Y, Ohmori T, Sharmin S, Ogawa M, Sasaki H, Nishinakamura R. 2014. Redefining the in vivo origin of metanephric nephron progenitors enables generation of complex kidney structures from pluripotent stem cells. Cell Stem Cell 14:53-67. http://dx.doi.org/10.1016/j.stem.2013.11.010.
56. Wellik DM, Hawkes PJ, Capecchi MR. 2002. Hox11 paralogous genes are essential for metanephric kidney induction. Genes Dev. 16:1423-1432. http://dx.doi.org/10.1101/gad.993302.